Recognition for emotionally arousing odors: A neuropsychological investigation

Sandra Pouliot Department of McGill University

Montreal, Quebec Canada

A thesis submitted to McGill University in partial fulfillment of the requirements of the degree of Doctorate of Philosophy

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Table of Content

Abstract VI Resume VIII Statement of Originality X Contribution of co-authors and other colleagues XII Acknowledgments XIV CHAPTER 1. INTRODUCTION 2 CHAPTER 2. LITERATURE REVIEW 6 1. EMOTIONAL AND 7 : Working Definitions 8 Memory 8 Emotions 9 Beneficial Effect of Emotions on Memory 11 Effect of Mood 11 Mood-State Dependent Memory 12 Mood Congruent Memory 13 Effect of Valence 14 Pleasantness Superiority 14 Unpleasantness Superiority 15 Effect of Arousal 15 Physiological Arousal 16 Stimuli with Arousing Properties 16 20 Interfering Effect of Emotions on Memory and Other Specific Effects..' 21 Effect of Mood 21 Age 21 Effect of Arousal 22 Intrusion Errors 22 Periphery versus Central Component of Stimuli 22 Paradigms 24 Retrieval Paradigms 25 Retention Interval 26 Personality 27 Cognitive Mechanisms Underlying the Effects of Emotional Arousal on Memory... 28 Emotions Guide Encoding and Retrieval 28 Some Theories '. 30 The Beginnings: Yerkes-Dodson, Walker, and Easterbrook 30 Cognitive Organization: Schemas 32 "Tick-Rate" Hypothesis 33 Levels of Processing Theory 34 Alternative Explanations 37 Event Distinctiveness 37 Differential Distribution of 37 Semantic Relatedness 38 Greater Rehearsal and Elaboration 38 Conclusion 41 Ill

2. NEUROBIOLOGICAL SUBSTRATES OF EMOTIONAL AROUSAL'S EFFECTS ON MEMORY 42 Emotional Memory in Nonhuman Animals 42 43 Epinephrine and Norepinephrine 44 Cholinergic Influences 46 Glucocorticoids 47 Interaction of the Basolateral Amygdala with other Brain Structures 48 Reconsolidation 50 Emotional Memory in Humans 51 Adrenergic Influences 52 Glucocorticoids 55 Amygdala and Emotional Memory 57 Bilateral Amygdala Lesion and Declarative Emotional Memory 58 Unilateral Amygdala Lesions and Emotional Memory 60 Brain Imaging Studies in Healthy Subjects 65 Encoding of Emotional Memory 65 Gender Differences in Encoding of Emotional Memory 69 Retrieval of Emotional Memory 70 Conclusion 73 3. ODOR MEMORY, AFFECTIVE INFLUENCES AND ITS NEUROANATOMICAL SUBSTRATES 75 Memory Systems and Olfactory Information 76 Odors and Nondeclarative Memory 77 Odors and 77 Odor and the Perceptual Representation System 80 Odors and Declarative Memory 80 Odors and 81 Hedonic value of odors 81 Odor identification 81 Odors and Episodic Memory 83 Odors and Short-Term Memory 85 Declarative Odor Memory and Affective Influences. 87 Odor-Cued Memory: Paired-Associate Learning 88 Odors as Cues to Autobiographic Events 89 Some Explanations for the "Proust effect" 91 Neuroanatomical Substrates of Odor Hedonics and Odor Memory 94 Anatomical Overview of the Olfactory System 95 Affective Dimensions of Olfaction 97 Lesion Studies 98 Studies 99 Odor Memory 101 Lesion Studies 101 Neuroimaging Studies 103 Conclusion 105 CHAPTER 3. PRELIMINARY STUDY 106 Introduction 107 IV

1. Assemble Odorants 109 2. Rating of Odorants with SAM*SMELL 109 3. Correlations between SAM*SMELL dimensions 112 4. Selection of Odorants for Odor Memory Tests 116 Conclusion 116 CHAPTER 4. STUDY 1 119 Abstract 120 Introduction 121 Experiment 1 123 Method 123 Results 128 Experiment 2 136 Method 137 Results 137 General Discussion 141 Connection with Study 2 153 CHAPTER 5. STUDY 2 154 Abstract 155 Introduction 156 Method 158 Results 167 Discussion 178 Connection with Study 3 186 CHAPTER 6. STUDY 3 187 Abstract 188 Introduction 189 Experiment 1 196 Method 196 Results 200 Experiment 2 202 Method 202 Results 206 General Discussion 210 CHAPTER 7. CONCLUSION 218 Alternative Explanations: General 220 Event Distinctiveness 221 Differential Distribution of Attention 222 Semantic Relatedness 223 Greater Rehearsal and Elaboration 224 Alternative Explanations: Specific to Olfaction 225 Intensity vs Arousal 225 Pleasantness vs Arousal 226 Familiarity vs Arousal 227 Odor Memory and MTLR Patients 228 Future Directions 230 REFERENCES 231 APPENDICES 281 V

Appendix A 282 Appendix B 287 Appendix C 288 Appendix D .289 Appendix E 292 Appendix F 293 Appendix G 295 Memory Discrimination and Response Bias Indices 297 Permissions and Copyrights 298 Ethics Certificate ' 302 VI

Abstract

The aim of this dissertation was to investigate if and how emotional arousal influences odor memory. I conducted three studies, one of which involved patients with resection from the medial temporal lobe including the amygdala (MTLR). In the first experiment of Study 1, participants showed better memory for odors rated as being more emotionally arousing than for odors rated as less arousing. Skin conductance was also greater for the odors rated as more arousing. In the second experiment of Study 1,1 did not replicate the arousal finding, but odors rated as being unpleasant and intense were remembered better than odors rated as pleasant and weak. In Study 2,1 found a specific odor memory impairment in MTLR patients. Like healthy individuals, MTLR patients remembered unpleasant odors better than pleasant ones. However, unlike healthy individuals, they did not remember emotionally arousing odors better than nonarousing ones. In Study 3,1 found that incidental learning and a long retention interval may not be necessary for emotional arousal to enhance odor memory. Also, depending on odor pleasantness, emotional arousal may enhance memory through different processes. For arousing unpleasant odors, consolidation processes may be more involved, whereas for arousing pleasant odors, attentional influences may be more important. Based on these findings, I conclude that the enhancement of memory by emotional arousal is not modality specific and extends to odorants, but that this effect may be relatively difficult to observe. Also, the results of Study 2 suggest that the amygdala might play a pivotal role in enhancing memory for emotionally arousing odors, like it does for other types of sensory information. Finally, with odorants the memory enhancing effect of arousal may differ importantly as a function of odor pleasantness, making the modulation of VII attentional and consolidation processes by emotional arousal not alternative, but complementary hypotheses. VIII

Resume

Cette dissertation avait pour objectif d'etudier si, de quelle maniere, l'eveil emotionnel influence la memoire olfactive. J'ai effectue trois etudes, dont une impliquant des patients ayant subi une resection du lobe temporal median incluant l'amygdale (MTLR). Dans la premiere experience de l'Etude 1, la reconnaissance des odeurs plus emotionnellement eveillantes a ete superieure a celle des odeurs moins eveillantes. Aussi, la reponse electrodermale etait plus elevee pour les odeurs plus eveillantes. Dans la deuxieme experience de l'Etude 1, je n'ai pas reproduit l'effet de l'eveil emotionnel, mais les odeurs desagreables et intenses ont ete mieux memorisees que les odeurs agreables et faibles. Dans l'Etude 2, j'ai trouve que les patients MTLR avaient un trouble de memoire olfactive specifique. Comme les participants sains, les patients MTLR ont demontre une memoire superieure des odeurs desagreables comparativement aux odeurs agreables. Toutefois, contrairement aux participants sains, ils n'ont pas montre d'avantage mnesique pour les odeurs plus emotionnellement eveillantes comparativement aux odeurs moins eveillantes. Dans l'Etude 3, j'ai trouve que l'apprentissage incident et qu'un long delai de retention ne sont pas necessaires pour que l'eveil emotionnel ameliore la memoire olfactive. De plus, selon le niveau d'agrement des odeurs, l'eveil emotionnel pourrait ameliorer la memoire selon des processus differents. Pour les odeurs eveillantes desagreables, la consolidation serait plus impliquee, alors que pour les odeurs eveillantes agreables, Finfluence de l'attention serait plus importante. A la suite de ces resultats, je suggere que 1'amelioration de la memoire par l'eveil emotionnel n'est pas specifique a une modalite sensorielle et s'applique aussi aux odeurs, mais que cet effet pourrait etre difficile a observer. De plus, les resultats de l'Etude 2 suggerent que l'amygdale pourrait jouer un role central dans 1'amelioration de la memoire des odeurs emotionnellement eveillantes, comme elle le fait pour l'information provenant d'autres modalites sensorielles. Finalement, en olfaction, l'effet ameliorateur de l'eveil emotionnel sur la memoire pourrait differer de maniere importante selon le niveau d'agrement de l'odeur. Ainsi, en olfaction, les propositions de modulation des mecanismes attentionnels ou des mecanismes de consolidation par l'eveil emotionnel ne sont pas des hypotheses alternatives, mais complementaires. X

Statement of Originality

In this doctoral dissertation, I present three original manuscripts investigating the influence of emotional arousal on odor memory. These manuscripts have been submitted to peer-reviewed journals.

The experiments reported in Study 1 represent the first attempt at measuring whether emotional arousal enhances odor memory as it does with words, pictures and stories (Christianson, 1992). I adapted SAM (Hodes, Cook, & Lang, 1985; Lang, 1980), a well known rating scale in emotion research, to create a new scale for odorants. I named this scale SAM* SMELL and I used it to select the odorants used in Study 1, and in the other experiments of this dissertation.

In Study 2,1 investigated whether the memory of patients with unilateral resection from the medial temporal lobe including the amygdala benefit from emotionally arousing qualities of odors. Other teams have shown that patients with bilateral lesions (e.g., Cahill, Babinsky, Markowitsch, & McGaugh, 1995) or unilateral resection (e.g., LaBar & Phelps, 1998) of the amygdala did not remember emotionally arousing words better than neutral words. I was the first to provide evidence that both amygdalae are necessary for emotional arousal to enhance odor memory.

In Study 3,1 tested whether incidental encoding and delayed memory tests are necessary for emotional arousal to enhance odor memory. I found that they were not. In nonolfactory sensory modalities, whether emotional arousal influences memory through modulation of attentional or consolidation processes is currently debated (Hamann,

2001; Sharot& Phelps, 2004). I found evidence indicating that depending on the pleasantness of the odor, emotional arousal would enhance memory through different processes. For arousing unpleasant odors, consolidation processes may be more involved, whereas for arousing pleasant odors, attentional influences may be more important. In olfaction, modulation of attentional and of consolidation processes by emotional arousal to influence memory are not alternative hypotheses, they are complementary. XII

Contribution of co-authors and other colleagues

I designed and conducted all the experiments reported in this dissertation. I also analyzed all the data and wrote each manuscript. However this work would have been impossible without the important contribution of many dedicated individuals:

1. Marilyn Jones-Gotman, my supervisor guided me through all the steps of this dissertation. She also read and provided constructive feedback to all manuscripts and other parts of this thesis. Her vast knowledge and constant quest for excellence and precision brought significant improvement to all my ideas and to all my experimental and written efforts.

2. Rhonda Amsel and Daniel Levitin are members of my committee. They provided me with useful statistical advice regarding the analysis of all experiments of this thesis.

3. Julie Hudry was a postdoctoral student in our laboratory at the MNI. She helped me to develop and conduct the experiments in Study 1. Her influence was especially important in the design of SAM* SMELL. She helped me in the preparation and selection of the odorants for preliminary and memory testing.

4. Joelle Crane was a post-doctoral student in Dr. 's laboratory. She provided me with invaluable advice in the selection and testing of patients with resection in the medial temporal lobe. She showed me almost everything I know about brain segmentation. Her help was indispensable when I was making volumetric measurements of the amygdala. She made all the hippocampus measurements in Study 2.

5. Sidonie Penicaud was a biology undergraduate student who did an independent study under my supervision. She tested many of the healthy participants in Study 2.

6. Laura McKeeman was a psychology undergraduate student and became a research

assistant. She tested most of the participants in Experiment 1 of Study 3. 7. Moustafa Bensafi was a post-doctoral student I had the opportunity to work with during a research internship in the Berkeley Olfactory Research Project. He generously shared his time and knowledge while I was there. The work we did and the discussions we had together directly influenced all the experiments reported here. XIV

Acknowledgments

I am indebted to many individuals who helped and supported me during this incredible academic adventure. I could never express enough gratitude to:

- Marilyn: Thank you Marilyn for believing in me, and for all the resources and extraordinary opportunities you gave me. I am grateful for the incalculable amount of energy you invested to make me a better researcher.

- Joelle Crane: Thank you for the pep talks and for your invaluable help, for the hippocampi, for the space and the computer I so often monopolized in your office!

- Dr. Brenda Milner: I will never forget your wit. Neither will I forget your kindness when I stole your chair in Joelle's office! You are an inspiration.

- Julie Hudry: Travailler avec toi a ete un reel plaisir, en plus tu m'as appris enormement.

- To all the MJG Lab members and MNI staff (Julie B., Julie H., Jelena, Krista, Dylan, Sidonie, Laura, Johan, Johannes, Leticia, Denise Klein, Annie and Line) that make the MNI a motivating and pleasant place to be.

- To all the patients (and other participants) who so willingly agreed to participate in my lengthy and not uniquely pleasant experiments...

- Rhonda Amsel and Daniel Levitin: I deeply appreciated your encouragements and help.

- A Sylvain Gagnon: Merci, tu m'as donne la meilleure introduction possible au fascinant monde de la psychologie et de la recherche. Merci d'avoir su me dire les bons mots quand il le fallait! Ma reconnaissance etait, est et sera infinie.

- To all my friends, especially each enthusiastic member of Asian Dragon and of Eye Catch; my mental health was between your hands (along with your paddle)!!!

- A ma famille: Merci maman, merci papa d'avoir cru en moi si fort et de toujours avoir ete la pour moi. Surtout quand je devais me plaindre ! Merci de m'avoir inculque la valeur du travail bien fait. Merci Barbara d'etre la meilleure soeur et copine au monde. Je vous aime!

- A Nicolas, mon chocolat

- The FCAR and the Savoy Foundation for giving me financial support. #

CHAPTER 1. INTRODUCTION 2

Introduction

There is a strong belief in the general population that the association existing between smell, emotion and memory is special and powerful. This association would be unique because smells are believed to help retrieve that are older, richer and more emotional than memories cued by any other type of sensory information. The power of this association has been explored not only by writers (e.g., Marcel Proust), but also by a number of experimental (e.g., Chu, Herz, Rubin).

Experimental enquiries revealed that odors are effective memory cues (Aggleton

& Waskett, 1999), that odors help retrieve personal experiences from the past (Chu &

Downes, 2000a, 2000b, 2002), and that they help retrieve memories that are more emotional, but not more accurate, than those cued by other types of sensory information

(Herz, 1996, 2004; Herz & Schooler, 2002). Many explanations for these effects have been proposed, such as mood-congruent effects (Bower, 1981), the encoding specificity hypothesis (Tulving & Thompson, 1973), the "differential cue affordance value" hypothesis (Chu & Downes, 2000b, 2002), the unique neuroanatomy of the olfactory system (Aggleton & Waskett, 1999; Chu & Downes, 2000b; Herz, 1997) and the arousing dimension of odors (Aggleton & Waskett, 1999; Herz, 1997).

The proposition that odors are good memory cues because they are especially emotionally arousing, or that emotionally arousing odors are well remembered, has never been investigated. This gap in research is stunning given that the relationship between episodic memory and emotional arousal has given rise, and still does, to a vast number of studies (for a review: Christianson, 1992). Thus, the aim of this doctoral dissertation was to investigate if and how emotional arousal influences odor memory. 3

In the preliminary study (Chapter 3), subjects were presented with a large number of odorants (130) and had to rate each one on various dimensions (intensity, pleasantness, familiarity and arousal) with an adaptation of the SAM scale (Bradley,

Greenwald, Petry, & Lang, 1992; Hodes, Cook, & Lang, 1985; Lang, 1980). This study was carried out to choose the odorants that would be used as memory targets in the subsequent studies of this dissertation and to test the efficiency of our odorant-adapted

SAM scale, the SAM*SMELL scale.

In the first study (Chapter 4), I conducted two experiments in which I assessed subjects' emotional reactions (with a rating scale and skin conductance) when they smelled different odors, and related these measures to their odor memory tested a week later through recognition.

In the second study (Chapter 5), I investigated whether patients who had undergone a unilateral surgical resection from the medial temporal lobe, including the amygdala, remembered emotionally arousing odors the same way healthy subjects did.

This question seemed especially relevant because, unlike healthy subjects, patients with bilateral (Adolphs, Cahill, Schul, & Babinsky, 1997; Cahill, Babinsky, Markowitsch, &

McGaugh, 1995; Markowitsch et al., 1994; Phelps et al., 1998) or unilateral (Adolphs,

Tranel, & Denburg, 2000; Brierley, Medford, Shaw, & David, 2004; Buchanan,

Denburg, Tranel, & Adolphs, 2001; Frank & Tomaz, 2003; LaBar & Phelps, 1998) amygdala lesions do not show memory enhancement for emotionally arousing stimuli in other modalities. Moreover, to understand better the role of the medial temporal lobe in memory for emotionally arousing odors, I analyzed patients' performance as a function of residual amygdalar and hippocampal volumes (assessed with structural MRI). 4

In the third and final study of this dissertation (Chapter 6), I investigated further the relationship existing between emotional arousal and odor memory with manipulations that took place during encoding or retrieval. In most studies that have shown an enhancing effect of emotional arousal on memory, the encoding was incidental and the effect of arousal was stronger after a long retention interval (e.g., Kleinsmith &

Kaplan, 1963, 1964; Sharot & Phelps, 2004). Therefore, I had designed an experimental paradigm (the one used in Chapters 4 and 5) in which subjects learned odors incidentally and were tested after a week-long retention interval. In this final study, I wanted to know whether those experimental conditions were necessary for emotional arousal to enhance odor memory. To reach that aim, I carried out two experiments, one in which the influence of retention interval was measured by testing odor memory immediately and a week after incidental encoding, and a second one in which the influence of learning intention was assessed by comparing odor memory after incidental and intentional encoding.

To provide a thorough understanding of my research question, I divided the literature review (Chapter 2) into three complementary sections. In the first section entitled "Emotional arousal and episodic memory", I reviewed the diverse effects emotions have been found to have on episodic memory and the cognitive mechanisms that were proposed to explain them. In the second section entitled "Neurobiological substrates of emotional arousal's effects on memory", I reviewed the neural underpinnings of emotional memory. I did this first by providing an overview of the findings obtained with nonhuman animals and second, in humans. The last part of the review deals with "Odor memory, affective influences and its neuroanatomical

substrates". In it, I started by outlining how olfactory information can be integrated in 5 the multiple memory systems; next I presented the current knowledge regarding affective influence on odor memory and, finally, I described the neuroanatomical substrate of odor hedonics and odor memory by reviewing lesion and neuroimaging studies. 6

CHAPTER 2. LITERATURE REVIEW 7

1. EMOTIONAL AROUSAL AND EPISODIC MEMORY

"Excitement may be the successor of other emotions. When fear is relieved by the sudden disappearance of a menace, as when one has killed a rattlesnake faced suddenly in the mountains, there is no instant calm. The alarm is gone, but the waters continue to be troubled as after a squall."

- George Stratton (1928)

The relationship existing between emotions and memory is a vast and complex one. An arousing experience, such as the one described by George Stratton, is likely to be remembered powerfully. Subjective experience provides us with many examples of emotion influenced souvenirs. For instance, a first kiss, or the death of a beloved family member, is remembered differently than a less emotional life event. The influence of emotion on memory has motivated, and still does, many scientific investigations. Most of them confirm the layman's intuition by showing that emotional information is not remembered in the same way that neutral information is (Christianson, 1992). However, there is no unequivocal pattern; the influence of emotions on memory is not a straightforward one. Some researchers report an enhancing effect of emotions

(Bohannon, 1988; Brown & Kulik, 1977; Yuille & Cutshall, 1986), while others find an impairing effect of emotions on episodic memory (Clifford & Hollin, 1981; Loftus &

Burns, 1982). This literature review will present numerous effects of emotions and emotional arousal on memory, the principal theories that have been proposed to explain them and some alternative explanations. As a preamble to the review, I will provide a brief overview of these psychological concepts. 8

Emotion and Memory: Working Definitions

Memory

Memory is an extremely complex and useful set of cognitively and neurobiologically mediated processes that permit access to old knowledge but also allow acquisition of new representations. Cognitive and neuropsychological evidence has led to a view of memory as divided into multiple systems (Schacter & Tulving, 1994). One of the most important of these divisions is the declarative versus nondeclarative memory distinction. Nondeclarative memory is not available to conscious experience and does not have the flexible quality (generalization) of declarative memories. , habituation and are types of learning belonging to the nondeclarative memory system. Episodic and semantic memories are part of the declarative memory system. Semantic memory refers to knowledge. Knowing that sentences are formed of words (subject, verb and complement) and that bicycles are widely used in China are examples of semantic memories. Episodic memory refers to the recollection of events or personal experiences that are associated with a spatiotemporal context (Tulving, 1983). Remembering a grocery shopping list or the color of your bicycle are examples of episodic memories. Emotions certainly have a great influence on nondeclarative memories (see LeDoux, 1995), but in this review I will focus on the episodic aspect of declarative memory. 9

Emotions

At least two different positions are defended regarding the nature of emotions.

Some groups posit that there are six basic and innate emotions (sadness, happiness, surprise, fear, anger and disgust) with distinct facial expressions and physiological activations. Through development and interaction with different situations, secondary emotions arise (Ekman, 1977; Ekman, Levenson & Friesen, 1983). The other view, more parsimonious, hypothesizes that emotions evolved from the primitive reflex of moving away from negative things and moving towards appetitive stimuli. In more complex organisms, emotions involve multiple responses facilitating adaptation to the environment. In humans, these responses can be measured by monitoring physiological, behavioral or language variations (Bradley & Lang, 2000; Davidson & Irwin, 1999).

Valence (pleasantness), emotional arousal and mood are components of emotions that are intimately related and difficult to separate. However, because their specific impact on episodic memory will be discussed, I will propose some distinctions. The motivational parameters underlying emotional response are believed to be valence and arousal, and it has been shown that emotional stimuli fluctuate along these dimensions

(Bradley, Greenwald, Petry, & Lang, 1992; Lang, Bradley, & Cuthbert, 1990; Russel,

1980).

When evaluating the valence of a stimulus, the organism appraises whether it is appetitive (pleasant) or aversive (unpleasant): that is, whether it should be approached or avoided (Bradley, Greenwald, Petry, & Lang, 1992). Pleasantness of stimuli is often measured with rating scales. The Self-Assessment Manikin (SAM) (Hodes, Cook, &

Lang, 1985; Lang, 1980) (Figure 1, top panel for valence ratings) is widely used by researchers. This pictorial rating system has the advantage of being easy to administer 10 and to understand. It also has good concordance with objective measures. For example, the facial electromyographic response of the corrugator ("frown") and zygomatic

("smile") muscles vary reliably with SAM pleasantness ratings of pictures (Greenwald,

Cook, & Lang, 1989). With odorants, Bensafi and colleagues (2002a) report a negative correlation between ratings of pleasantness (on a simple 1-9 rating scale) and heart rate.

Figure 1. Self-Assessment Manikin (SAM) used to rate valence (pleasantness, top row) and arousal (vigor/mobilization, bottom row). From Lang, P. J., 1980, Behavioral treatment and bio-behavioral assessment: Computer applications. In J. B. Sidowski, J. H. Johnson, & T A. Williams (Eds.), Technology in mental health care delivery systems (pp. 119 -137). Norwood, NJ: Ablex Publishing. Copyright 1980 by Peter J. Lang. Reprinted with permission.

The arousal dimension of emotion refers to the activation of the sympathetic branch of the autonomic nervous system. Simply said, to be aroused means to be wide awake, alert and full of pep (Duffy, 1962; Thayer 1989). As arousal increases, the probability of falling asleep diminishes (Corcoran, 1965, 1981). Today, it is believed that emotions must include some form of physiological arousal (mostly sympathetic) and of cognitive evaluation (Mandler, 1992; Reisberg & Heuer, 1995). In research paradigms, arousal has been operationalized with subjective ratings of stimuli (e.g., rating scale varying on a sleepy-excited continuum; Figure 1; lower panel) and through 11 psychophysiological measures like the electrodermal response. For example, with pictures a linear increase was found between SAM ratings of arousal and size of electrodermal response (Greenwald, Cook, & Lang, 1989; Lang, Greenwald, Bradley, &

Hamm, 1993). With odors, a positive correlation was also found between electrodermal response and ratings of arousal, this time using a simple 1-9 scale (Bensafi et al., 2002a).

Because psychophysiological and subjective measures covary reliably, subjective measures are considered sufficient and are most often the only ones used (Bradley,

Greenwald, Petry, & Lang, 1992).

Whereas valence or pleasantness seems to characterize the direction of the emotional reaction, arousal seems to define its intensity. However valence and pleasantness are not two totally independent dimensions of emotional reactions. It has been shown that as the rated pleasantness or unpleasantness of a picture, sound or word increases, so does its arousal rating, resembling a U-shaped distribution (Bradley &

Lang, 1999a, 1999b; Lang, Bradley, & Cuthbert, 1999).

Finally, moods have been defined as "little emotions" that, unlike emotions, are not accompanied by significant psychophysiological arousal. They tend to be more subtle, to last longer and to be less intense than emotions. Compared to emotions, they are also relatively nonspecific. Moods are said to be an internal state or an internal context (Mandler, 1992). Compared to emotions, moods are more a vague internal state.

Beneficial Effect of Emotions on Memory

Effect of Mood

It is well accepted that the context in which an event occurs plays an instrumental role in retrieving it. Tulving's (1983) encoding specificity principle states that when something is stored in memory, it is not stored alone. The context in which an 12 event occurred is also encoded. can be triggered when elements of this context are re-presented. An individual's mood is a unique and often salient aspect of context.

Reiff and Scheerer (1960) were the first to propose that this "experiential" context (the mood) would act as a powerful retrieval cue.

Mood-State Dependent Memory

Bower (1981) described mood-state dependent memory as enhanced recall when the emotional state one was in during encoding is reinstated during recall. This also implies worse memory if recall is attempted in a different mood than during original learning. Bower (1992) has underlined three necessary conditions for mood dependent memory to happen. First, the induced mood must be intense. Second, the memory test must provide few retrieval cues (no recognition test) so the subject has to generate his or her own "internal cues" (including the "experiential" context) to retrieve the target. And third, mood dependent memory has a greater chance of being observed with autobiographical information than with artificial laboratory material.

Bower (1981) developed a network model of emotion to explain the effect of mood on memory (Figure 2). In his model, information is stored as nodes in a network and related nodes are interconnected. When information is accessed, the relevant node is activated and this activation spreads to connected nodes, making them easier to access.

In this network, a node corresponds to each emotional state. 13

Figure 2. Bower's (1981) network model of emotions. When studying word pairs (dying dog, lost money, happy days, etc.) in Context 1 while feeling Emotion 1, word pairs become associated to this context and that emotion. At recall, Context 1 is reactivated (because subjects are asked what they learned during that specific context) and this activation spreads in the network. Because Context 1 is associated with many things, it is a weak cue. If during recall the subject is returned to the same initial emotional state, activation from the Emotion 1 node will spread and it will sum with the activation spreading from Context 1. The summated activation makes the target more accessible to recall. S= subject, P= predicate. From "Mood and memory", by G. H. Bower, 1981, American , 36(2), p. 136. Copyright by G. H. Bower, reprinted with permission.

Mood Congruent Memory

Researchers find the effect of mood on episodic memory to be exasperating because attempts to replicate it have ended in both successes (Eich, MacAuley, & Ryan,

1995; Eich & Metcalfe, 1989 ; Ucros, 1989) and in notable failures (Bower & Mayer,

1989; Wetzler, 1985). These failures have underlined the necessity of distinguishing mood dependent memory from mood-congruent memory. Mood-congruent memory is the phenomenon in which subjects attend more to stimuli that match their emotional state (Bower, 1981). For example, individuals remember unpleasant or pleasant words better if they were, respectively, made sad or happy (through mood induction) during encoding (Bower, 1981, 1992). In mood congruent memory, the crucial effect takes 14 place at encoding because during retrieval subjects'are in a neutral emotional state.

During encoding, stimuli that are congruent with subjects' emotional state would attract their attention and would receive deeper processing.

Effect of Valence

It is widely believed that a powerful link exists between emotional valence, or pleasantness, and memory strength. Stimuli associated with positive and negative emotions have been reported to be learned very well (Christianson, 1992).

Pleasantness Superiority

Matlin and Stang (1978) introduced and defended the "Pollyanna principle". They were inspired by the cheerfully optimistic heroine of a classic of children's literature: the novel Pollyanna written by Eleanor Porter (1913). Matlin and Stang (1978) concluded that we are all Pollyannas. They present evidence that pleasantness predominates in human culture and that pleasant items are processed more accurately and efficiently than unpleasant or neutral items. They also present evidence that the "Pollyanna principle" extends to the field of learning and memory. They report experiments in which pleasant information is remembered better than unpleasant information. Selective recall of pleasant information was demonstrated with recall of daily experience (Meltzer, 1931:

Thomson, 1930; Holmes, 1970), with recall of word lists (Lynch, 1932; Griffith, 1920;

Rychlak & Saluri, 1973) and in paired associate learning (Cason, 1932; Carter, 1935;

Lott, Lott & Walsh, 1970; Drinkwater, 1972). However, Matlin and Stang (1978) acknowledged that better recall for pleasant compared to unpleasant items is not always observed. They conducted a multiple regression analysis on data from 99 studies investigating selective recall of pleasant information (in 60 of the studies selective recall was demonstrated) and found that two factors significantly influenced the likelihood of 15 obtaining better memory for pleasant compared to unpleasant items. These factors were the implementation of longer retention intervals and of perfect learning (mastery in performance was required).

Unpleasantness Superiority

Despite the beliefs of Matlin and Stang (1978), reports of a memory advantage for unpleasant or traumatic information are seen often (Christianson & Loftus, 1987). For example, Yuille and Cutshall (1986) interviewed of a murder and report high accuracy in their recall of the murder. The "weapon focus" phenomenon, where the weapon used in a crime is fairly well described by witnesses, is another indication of an advantage for unpleasant or traumatic information in memory (Loftus, Loftus, & Messo,

1987; Maas & Kohnken, 1989).

However, when memory for unpleasant and pleasant words or naturally occurring personal emotional events is assessed, often no advantage for unpleasant compared to pleasant items is unveiled (Bradley & Baddeley, 1990; Thompson, 1985). Bradley et al.

(1992) reproduced these findings with pictures. They pointed out a shared quality of the pleasant and unpleasant stimuli that were remembered better; those pictures were rated as being more emotionally arousing. Indeed, the more a stimulus is polarized in one direction or the other on the pleasantness dimension, the more arousing it will tend to be

(Bradley & Lang, 1999a, 1999b; Lang et al., 1999). Arousal may very well be the component of emotions that is responsible for this reported pleasantness effect.

Effect of Arousal

From an evolutionary perspective, it seems adaptive to have enhanced memory for emotionally arousing stimuli (Davidson, 2003; Joseph, 1996). Indeed, whether pleasant (e.g., a love affair) or not (e.g., being robbed), emotionally arousing events are 16 normally more important for survival and for gene transmission than nonarousing or neutral events.

Physiological Arousal

Physiological arousal can have beneficial effects on the cognitive processing of information. It facilitates the detection of stimuli. Hamilton, Fowler and Poirier (1989) showed that with high levels of arousal, sustained detection of simple stimuli is facilitated, as is rapid response to those stimuli. Second, arousal also facilitates the encoding of stimuli for long term retention. These beneficial effects should not be particularly surprising. Indeed, most models of declarative memory imply that being aroused, alert or attentive is a good, if not a necessary, thing for a solid memory trace

(Revelle & Loftus, 1992).

A series of experiments have used white noise to induce higher arousal (and to increase electrodermal response). When white noise is presented during paired associate learning, subjects exhibit better memory than in the absence of white noise (Berlyne,

Borsa, Craw, Gelman, & Mandell, 1965; Berlyne, Borsa, Hamacher, & Koenig, 1966;

McLean, 1969). Caffeine administration has also been used to manipulate arousal levels.

Increase in memory is reported after administration of coffee or of a caffeinated drink

(Haskell, Kennedy, Wesnes, & Scholey, 2005; Warburton, Bersellini, & Sweeney,

2001). Loftus (1990) manipulated high and low arousal levels by assigning subjects to a physical exercise or a relaxation group. The high arousal group forgot less of a studied

word list than did the low arousal group.

Stimuli with Arousing Properties

It appears clear that physiological arousal can improve memory. Memory

improvement is also found when physiological arousal is associated with emotion- 17 eliciting stimuli. Indeed, the memory enhancing effect of emotionally arousing stimuli has been demonstrated with different types of material and various experimental paradigms.

Corteen (1969) found that aurally presented words that led to high arousal

(measured through electrodermal recordings) were remembered better than those producing lower arousal both 20 minutes and 2 weeks after encoding. Craik and

Blankstein (1975) also reported that verbal items associated with higher arousal at encoding (more important electrodermal response) are recalled better in a subsequent memory test.

Bradley et al. (1992) asked subjects to rate how arousing and how pleasant they found each picture of a series. Immediately and one year after this incidental encoding session, subjects wefe submitted to an unexpected test. Irrespective of the rated pleasantness, the pictures rated as being more arousing were remembered better than the less arousing ones. Also, with a speeded recognition test, arousing pictures were recognized faster than nonarousing ones and subjects made more errors with the nonarousing pictures (Bradley, Greenwald, Petry, & Lang, 1992).

Andrews (1990) used scenes from commercially successful movies as memory targets. Participants studied scenes that varied in emotional content but that were equivalent in duration and relevance to the movie plot. Six to 18 months later, the participants were tested and better memory was reported for the emotional compared to the nonemotional scenes. Heuer and Reisberg (1990) presented their subjects either a neutral or an emotional story. Each story consisted of 12 pictures accompanied by a narrative. The first and last parts of both stories were the same. The middle part of the stories differed in the degree to which the pictures and narrative were arousing. Two 18 weeks later, subjects were submitted to a surprise memory test. Those who experienced the emotionally arousing story remembered more information than those presented with the neutral story. This advantage was specific to the central part of the story, the part differing in emotional content.

-o— Neutral story -•—Arousing story •a ~

"TO O 0 i_ f _ 0 2 4—* o 'a. c 03

Phase 1 Phase 2 Phase 3

Figure 3. Phase by phase recall of emotionally arousing and neutral pictures. From "A novel demonstration of enhanced memory associated with emotional arousal", L. Cahill and J. L. McGaugh, 1995, Consciousness and , 4, p.417. Copyright by Elsevier. Reprinted with permission.

However, it might be argued that the emotional items were more memorable because they differed in novelty or in complexity and not because of their supposed emotional dimension. To circumvent that problem, Cahill and McGaugh (1995) designed an experiment very similar to the one of Heuer and Reisberg (1990), but they used the same pictures in both the neutral and the emotional versions of the story and kept the two plots as similar as possible. Their results, depicted in Figure 3, were similar to those of Heuer and Reisberg (1990). With that additional control, Cahill and 19

McGaugh (1995) demonstrated the strength of the effect of enhanced memory for emotionally arousing stimuli.

Enhancement of memory by emotional arousal is much more than a laboratory artefact. For example, Wagenaar and Groenewerg (1990) compared two testimonies, made at a 40-year interval, of 78 former prisoners of a Nazi concentration camp. They found that even after 40 years, the concentration camp experience was remembered in great detail. Yuille and Cutshall (1986) interviewed witnesses of a clearly emotional event, a daylight shooting involving one dead and one wounded. Even when the witnesses were interviewed 4 to 5 months after the crime, their reports accurately reflected the police report, especially concerning the details of the action and the description of the objects on the crime scene. Another example of the strength of the enhancing effect of emotional arousal on memory outside the laboratory was observed after the 1995 earthquake in Kobe, Japan. This is an event likely to be strongly emotionally arousing. Memories of patients with Alzheimer's disease were examined and it was found that recollections of the earthquake were well conserved compared with memory for a less emotional event (a first MRI examination) (Ikeda et al., 1998).

The intensity of an emotional event seems to be strongly correlated with its vividness or clarity in memory. Reisberg and Heuer's (1995) results support this proposal. They gave a list of personal events (e.g., graduation, first job) to their participants and asked them to rate the vividness of their memory for each one and also to rate how emotional each event was when it happened. They found a strong positive correlation between vividness and emotionality ratings, and this correlation was independent of the initial pleasantness of the event. 20

Flashbulb Memory

A discussion of emotional intensity and the vividness of memory in the "real" world would hardly be exhaustive without referring to "flashbulb memory" (Brown &

Kulik, 1977). Flashbulb memories were first described as detailed and permanent memories for the circumstances surrounding a major or very surprising (and emotionally arousing) event. Brown and Kulik (1977) argued that flashbulb memories necessitated a special mechanism that was triggered when an event exceeded criterion levels of surprise and consequentiality (or emotional arousal). Since flashbulb memories were first described, almost every noteworthy public event became a research opportunity.

Flashbulb memories have been investigated surrounding the attempted assassination of

President Ronald Reagan (Pillemer, 1984), the explosion of the space shuttle Challenger

(Bohannon, 1988; McCloskey, Wible, & Cohen, 1988), the assassination of the Swedish

Prime Minister Olof Palme (Christianson, 1989), the O.J. Simpson murder trial

(Schmolck, Buffalo, & Squire, 2000), the death of princess Diana (Hornstein, Brouwn,

& Mulligan, 2003) and the terrorist attacks of September 11, 2001 (Greenberg, 2004;

Talarico & Rubin, 2003).

However, flashbulb memories are not as accurate as they were once believed to be. Flashbulb memories are not immune to and memory distortions; as the time between the original event and recall increases so does forgetting and errors in recollections (Schmolck, Buffalo, & Squire, 2000). Moreover, it was demonstrated that what characterized flashbulb memories the most was not their accuracy but the high belief (or confidence) subjects had in their accuracy (Talarico & Rubin, 2003). 21

Interfering Effect of Emotions on Memory and Other Specific Effects

These inaccuracies and forgetting suggest that the effect of emotions on memory is not uniquely enhancing. Because our memory capacity is limited, it also seems important to be able to ignore or forget some things and to devote more attention to others. Thus, an interfering effect would be adaptive as well.

Effect of Mood

It is often reported that with the induction of a depressed mood, subjects show worse recall than when in a neutral mood (Ellis, Thomas, McFarlane, & Lane, 1985;

Ellis, Thomas, & Rodriguez, 1984). However, the common belief that depressed individuals are inefficient in cognitive tasks may lead subjects to perform accordingly.

Mood congruence effects vary as a function of mental health. In a meta-analysis,

Matt, Vazquez and Campbell (1992) found that when presented with an equal number of positive, neutral and negative stimuli, nondepressed subjects recall around 8% more positive than negative stimuli and subclinically depressed subjects recall positive and negative stimuli equally well, but depressed individuals recall about 10% more negative than positive stimuli.

Age

The Socioemotional Selectivity Theory (Carstensen, Fung, & Charles, 2003) hypothesizes that older adults, or individuals perceiving their remaining time as limited, place more value on emotionally meaningful goals and exhibit a bias towards positive information in attention and memory. The findings of Charles, Mather and Carstensen

(2003) are in agreement with the Socioemotional Selectivity Theory. They presented 32 pictures (16 neutral, 16 emotional [of which 8 were positive and 8 negative]) to young

(18-29 years old), middle aged (41-53) and older adults (65-80). Fifteen minutes after 22 viewing the pictures, participants were submitted to unexpected recall and recognition memory tests. The authors found that relatively fewer negative than positive and neutral pictures were recalled with age. The pattern of results was similar with recognition: younger adults recognized relatively more negative than neutral or positive pictures; older adults showed comparable memory for negative, neutral or positive pictures.

Effect of Arousal

For many psychologists, emotionality clearly undermines memory accuracy

(Kassin, Ellsworth, & Smith, 1989; Yarmey & Jones, 1983). Moreover, experts on agree that very high levels of stress (or arousal) impair the accuracy of eyewitness testimony (Kassin, Ellsworth, & Smith, 1989; Yerkes & Dodson,

1908). Arousal's effect on memory manifests itself differentially depending on the central or peripheral nature of information, on encoding and retrieval paradigms, on length of retention interval and even as a function of a subject's personality.

Intrusion Errors

Heuer and Reisberg (1990) report more intrusion errors in the recall of subjects who viewed an emotional story compared to subjects who saw a neutral one. When faced with an emotional story, the plot is well recalled but subjects tend to confabulate about the characters' motives or reactions.

Periphery versus Central Component of Stimuli

Numerous studies report a pattern of enhanced memory for central information

(sometimes referred to as the gist) and worse memory for peripheral information

(sometimes referred to as details) (Burke, Heuer, & Reisberg, 1992; Christianson, 1984;

Christianson & Loftus, 1987, 1991). Peripheral, but not central, information refers to those aspects of an event that can be modified without changing the event's identity. The 23 color of the background of a scene, the angle in which a photograph is taken or minor aspects of clothing are examples of peripheral details (Heuer & Reisberg, 1992).

Kebeck and Lohaus (1986) presented a film relating an argument between a teacher and a student. One group of subjects viewed a version in which the argument escalated, and a second group viewed a version in which the argument stayed calm. In the subsequent immediate memory test, subjects who had seen the emotional version recalled as much central information as the subjects who had viewed the neutral version.

However, the participants in the emotional condition had a poorer memory for the peripheral details of the argument.

Additional evidence that emotions weaken memory for peripheral details was collected by Christianson and Loftus (1987, 1991). In their experiments, subjects were shown pictures that recounted either a traumatic or a neutral story. During each one, subjects were asked to write a word or a sentence describing what was distinctive in the picture. Following the last one, subjects were tested for their memory of the self- generated word or sentence and for recognition of the original pictures. The distracters were similar to the original pictures but were taken from a different camera angle.

Christianson and Loftus considered that type of information to be a detail. They found that subjects who had seen the traumatic version had a better memory for the central information (words and sentence) and a worse memory for details (recognition of correct photographic angle) compared to subjects who had seen the neutral version.

Loftus and Burns (1982) showed their subjects one of two versions of a brief film about a bank robbery. In one version, the robber runs away and shoots a little boy in the face. In the other version, the robber runs away and the bank manager tells clients and employees to remain calm. Immediately after viewing the film, participants were 24 submitted to a memory test for the first part of the films (it was the same in both versions). Participants who had seen the version in which the little boy was shot remembered fewer peripheral details than participants who had viewed the neutral version.

Encoding Paradigms

In most studies of emotional arousal and memory, the learning instructions are incidental. At encoding, participants are not aware that their memory will be tested subsequently because researchers want to minimize, or control, the influence of rehearsal and other strategies on emotional memory.

I am aware of three studies that have manipulated encoding instructions. In the first one, McLean (1969) conducted two experiments of paired-associate learning that differed in learning instructions; in one they were incidental and in the other intentional.

McLean (1969) found that it was only after incidental learning, and not after intentional learning, that participants remembered more of the arousing than nonarousing pairs.

A second study of arousal and memory in which encoding instructions were manipulated was conducted by Heuer and Reisberg (1990). They compared memory

(after a retention interval of 2 weeks) for 12 pictures depicting either an arousing or a neutral story. The group shown the arousing story was told only to attend to the story

(incidental encoding). Another group, shown the neutral pictures, was told that their memory would be tested (intentional encoding). The group that saw the arousing pictures had a better memory than the group that saw the neutral ones. However, this effect was more evident for the middle part of the story (which included different pictures). The arousing group also remembered better the final pictures, which were the same for both groups. 25

Finally, the third study of memory and emotional arousal that manipulated learning intention consisted of two experiments in which participants were younger and older adults (Kensinger, Piguet, Krendl, & Corkin, 2005). One experiment had incidental and the other had intentional learning instructions. In both experiments, 40 pictures were presented, half neutral and half emotional (negative). Fifteen minutes later, participants were submitted to a recognition test for central or peripheral fragments of encoded or foil pictures. The effect of learning instructions in this study varied as a function of age. With incidental instructions, both groups (young and old) were more accurate in their recognition of the central parts of the negative compared to neutral pictures. For the peripheral parts, both age groups were more accurate at recognition of neutral pictures. With intentional learning instructions, younger and older adults remembered, again, more negative than neutral central elements. However, only the younger adults overcame the emotional attentional bias and remembered peripheral elements of negative and neutral pictures equally well.

It seems that when the encoding is incidental, emotionally arousing stimuli grab more attentional resources, explaining why they are remembered more accurately than nonarousing information. When subjects are explicitly told to remember, they can overcome the emotional attentional bias and devote equal attention (or cognitive resources) to arousing and nonarousing information. This could explain why the memory enhancement effect for emotionally arousing information is stronger with incidental instructions.

Retrieval Paradigms

The way memory is tested (recall vs. recognition) also contributes to the effect of emotional arousal on episodic memory. Christianson (1984) and Christianso'n and Loftus 26

(1987) presented to their subjects one of two slide sequences of pictures that depicted an emotional or a neutral version of a same event. The subjects who viewed the emotional sequence recalled more central features than did those who saw the neutral version.

However, if the subjects were tested by recognition, no difference was detected. If suitable retrieval cues are provided, the impact of emotion on memory may not be observable, even if it is present. In a recognition test all of the information is available to the subject and there is no need for him to generate retrieval cues. In that situation, the advantage given by a richer emotional memory trace by the generation of more powerful retrieval cues would become irrelevant, and the memory effect eliminated.

Retention Interval

The length of the time interval separating presentation of the to-be-remembered material from recollection is another factor that clearly seems to modulate the impact of emotion on memory.

Kleinsmith and Kaplan (1963,1964) were among the first to provide evidence that an interaction takes place between retention interval and memory for emotionally arousing information. They found that at short intervals (immediate test), memory was poorer for emotional compared to neutral words, and that at longer intervals (1 week later) this pattern reversed and memory for emotional words was superior. These results have been replicated many times (Baddeley, 1982; Butter, 1970; Farley, 1973; Kaplan &

Kaplan, 1969; McLean, 1969; Osborne, 1972; Quevedo et al., 2003; Walker & Tarte,

1963), but some studies failed to replicate this interaction (Corteen, 1969; Maltzman,

Kantor, & Langdon, 1966). Because of these inconsistencies, Park and Banajii (1996) carried out a meta-analysis. They concluded that this rebound in memory accuracy for 27 emotional material as a function of retention interval was a reliable effect, if not especially large.

Burke, Heuer and Reisberg (1992) reported another effect of retention interval that must be considered. They presented subjects with a neutral or emotional slide sequence of pictures and tested some subjects immediately after presentation, some a week later and others on both occasions. Subjects who were tested a second time after a week performed better than did subjects tested for the first time after a week. The immediate test seemed to act as a rehearsal and "fixed" a memory pattern. The effects of arousal in the one-week second test were similar to those observed in the immediate test.

These effects did not resemble those of arousal when memory was tested after a week for the first time. If subjects are tested twice, the effect of emotion on memory may be abolished.

Personality

Introverts are claimed to be more "naturally" aroused than extroverts, and extroverts are claimed to show faster arousal habituation (Gale, 1981; Revelle & Loftus,

1992). Bowyer, Humphrey and Revelle (1983) examined whether introverts' and extroverts' memory performance differs (the arousing quality of the information to learn was not manipulated). They (1983) found that the performance of extroverts, and not of introverts, deteriorated rapidly over time in a forced choice recognition study.

Interestingly, when the extroverts' arousal level was increased with a moderate dose of caffeine, this decay in performance disappeared.

However, other studies claim that there is no tonic psychophysiological (baseline

SCR) difference between low and high sensation seekers (a correlate of intro- extraversion) (Neary & Zuckerman, 1976; Ridgeway & Hare, 1981; Smith, Davidson, 28

Smith, Goldstein, & Perlstein, 1989). In contrast, Smith, Davidson, Smith, Goldstein and

Perlstein (1989) reported that high sensation seekers have higher phasic psychophysiological responses (SCR in response to a stimulus) and show higher word recall than low sensation seekers.

Cognitive Mechanisms Underlying the Effects of Emotional Arousal on Memory

In the previous section, I reviewed the current knowledge concerning the diverse effects of emotions on memory. In the following section, I will focus on some of the cognitive models and theories that have been proposed to account for the effects of emotions on memory.

Emotions Guide Encoding and Retrieval

It is now clear that memory for emotionally arousing events is good but not equivalent to an exceptionally clear picture, as implied by the notion of flashbulb memory (Brown & Kulik, 1977; Yarney & Bull, 1978). Nevertheless, special processing seems to take place during encoding, consolidation and probably during retrieval of emotionally arousing events (Eysenck, 1976; Ochsner & Schacter, 2000).

The emotional Stroop and emotional priming provide empirical evidence that emotion guides encoding by modifying early processing of information. In the emotional

Stroop, subjects are asked to name the color in which emotional and neutral words are printed and not to read the words out loud. The emotional Stroop effect refers to the fact that it takes more time for subjects to name the color of emotional compared to neutral words. This was interpreted as evidence that emotional stimuli are capturing attention

(Pratto & John, 1991) or as an indication that there is a perceptual bias favoring automatic encoding of emotional stimuli (Williams, Matthews, & MacLeod, 1996). 29

Hansen and Hansen (1988) showed their subjects large matrices of faces and found that angry faces in happy and neutral "crowds" were detected much faster than the opposite (detecting happy or neutral faces in an angry "crowd"). These authors interpreted their data as suggesting emotional priming, which is a pre-attentional automatic processing of emotional information. This anger superiority effect does not mean that happy faces are not emotional, only that attention to angry or threatening faces has a higher survival value. In Ohman's (1979) view, this automatic and nonconscious emotional evaluation of stimuli activates an orienting response and the stimuli become the focus of attention. In this way, critical emotional details will automatically be attended to. Emotional stimuli are also easier to detect in attentional blink paradigms

(Anderson & Phelps, 2001; Chun & Potter, 1995). This emotional priming would promote memory for central and not for peripheral detail because it was the central emotional information, and not the peripheral detail, that became the focus of attention.

Other evidence indicating that the processing of emotional information during , or encoding, does differ without the intervention of consciousness was obtained by Christianson and Fallman (1990). They presented aversive, neutral and appetitive pictures very briefly (50ms) and found that aversive pictures were recalled better. As suggested by Hansen and Hansen (1988) and by Ohman and Dimberg (1984), this predisposition to detect and retain emotional characteristics of information may reflect some survival value from earlier stages in human evolution.

Emotionally arousing stimuli are difficult to ignore. If these stimuli direct encoding by capturing attention, they probably can influence retrieval of information as well. Remembering information is a constructive process in which retrieval cues and memory trace are combined (Bartlett, 1932; Schacter, 1982; Tulving, 1983). The current 30 emotional state of the subject and the emotional properties of the retrieval cues are likely to influence what is remembered. Christianson (1992) suggested that shortly after witnessing an emotional episode, subjects are likely to be still emotional and this might interfere with and disrupt short-term memory.

Some Theories

In this section, the most articulate or popular theoretical proposals that have been advanced to account for emotions' effect on memory will be introduced.

The Beginnings: Yerkes-Dodson, Walker, and Easterbrook

optimal level

oCD c CO E

Q. & point of O waking E 0

low medium high

Arousal Figure 4. The Yerkes-Dodson law (1908) illustrating the relationship between performance (memory) and arousal.

It was traditionally reported that an increase in arousal from a low to a moderate level improves memory, but that an increase from a moderate to a high level leads to a decrement (Yerkes & Dodson, 1908) (Figure 4). In some situations this model still seems correct. For example, Deffenbacher (1983) reviewed the literature on arousal and eyewitness testimony and concluded that most studies supported the inverted U-shape function. However, the Yerkes-Dodson law is insufficient. It cannot explain the 31 interaction implicating type of emotional material (arousing versus nonarousing) and type of detail information (central versus peripheral), retention interval (immediate versus delayed) and type of memory test (recall versus recognition).

The next theoretical proposal about the effects of emotional arousal on memory was made by Walker in 1958. He proposed that the increase in physiological arousal associated with emotions produces a temporary inhibition of retrieval during the formation of a memory trace. This hypothesis can only explain the interaction that is observed between emotional information (arousing or not) and retention interval

(immediate versus delayed).

According to the "Easterbrook claim", physiological arousal results in a narrowed attention (Bruner, Matter, & Papanek, 1955; Easterbrook, 1959). This narrowing of attention leads subjects to be attentive to a smaller proportion of the information available in the environment. This claim implies that subjects will pay close attention to central aspects of information to the detriment of peripheral aspects. Indeed, this narrowing of attention seems inevitable given that cognitive ability is limited. In an emotionally arousing situation an individual does not have the luxury to admire the

"scenery", and will pay attention to the emotionally significant information

(Christianson, 1992). The "Easterbrook claim" can explain the effect of type of encoding instructions (incidental versus intentional). Indeed, Kensigner et al., (2005) have demonstrated that when young adults are told explicitly to memorize information, they are able to overcome the attentional bias caused by emotion and to remember neutral and emotional information equally well.

However, the "Easterbrook claim" cannot explain the interaction between type of detail information (central versus peripheral) with retention interval (immediate versus 32 delayed), nor the effects related to type of test (recall versus recognition). Hence, the

Easterbrook claim also offers an incomplete explanation of the impact of emotional arousal on declarative memory.

Cognitive Organization: Schemas

Some researchers have related the effects of emotions on memory to schemas. A is a coherent and structured cognitive representation that organizes experience

(Bartlett, 1932; Horrowitz, 1991; Mandler, 1988). Schemas can represent concrete domestic activities (e.g., how to bake a cake) or abstract concepts (e.g., love or justice).

When encountering an emotionally arousing situation or event, the corresponding schema will be activated automatically (Mandler, 1992).

Schemas direct attention to schema-relevant information, which will be noted and remembered, whereas information not relevant to the activated schema will go unnoticed and will be remembered poorly (Levine & Burgess, 1997; Stein, Liwag, &

Wade, 1996). In an emotional situation, it is presumed that the central details are schema-relevant information while the peripheral details are schema irrelevant. Schemas also guide retrieval. At recall, schemas will specify the "gist" of the to-be-remembered information and, in this way, lead to veridical memories as well as to context-related intrusion errors. In fact, schemas fill in for the unattended information (Mandler, 1992;

Ochsner & Schacter, 2000).

The application of schema theory to memory for emotional information certainly deserves interest but it also provides incomplete explanations. It explains well why in emotional events, central compared to peripheral details are remembered and recalled better. It also describes why intrusion errors are likely to be encountered in the recall of emotional material. However, to explain the memory advantage of central details of 33 emotionally arousing events, it has to be awkwardly assumed that in nonarousing events, the central details are schema irrelevant. This theory is also silent on the retention delay

(immediate versus delayed) and memory tests effects (recall versus recognition).

"Tick-Rate " Hypothesis

According to the "tick-rate" hypothesis, said to be in direct analogy to the clock speed of a computer, emotional arousal increases the rate at which information in the environment is sampled or encoded (Humphreys & Revelle, 1984; Revelle, 1989;

Revelle & Loftus, 1992). In this way, more emotionally arousing than neutral information is encoded per unit of time. Shortly after encoding, it may be more difficult to retrieve emotional events compared to their neutral siblings because more information has been encoded in the former, making emotional events more susceptible to interference. After longer intervals, encoded emotional events will have undergone more consolidation. Because more information has been encoded, more connections with internal and external contexts are possible (Crowder, 1976). This enriched consolidation would result in a relatively better long term recall of emotionally arousing events compared to neutral or nonarousing events.

The "tick-rate" hypothesis is attractive and it provides a compelling explanation for the interaction between type of emotional information (arousing versus nonarousing) and retention interval (immediate versus delayed). With little extrapolation, the effect related to type of memory test can also be explained. Emotional events undergo more consolidation, which makes them easier to retrieve. In a recognition test, this advantage might not be apparent because all the retrieval cues are present. However, the theory loses its appeal when it is unable to account for the memory effect related to type of detail information (central versus peripheral). 34

Levels of Processing Theory

The seminal level of processing theory (Craik & Lockhart, 1972) has been applied to memory for emotionally arousing information (Robinson, 1980). This theory states that maintenance rehearsal (e.g., auto-repetition of perceptual properties of stimuli, shallow processing) does not improve long-term memory, whereas elaboration

(e.g., generation of associations, deep processing) does (Craik & Lockhart, 1972; Craik

& Tulving, 1975). It is assumed that following the perception of a neutral versus an emotionally arousing event, subjects engage in differential processing. For example, viewing a picture of a freshly mutilated child is more likely to lead an individual to be concerned about this child's story and elaborate around it than after viewing a picture of the same child sitting quietly with all his body parts intact. Hence, it is supposed that neutral events are associated with maintenance rehearsal and that arousing events lead to a deeper or more elaborated processing that enhance memory by creating a richer memory trace.

With a few tenable assumptions, Craik and Lockhart's (1972) levels of processing theory predicts with relative accuracy the effects of emotions on memory.

The theory states that elaboration improves long-term memory, and this clearly explains why emotionally arousing stimuli are remembered better after a delay. If it is assumed that central details of emotional information are more arousing than peripheral ones, the theory also explains the effect relative to the type of detail information (central versus peripheral). The theory could also account for the type of test effect (recall versus retrieval) if it is considered that elaboration produces a richer memory trace. At recognition, the advantage of the richer memory trace in the generation of retrieval cues 35 will be obliterated by the presence of the to-be-remembered material, which is probably the most powerful retrieval cue one can imagine.

However, this theory is based on elaborative and rehearsal processes. When these processes are experimentally controlled, emotional arousal still has a specific effect on memory (Guy & Cahill, 1999; Heuer & Reisberg, 1990).

As can be seen, at the moment, no proposed theory can account for all the effects emotional arousal has on memory (Table 1). To understand these interactions it will probably be necessary to integrate findings from . Table 1

Some Effects of Emotional Arousal on Declarative Memory and Explanatory Theories

Arousing Intrusion errors Peripheral versus Incidental versus Recall versus Immediate versus central intentional recognition versus delayed nonarousing information encoding test information

Yerkes-Dodson +

Walker +

"Easterbrook + + + claim"

Schemas + + -/+

"Tick rate" + -/+ + hypothesis

Levels of + -/+ -/+ + processing Note. - cannot explain, + can explain, -/+ can explain with some assumptions. 37

Alternative Explanations

It could be argued that factors other than emotional arousal per se modulate the preceding memory effects.

Event Distinctiveness

Emotional events can be seen as more distinctive and unusual than neutral events. Indeed, distinctiveness has been shown to ameliorate memory (Hunt & Elliott,

1980; McDaniel & Einstein, 1986). Christianson and Loftus (1991) investigated that specific hypothesis by comparing memory for a sequence of neutral pictures (woman riding a bike), with memory for emotional (woman lying wounded beside her bike) and distinctive/unusual pictures (woman carrying a bike on her shoulders). They found that the peripheral details were recalled equally well in the emotional and distinctive conditions. However, recall for the central details (e.g., color of the woman's clothing) was improved only in the emotional condition. These results make it unlikely that distinctiveness by itself is responsible for the effect of emotion.

Differential Distribution of Attention

The effects of emotion on memory could also potentially be explained by a different distribution of attention at initial processing of information. Actually, the more attention paid to some aspect of an event, the more securely this aspect will be remembered (Bower, 1992). To explore this alternative hypothesis, Christianson, Loftus,

Hoffman and Loftus (1991) manipulated the amount of time their subjects attended to specific detail information of emotional and neutral pictures. They did so by presenting each picture for 180 ms and preceding its presentation by a fixation point. Despite this early attentional control, the central details of emotional pictures were retained better than the central details of neutral ones. Another experiment in the same study 38

(Christianson, Loftus, Hoffinan, & Loftus, 1991) used a slightly different procedure but produced comparable data. Subjects were allowed to fixate emotional and neutral pictures normally, but their eye movements were recorded. It was found that subjects fixated the central details of emotional pictures more often than they did for neutral pictures. However, when fixation to central detail information was equivalent in both types of picture, memory for the central details of emotional pictures was still superior to that of neutral ones. This indicates that while they may matter, eye movements and early attentional focus cannot explain all of emotions' effects on memory.

Semantic Relatedness

The effect of semantic relatedness has been used to explain the memory enhancement observed for emotional stimuli. Interrelated information is remembered better than nonrelated information because the search parameters are reduced during retrieval (facilitating it) (Puff, 1970; Tulving & Pearlstone, 1966). According to Talmi and Moscovitch (2004), emotionally arousing information would be remembered better mostly because it is more interrelated than neutral information, and emotional arousal itself would play only a minor role in enhancing memory.

However, Buchanan, Etzel, Adolphs and Tranel (2006) demonstrated additive effects of semantic relatedness and emotional arousal. Words that are semantically related are remembered better than words that are not; however, a combination of semantic relatedness and of emotional arousal (for example in taboo words) results in optimal free recall and recognition.

Greater Rehearsal and Elaboration

It could also be argued that the effects emotions have on memory are due to the greater rehearsal and elaboration emotional stimuli receive. Indeed, we think and talk 39 much more about emotional memories than nonemotional ones (Schacter, 1996).

Thomas and Diener (1990) asked their subjects to write daily in a diary and found that their subjects rehearsed and remembered the negative events more. Other studies also report a modest positive correlation among emotion, rehearsal and memory (Cohen,

Conway, & Maylor, 1994; Conway & Bekerian, 1988; Rubin & Kozin, 1984; but see

Bohannon, 1988; Christianson & Loftus, 1990).

However, emotions' effects on memory are not reproduced with manipulations leading to closer attention, rehearsal and elaboration. Heuer and Reisberg (1990) demonstrated this by comparing memory for a neutral story to memory for an emotional one. One group was presented with the emotional story and three groups were presented with the neutral one. The stories were made of pictures and narratives that were matched as much as possible. Both stories consisted of sequences of 12 pictures accompanied by

12 sentences. The three first and last four pictures and sentences were the same in both stories. They depicted a mother and her son going to visit the father at his workplace. In the neutral version the father is a mechanic and repairs a car. In the emotional version, the father is a surgeon who operates on the victim of a car accident.

There were three neutral story conditions. In one group subjects were told only to attend to the story. In the "problem-solving" group, subjects looked at the neutral story and were told that it mimicked recent news or a recent movie and that their only task was to find what event was being mimicked. This manipulation allowed the researchers to observe the effect of close attention. In the third neutral group, the "memorizing" group, subjects looked at the same neutral story but were told that they should remember

as much as possible because their memory would be tested. With that condition, the researchers wanted to measure the effect of rehearsal. In the emotional condition, 40 subjects simply looked at the emotional story. Heuer and Reisberg (1990) found that close attention and rehearsal influenced memory but not in the same way emotions did.

Subjects in the three neutral conditions remembered the gist of the story well, but compared to subjects in the emotional condition they did not show any advantage in remembering central compared to peripheral details.

Guy and Cahill (1999) also concluded that overt rehearsal was not sufficient to explain the enhancement of memory for emotionally arousing events. They showed subjects arousing and neutral films and asked them either not to discuss the films with anyone (no rehearsal condition) or to discuss the films with at least three persons

(rehearsal condition). One week later, subjects came back to the laboratory expecting to view more films, but instead their memory for the films was tested. Guy and Cahill

(1999) found better memory for arousing films in all conditions and that the advantage of arousing versus neutral films did not differ as a function of rehearsal. However, these results can be questioned because the manipulation of overt rehearsal appears weak.

Even if subjects were asked in a post-experimental questionnaire whether they had complied or not with the instructions (of talking or not about the films) and were assigned to the other experimental condition if they had not complied, subjects could still have rehearsed without talking about the films. Moreover, subjects in the talking conditions could have talked about superficial aspects of the films, which compared to semantic elaboration (deep encoding) is not an efficient encoding strategy (Craik &

Lockhart, 1972; Craik & Tulving, 1975).

If greater distinctiveness, semantic relatedness, additional attention and rehearsal cannot, on their own, explain how emotion has a selective influence on memory, it does 41 not mean that their combined effect is inconsequential. Emotions may modulate memory by changing the way information is processed during encoding and retrieval.

Conclusion

The conflict in the literature concerning the direction of the effect of emotional arousal on memory is only apparent. If the complex interactions involved in the effect are ignored, conflict is inevitable. Emotional arousal has both enhancing and reducing effects on memory performance. Not only the arousing quality of the memory material

(arousing/neutral), but the, type of information (central/peripheral), the type of test

(recall/recognition) and the time of test (immediate/delayed) are factors critically involved in the interaction. They must be considered in any serious investigation of the effect. 42

2. NEUROBIOLOGYAL SUBSTRATES OF EMOTIONAL AROUSAL'S EFFECTS ON MEMORY

"The attention which we lend to an experience is proportional to its vivid or interesting character; and it is a notorious fact that what interests us most vividly at the time is, other things equal, what we remember best. An impression may be so exciting emotionally as almost to leave a scar upon the cerebral tissues... "

- , Principles of Psychology, (1890)

As seen in the first part of this review, emotional arousal modulates memory strength; that is, it seems to enhance or impair encoding and of information relative to its emotional importance (Cahill, 2000). As suspected by William James, emotionally arousing events, pleasant or not, activate hormonal and brain systems that will consolidate these events in memory (Cahill, 1999; Cahill & McGaugh, 1998;

McGaugh, 2004). In this section, I will review the current knowledge regarding the neurobiological substrates of emotional memory. First, I will do this in nonhuman animals and second, in humans.

Emotional Memory in Nonhuman Animals

Emotionally arousing events, such as receiving a foot shock or having to find a submerged and hidden platform in a pool, are events that rodents remember well generally. The cascade of hormones and neurotransmitters released during these, or any other, emotional experiences has long been suspected to play a central role in the strength of emotional memories. The amygdala also appears to be a key structure in emotional memory. Now I will review evidence indicating that the enhancement of memory for emotionally arousing stimuli is mediated by an interaction of epinephrine, norepinephrine, acetylcholine, corticosterone and the basolateral amygdala (McGaugh,

2004a). 43

Amygdala

The amygdala is an almond-shaped structure located in the anterior portion of the medial temporal lobe. The amygdala is comprised of a set of densely interconnected nuclei. Among them, the basolateral and centromedial nuclei have received the most attention. Most sensory inputs project from the thalamus and cortex to the basolateral nucleus, whereas most amygdala outputs originate from the centromedial nucleus

(Eichenbaum, 2002). Since Kluver and Bucy in 1937, amygdala functions have been associated with mammalian emotions. They found that monkeys with amygdala lesions exhibited considerable emotional changes such as loss of fear of previously feared stimuli, enhanced attempts to copulate with members of the same sex or of other species and attempts to eat inappropriate objects (Kluver & Bucy, 1937; Weikrantz, 1956).

Goddard (1964) was among the first to suggest that the amygdala is involved in . The performance of his rats on an aversive task was impaired when they received electrical stimulation in the amygdala shortly following training.

This disruption of memory consolidation by amygdala stimulation has been replicated many times (Kesner & Wilburn, 1974; McGaugh & Gold, 1976). However, it has been found that when the intensity of the stimulation and the training conditions are varied, the electrical stimulation can either enhance or impair inhibitory avoidance1 (Gold,

Hankins, Edwards, Chester, & McGaugh, 1975), indicating a modulatory influence of the amygdala on aversive training.

1 Inhibitory avoidance training is a behavioral task in which a rat is placed in a brightly-illuminated chamber facing a guillotine door. When the rat turns in the opposite direction, the guillotine door opens and gives access to a darker chamber. The time it takes the rat to enter the darker chamber is recorded, and when the rat enters this chamber, the door closes and the rat receive a foot shock. Rats are tested 24 to 96 hours later, in the same manner as training but they receive no foot shock. The time it takes to enter the darker chamber is recorded and the critical dependent variable is the difference in latency to enter the darker chamber before and after inhibitory avoidance training. 44

To make sure that a treatment (drug or electrical stimulation) influences memory consolidation mechanisms, and not acquisition or retrieval processes, researchers have administered treatment after training. Many studies have used post-training treatments to show that the amygdala is involved in memory consolidation (Breen & McGaugh, 1961;

Ellis & Kesner, 1983; Petrinovich, Bradford, & McGaugh, 1965). It has also been demonstrated that the amygdala influences consolidation of long-term, and not of immediate, memory because the effect of post-training treatments could be observed when rats were tested at least 24 hours after training and not a few hours after (Barros,

Pereira, Medina, & Izquierdo, 2002; Bianchin, Mello e Souza, Medina, & Izquierdo,

1999; Schafe & LeDoux, 2000).

It now appears that it is the basolateral nucleus of the amygdala, and not its central nucleus, that modulates memory consolidation (DaCunha, Roozendaal,

Vazdarjanova, & McGaugh, 1999; Parent & McGaugh, 1994; Tomaz, Dickinson-Anson,

& McGaugh, 1992). The extensive evidence that post-training treatment in the basolateral nucleus of the amygdala influences memory for many types of training2 strongly suggests that the amygdala is not the locus where emotional memories are stored. Rather, the basolateral nucleus of the amygdala regulates memory consolidation in other brain areas (McGaugh, 2004a).

Epinephrine and Norepinephrine

Epinephrine (or adrenaline) is a hormone that is normally released by the adrenal gland after the occurrence of an event that is stressful enough to arouse the sympathetic

2 Post-training treatment in the basolateral nucleus of the amygdala has effects on memory tasks that have been shown to depend critically on the integrity of other brain structures, such as cued fear conditioning (Schafe & LeDoux, 2000), radial and water maze cued and spatial training (Packard, Cahill, & McGaugh, 1994; Packard & Chen, 1999). 45 nervous system. Norepinephrine is also a hormone released by the adrenal gland, but when in the central nervous system it acts as a neurotransmitter. Both epinephrine and norepinephrine enhance memory (McGaugh, 2004a; Mclntyre, Hatfield, & McGaugh,

2002). However, after lesioning the stria terminalis, an important efferent pathway from the amygdala to basal forebrain, Liang and McGaugh (1983) did not observe the memory enhancing effect of epinephrine they were expecting. This study was the first to give rise to the suggestion that the effect of epinephrine on memory might implicate the amygdala.

Numerous studies now support the involvement of the amygdala in the memory enhancing effect of epinephrine. For example, when the amygdala is lesioned, rats do not benefit from administration of epinephrine (Cahill & McGaugh, 1991). They do not benefit either from epinephrine when they receive intra-amygdala post-training injection of a B-adrenoreceptor antagonist (propranolol), (Liang, Juler, & McGaugh, 1986). In the same vein, many studies have reported enhanced memory after post-training injection of norepinephrine or of fl-adrenoreceptor agonist4 (clenbuterol) in rats' amygdala (Ferry & McGaugh, 1999; Hatfield & McGaugh, 1999; Introini-Collison,

Miyazaki, & McGaugh, 1991; Liang, McGaugh, & Yao, 1990). Similar results have been obtained after post-training administration of ai-adrenoreceptor antagonist

(prazosin: memory impairment) or ai-adrenoreceptor agonist (phenylephrine: memory enhancement) in rats' basolateral amygdala-nucleus (Ferry, Roozendaal, & McGaugh,

1999).

3 An antagonist is a drug that binds to a cell receptor and blocks its action. 4 An agonist is a drug that binds to a cell receptor and triggers an action, 46

Recent findings suggest that epinephrine affects memory first by activation of the

B-adrenoreceptors on the vagus nerve, which projects to the nucleus of the solitary tract.

The nucleus of the solitary tract provides norepinephrine activation in the amygdala

(Liang, 2001; Packard, Williams, Cahill, & McGaugh, 1995; Williams & Clayton, 2001;

Williams & McGaugh, 1992). Because rats in which higher levels of norepinephrine are found after inhibitory avoidance training have better performance, noradrenergic activation in the amygdala appears to play an important, if not crucial, role in memory consolidation (McGaugh, 2004a; Mclntyre, Hatfield, & McGaugh, 2002).

Cholinergic Influences

Memory consolidation is also affected by activation from the neurotransmitter acetylcholine in the amygdala. Indeed, lesion of the stria terminalis abolishes the memory-enhancing effect of cholinergic drugs (Introini-Collison, Arai, & McGaugh,

1989). As with norepinephrine, researchers have investigated the effects of post-training amygdala infusion of muscarinic cholinergic agonists and antagonists. It has been found that muscarinic cholinergic agonists enhance performance (on many tasks), but antagonists impair it (Introini-Collison, Dalmaz, & McGaugh, 1996; Passani et al., 2001;

Power, Vazdarjanova, & McGaugh, 2003; Schroeder & Packard, 2002). Acetylcholine has also been shown to be released in the amygdala during training. Gold (2003) and

Mclntyre, Marriot and Gold (2003) have found that acetylcholine levels in the amygdala

increase as rats perform a spontaneous alternation task and that this increase is correlated with success on the task. 47

Glucocorticoids

After an arousing or stressful event, the adrenal cortex secretes not only epinephrine, it also releases another hormone, the glucocorticoid corticosterone, through the action of the hypothalamic-pituitary-adrenal axis (HP A). Activation of the HP A engages a cascade of hormones (Francis & Meaney, 1999). The hypothalamus first releases corticotrophin releasing factor (CRF), which initiates the liberation of adreno- corticotrophin hormone (ACTH) from the pituitary, which triggers the adrenal cortex to release glucocorticoids (Cortisol in humans, costicosterone in rats). Corticosterone crosses the blood-brain barrier and activates glucocorticoid receptors. The amygdala contains two types of receptor that glucocorticoids can bind to: mineralocorticoid and glucocorticoid receptors (Allen & Allen, 1974). When glucocorticoids (for example dexamethasone, a synthetic glucocorticoid) are administered following training, memory consolidation is enhanced (Hui et al., 2004; Lupien & McEwen, 1997; Sandi,

Loscertales, & Guaza, 1997).

The basolateral nucleus of the amygdala seems to mediate the effect of glucocorticoids on memory. After lesion of this nucleus, dexamethasone does not enhance memory any more (Roozendaal & McGaugh, 1996). Similarly, posttraining infusion of a glucocorticoid agonist (RU28362) in the basolateral amygdala enhances memory (Roozendaal & McGaugh, 1997).

The effect of glucocorticoids on memory appears to involve noradrenergic activation within the amygdala. Brain stem nuclei like the nucleus of the solitary tract have noradrenergic projections to the amygdala. Roozendaal, Williams and McGaugh

(1999) have demonstrated that when a glucocorticoid agonist is infused in the nucleus of the solitary tract, inhibitory avoidance learning is enhanced. However, if a 13- 48 adrenoreceptor agonist is injected into the basolateral amygdala the enhancement caused by the glucocorticoid agonist is blocked.

Cholinergic activation within the basolateral amygdala also seems to be involved in the memory enhancing effect of glucocorticoids. For example, if a cholinergic antagonist (atropine) is injected in the basolateral amygdala, the memory enhancing effect of dexamethasone (a synthetic glucocorticoid) or of a glucocorticoid agonist

(RU28362) will be blocked (Power, Roozendaal, & McGaugh, 2000).

Interaction of the Basolateral Amygdala with other Brain Structures

Norepinephrine, acetylcholine and glucocorticoids have converging action in the basolateral amygdala to modulate memory consolidation. There is more and more evidence that activation of the basolateral amygdala modulates memory consolidation in other brain regions (Figure 5).

The amygdala projects directly to the caudate (via stria terminalis) and directly and indirectly to the hippocampus (Petrovitch, Canteras, & Swanson, 2001; Pitkanen,

2000). As discussed previously, it has been shown that lesions of the stria terminalis block the memory-enhancing effect of epinephrine (Liang & McGaugh, 1983) and of cholinergic drugs (Introini-Collison, Arai, & McGaugh, 1989). However, lesions of the stria terminalis also disrupt the memory-enhancing effect of infusion of a cholinergic agonist (oxotremorine) in the caudate nucleus (Packard, Introini-Collison, & McGaugh,

1996). 49

^ ! ,«Jr N-'-m.i:rtex j loXfMIII-il-Mj

v, 1 Hi|'|)or.r-impus j

! f ~~~ """> \ ^ C-..i.i«itri nucleus 1 BasoMteral .-uiiyQfl.il'i V, Otnc-i Uciin regions j

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Figure 5. Schematic representation of the current neurobiological understanding of emotional arousal's enhancing effect on memory. Emotional arousal induces the release of adrenal hormones (epinephrine and glucocorticoids). This in turns activates sustained release of noradrenaline in the basolateral amygdala. This amygdala activation helps memory consolidation by influencing neuroplasticity in regions involved in memory. From "Memory—a century of consolidation", by J. L. McGaugh, 2000, Science, 287, p.249. Copyright by AAAS, Reprinted with permission.

In well-designed experiments, Packard and colleagues (Packard, Cahill, &

McGaugh, 1994; Packard & Teather, 1998) have shown that when rats trained in the water maze (rats have to swim to find a submerged and invisible platform) were infused posttraining with amphetamine in the caudate, memory for visual cues was selectively enhanced. When the amphetamine was infused into their dorsal hippocampus, was enhanced. However, when the infusion was in the amygdala, both types of memory were enhanced. Additionally, when the hippocampus or the caudate was inactivated (with lidocaine, a local anesthetic) before testing, spatial or was impaired, respectively. Importantly, inactivation of the amygdala prior to testing did not block either type of memory. These results imply that memory processing going on 50 in the caudate and in the hippocampus is significantly influenced by amygdala efferences, but that the amygdala is not the site of memory.

The basolateral amygdala influences hippocampal neuroplasticity (Abe, 2001). It has been demonstrated that electrical stimulation of the basolateral amygdala enhances long term potentiation5 in the dentate gyrus of the hippocampus (Ikegaya, Saito, & Abe,

1995; Ikegaya, Saito, & Abe, 1994). Even if it has not been established what are the specific pathways that connect the basolateral amygdala with the hippocampus, these results clearly indicate that modifying amygdala activity modulates hippocampal neuroplasticity (McGaugh, 2004a).

Reconsolidation

A discussion of the neurobiological underpinnings of the influence of emotion on memory would be incomplete without referring to reconsolidation. Nader and colleagues

(2000a; 2000b; 2004) have demonstrated that when consolidated fear memories are reactivated (by retrieval) they become fragile, or prone to forgetting, and undergo reconsolidation (where protein synthesis is required). If anisomycin (a protein synthesis inhibitor) is infused in the lateral and basal nuclei of the amygdala shortly after a memory test, will be observed in future tests of this memory.

These findings do not fit into the traditional view of consolidation. In this view, memories have a linear history: they are first in a labile, fragile state (in short-term memory) and with time they become more stable (long-term memory) (Hebb, 1949;

McGaugh, 2000). Instead, Nader and colleagues' (2000a; 2003) findings suggest that when fear memories are retrieved (reactivated), they require protein synthesis in the

5 Long term potentiation is a modification of synaptic function, associated with learning: after repetitive high frequency electrical stimulation, higher amplitude of synaptic potential to a single pulse will be observed. 51 lateral and basal nuclei of the amygdala to be stabilized or to remain accessible later.

Each time retrieval takes place, reconsolidation occurs.

One of reconsolidation's most promising applications seems to be in the treatment of post-traumatic stress disorder. Indeed, it might be possible to treat individuals suffering from post-traumatic stress disorder by reactivating their in specific conditions. Also, reconsolidation processes are a potential hopeful avenue to understand the relationship between learning and forgetting (Nader, Schafe, &

LeDoux, 2000b).

Emotional Memory in Humans

In humans too, emotionally arousing events, like witnessing a crime or having a surprise birthday party, tend to be well remembered. In humans, as in nonhuman animals, emotionally arousing events trigger a cascade of hormones and neurotransmitters. And in humans too, the amygdala appears to play a pivotal role in enhancing memory for emotional events. As I did for nonhuman animals, I will now review the scientific literature concerning the role that endogenous substances, like adrenaline and Cortisol, play in emotional memory. I will also present findings, obtained in patients with bilateral or unilateral amygdala lesions, that indicate the amygdala's importance in enhancing memory for emotional information. Finally, I will show how functional neuroimaging investigations of emotionally influenced memory are tremendously important for understanding how memory for emotional information differs from memory for nonemotional events. 52

Adrenergic Influences

As seen in the previous section about emotional memory in nonhuman animals, there is substantial evidence that enhanced memory for emotional experience results, in part, from adrenergic activation. In humans, Cahill, Prins, Weber and McGaugh (1994) were the first to demonstrate that better memory for arousing information also involves the hormone adrenaline. They gave subjects either a placebo or propanolol (a 13- adrenergic antagonist) one hour before viewing an emotional or a neutral story. Memory for the story was tested a week later. In the neutral-story condition, recall was equivalent in the placebo and propanolol groups. However, in the emotional-story condition, placebo subjects recalled more story elements than subjects who were given propanolol.

Because propanolol did not modify subjective emotional reactions subsequent to story presentation, and it selectively impaired memory for the emotional story, Cahill et al.

(1994) concluded that in humans storage of emotionally arousing information involves

B-adrenergic receptors.

Supporting the previous findings, O'Carroll, Drysdale, Cahill, Shajahan and

Ebmeier (1999) found that administration of yohimbine (a B-adrenergic agonist) increased memory for an emotionally arousing story when tested one week later, relative to a placebo group. They gave another group metropobol (B-adrenergic antagonist) and memory for the arousing story was impaired relative to the yohimbine and the placebo groups.

Soetens, Casaer, D'Hooge and Hueting (1995) found that pre and post-learning injection of amphetamine (drug stimulating the adrenergic system) ameliorates the long- term retention of unrelated word lists. Because only long-term and not short-term 53 memory was better after amphetamine injections, it was concluded that amphetamine influenced memory consolidation processes. Cahill and Alkire (2003) also found evidence of adrenergic implication in the modulation of memory consolidation. They gave subjects infusion of saline or epinephrine immediately after they had viewed a series of relatively neutral pictures. Subjects who had received epinephrine infusion had better memory for the pictures than subjects who had received the saline. These findings demonstrate that human long-term memory consolidation is enhanced when a stress hormone is released.

From the previous findings, it is not clear whether these memory modulating effects involve peripheral or central adrenergic receptors. In 1998, van Stegeren,

Everaerd, Cahill, McGaugh and Gooren compared the memory for emotional and neutral picture stories in subjects who were given either a placebo, propanolol or naldonol.

Propanolol is a B-adrenergic antagonist that can cross the blood-brain barrier and act on central and peripheral B-adrenergic receptors. Naldonol is also a B-adrenergic antagonist, but unlike propanolol, does not cross the blood-brain barrier easily and acts mostly on peripheral receptors. It was found that only propanolol, and not naldonol, impaired memory for the emotional story. This suggests that central B-adrenergic receptors are involved in the memory of emotional information.

Recent findings indicate that gender should also be considered in theories of emotionally influenced memory. Cahill and van Stegeren (2003) have found a sex- related impairment of emotional memory after B-adrenergic blockade. They reanalyzed data previously published (Cahill, Prins, Weber, & McGaugh, 1994; van Stegeren,

Evaraed, Cahill, McGaugh, & Goeren, 1998) and found that in men, propanolol impaired memory for central and not for peripheral information of an emotional story. In 54 women, the deficits were in the opposite direction: propanolol impaired memory for peripheral details and not for central parts of the emotional story.

Further, in a functional magnetic resonance imaging (fMRI) study, Strange and

Dolan (2004) found that successful encoding of emotional, not of neutral, words increased amygdala activation during encoding. Words that led to more amygdala activation during encoding evoked greater hippocampal activation during retrieval.

Administration of propanolol during encoding abolished the amygdala response at encoding and the hippocampus activation at retrieval. Thus, it appears that these amygdala and hippocampal activations at encoding and retrieval of emotional words require B-adrenergic stimulation during encoding.

However, how can substances associated with arousal that do not cross the blood-brain barrier (i. e., adrenaline, amphetamines) influence memory? Because of evidence in the rat literature that epinephrine affects memory primarily by activation of

B-adrenoreceptors on the vagus nerve (Liang, 2001; Packard, Williams, Cahill, &

McGaugh, 1995; Williams & Clayton, 2001; Williams & McGaugh, 1992), Clark,

Naritoku, Smith, Browning and Jensen (1999) tested memory of human subjects following vagal nerve stimulation. Vagal nerve stimulation is used to suppress intractable epileptic seizures. Subjects had to read paragraphs in which some words were highlighted. Half of the subjects received vagal nerve stimulation after reading the paragraphs and the other half received sham stimulation. Subjects who received vagal nerve stimulation had better memory for the highlighted words than subjects who received sham stimulation. This study demonstrates that in humans, as in rats, peripheral substances can affect learning via vagal nerve afferents. 55

Glucocorticoids

There is abundant evidence that the glucocorticoid Cortisol (a hormone) also plays a modulating role in human emotional memory (Lupien et al., 2005). Enhancing and impairing effects are reported. It seems that the effects of Cortisol on memory vary according to the mnesic process involved and the arousing dimension of the information to be remembered.

When endogenous Cortisol levels are increased before encoding, memory for emotional information is generally enhanced. Buchanan and Lovallo (2001) were the first to conduct an experiment with human subjects where Cortisol was administered before encoding. They found that memory for emotionally arousing pictures was better than memory for neutral pictures in the subjects who were given the Cortisol before encoding. Similar enhancement of memory for arousing compared to neutral pictures was obtained when pre-learning Cortisol elevation was caused by cold pressor stress6

(Cahill, Gorski, & Le, 2003). In the same vein, Maheu, Joober, Beaulieu and Lupien

(2004) have demonstrated that when metyrapone (a corticosteroid synthesis inhibitor) is administered before the incidental encoding of a story made of neutral and emotional parts, memory (tested a week later) for both neutral and emotional sections of the story is impaired. Abercrombie, Kalin, Thurow, Rosenkranz and Davidson (2003) also found enhanced memory for arousing and nonarousing pictures when Cortisol was given before encoding.

When endogenous Cortisol levels are increased before retrieval, memory performance is generally impaired, and again emotional information seems more

6 Cold pressor stress is a task in which a subject's arm is immersed in ice cold water for up to three minutes. 56 vulnerable to its effects. In a landmark study, de Quervain, Roozendaal, Nitsch,

McGaugh and Hock (2000) have demonstrated that cortisone administered one hour before a delayed test impairs performance. However, when cortisone was administered immediately before or after encoding it did not influence memory. The de Quervain et al. (2000) study only involved neutral information but more recent studies show evidence that when Cortisol levels are increased before the memory test, either by pharmacological or psychosocial manipulations (i.e., asking participants to give a five- minute speech on personal strengths and weaknesses in front of a committee) memory deficits are more pronounced for arousing than for nonarousing information (Kuhlmann,

Kirschbaum, & Wolf, 2005; Kuhlmann, Piel, & Wolf, 2005). However, two studies have reported more important deficits for neutral compared to unpleasant information (Jelicic,

Geraerts, Merckelbach, & Guerrieri, 2004; Tops et al., 2003). The fact that these authors tested memory immediately after encoding might explain this discrepancy. Time of day when subjects were tested (because of the circadian rhythm of Cortisol: peak in the morning and nadir in late afternoon) and subject gender might also explain the discrepancies.

These findings indicate that Cortisol can influence memory formation during acquisition, consolidation and retrieval. These effects seem more important if the information is emotionally arousing. An arousing event or arousing learning condition will cause adrenergic activation which, through interaction with the increased circulating

Cortisol, will result in increased encoding and/ or consolidation. This interaction between corticosteroids and adrenergic mechanisms is thought to occur in the amygdala and hippocampus. Two types of glucocorticoid receptors are found in the amygdala: mineralocorticoid (MR) and glucocorticoid (GR). MR have more affinity with Cortisol 57 than GR (Reul & de Kloet, 1985), but GR activation is necessary for long-term memory consolidation (de Kloet, Oitzl, & Joels, 1999; Sandi, 1998). When the brain is in this

"consolidation mode", retrieval is impaired (Roozendaal, 2002). Thus retrieval impairments in stressful events such as job interviews and oral examination become more readily understandable.

Amygdala and Emotional Memory

It has long been suspected that the amygdala plays a key role in emotional and memory processing (e.g., Aggleton, 1992) and the first indication that the amygdala could have a significant role in human emotional memory was obtained many years ago.

Stimulation of the amygdala in temporal lobe epilepsy patients induced the re- experiencing of personal events that have a strong emotional meaning (Chapman,

Walter, Markham, Rand, & Crandall, 1967; Gloor, Olivier, Quesney, Andermann, &

Horowitz, 1982; Heath, Monroe, & Mickle, 1955). It was also found that subjects surgically implanted with depth electrodes have increased firing in amygdala neurons when they recall emotional events (Halgren, 1992).

It is now generally accepted that memory involves multiple systems that necessitate distinct but interacting brain areas (Squire & Knowlton, 2000). Two medial temporal-lobe systems are thought to be involved in emotionally influenced memory: the nondeclarative and the declarative system (Phelps, 2004). The nondeclarative system relies primarily on the amygdala, for example in fear conditioning (in which a neutral stimulus becomes aversive after being paired with an unpleasant event). However, the declarative system also depends on the hippocampus, for example when subjects remember better the arousing part of a story. 58

Evidence that these memory systems, which can involve emotions, were dissociated was provided by Bechara et al., (1995). They studied nondeclarative and declarative learning in individual patients with distinct brain lesions. One patient had bilateral amygdala damage and another had bilateral hippocampal damage. They found that the patient with amygdala damage had intact declarative knowledge for the conditioning contingencies (e.g., he knew that a blue square (conditioned stimulus, CS) predicted a loud sound (unconditioned stimulus, US)) but did not demonstrate the expected nondeclarative learning (e.g., he did not show a larger skin conductance response when re-presented with the blue square (conditioned response, CR)). However, the patient with bilateral hippocampal lesions showed the opposite pattern of learning.

He could not report that the CS predicted the US, but he showed the expected CR.

Bilateral Amygdala Lesion and Declarative Emotional Memory

These findings suggest that the two memory systems operate independently. It has long been believed that the amygdala was mostly, if not exclusively, involved in nondeclarative emotional memory. That belief has been convincingly refuted with a series of studies showing impaired declarative memory for emotional information.

First, Markowisch and collaborators (1994) showed that two individuals with

Urbach-Wiethe disease7 (UWd) were impaired in memory for emotional pictures and words. Second, Cahill, Babinsky, Markowitsch and McGaugh, (1995) demonstrated that a UWd patient did not show the expected memory enhancement for the emotional part of a narrated emotional story accompanied by matching pictures. With another UWd individual, Adolphs, Cahill, Schul and Babinsky (1997) replicated this finding. Finally,

7 UWd (or lipoid proteinosis) is a rare genetic disorder characterized by deposits of hyaline (translucent) material on the skin, oral mucosa and pharynx. Half of the UWd cases also have deposits in the medial temporal lobe that can affect the amygdala selectively. 59

Phelps and collaborators (1998) found that a woman with bilateral amygdala damage was impaired not only in fear conditioning but also in the recognition of arousing words.

In these four studies, the declarative memory deficits were restricted to the absence of memory enhancement for emotional material (story, pictures or words) and patients had selective amygdala damage. Moreover, patients' memory for neutral information and their emotional reactions to the memory items did not differ from that of healthy participants.

This suggests that the amygdala's activity is more important in boosting memory of emotionally arousing information than in generating emotional reactions. Amygdala damage does not grossly impair emotional declarative memory; it eliminates the memory enhancement normally observed with emotional or physiological arousal

(Phelps, 2006). Consequently if the hippocampus, and not the amygdala, is damaged, one should expect impaired declarative memory only and not a reduction in the enhancement of memory for emotionally arousing information. This prediction was tested and confirmed in two experiments. Patients with amnesia of diverse aetiology

(never including amygdala damage) were presented with emotionally arousing or neutral pictures or with an illustrated and narrated story comprising emotional and neutral sections. Emotional arousal enhanced recall of the arousing pictures and story sections in a proportional way in amnesics and healthy individuals (Hamann, Cahill, McGaugh, &

Squire, 1997; Hamann, Cahill, & Squire, 1997).

Because amygdala pathology happens in the early stages of Alzheimer's disease

(AD) (Chow & Cummings, 2000), it should not be surprising to find impairments in the declarative emotional memory of patients suffering from AD. Some researchers have reported preserved enhancement in memory for an emotional story (Kazui et al., 2000; 60

Moayeri, Cahill, Jin, & Potkin, 2000), while others show impaired enhancement in the memory of negative pictures (Hamann, Monarch, & Goldstein, 2000). In a study of AD patients who experienced an emotionally arousing event, the Kobe earthquake, a significant correlation between amygdala volume (measured by magnetic resonance imaging) and memory for the earthquake was uncovered (Mori et al., 1999). This suggests that when sufficient amygdala pathology is present, AD patients will experience deficits in emotional declarative memory.

Unilateral Amygdala Lesions and Emotional Memory

Considerable knowledge on the biological bases of memory has been gathered with postsurgical studies of patients who have undergone unilateral resection from the medial temporal lobe for the relief of intractable epileptic seizures. Patients with unilateral medial temporal-lobe damage have been found to show subtle material specific memory deficits (Milner, 1965, 1970). Studying patients with brain lesions is crucial to understand the relationship between brain regions and cognitive functions.

However, because bilateral amygdala lesions are a rare occurrence and bilateral medial temporal lobe lesions give rise to amnesia (Milner, 1968; Scoville & Milner, 1957), which adds confusion to the discussion of the selective role of the amygdala for emotionally influenced memory, studies of patients with a unilateral lesion is highly informative. In the following section, I will review the literature concerning the effects of unilateral medial temporal-lobe resection, including the amygdala, on declarative emotional memory.

In the first study of declarative emotional memory in patients with a surgical resection including the amygdala, Phelps, LaBar and Spencer (1997) found no difference 61 between control subjects and patients. They asked subjects to rate how negative or positive were each word of a series (nine negative, nine positive and nine neutral) and submitted subjects to a surprise recall one minute after incidental encoding. All groups had better memory for the negative and positive than the neutral words. This finding suggested that an intact amygdala was not necessary to remember emotional information and points to the obvious fact that other brain areas are involved in episodic emotional memory. This result should not be overly surprising given that no subject exhibited increased skin conductance to the emotional words and that memory was tested only one minute after encoding. Enhancement in memory for emotionally arousing information is f known to require longer retention intervals (Kleinsmith & Kaplan, 1963, 1964; Park &

Banaji, 1996). Moreover the emotional dimension of this task was more semantic than arousing. This semantic component might have given subjects an additional organizational strategy that benefited their memory (Talmi & Moscovitch, 2004). A year later, LaBar and Phelps (1998) presented their subjects with words that were either neutral or arousing and memory was tested twice. The first surprise free recall test took place immediately after encoding and the second test was one hour after encoding. They found that despite equivalent ratings of arousal to the words, patients with resection including the left or the right amygdala did not remember arousing words better than the neutral ones after the longer retention interval.

In the subsequent set of studies about the impact of unilateral amygdala damage on enhanced memory for emotional information, researchers changed their experimental paradigm. Subjects were presented a series of 12 pictures accompanied by a narrated story (the "Heuer and Reisberg" story of a little boy going to visit his dad at work) or a 62 series of unrelated arousing and nonarousing pictures accompanied by descriptive narrated sentences. The encoding was always incidental and memory was tested after a longer retention interval (the retention interval was longer than the one used in the first studies about the impact of amygdala damage on memory for emotional information (see previous paragraph), e. g., after two hours, a day or a week). The common finding of these studies was that patients with unilateral amygdala lesions did not show enhanced memory of arousing compared to nonarousing information. Also, they reported that patients with lesions of the left amygdala did not show memory enhancement for these arousing stimuli (Adolphs, Tranel, & Denburg, 2000; Brierley, Medford, Shaw, &

David, 2004; Buchanan, Denburg, Tranel, & Adolphs, 2001; Frank & Tomaz, 2003).

A recent study using the same experimental paradigm ("Heuer and Reisberg" story, and memory test a week after incidental encoding) suggests that the time at which the amygdala damage occurred may be as important as the side of damage in eliminating the memory enhancement. Shaw, Brierley and David (2005) found that only patients who had amygdala damage early in life (their excised amygdala had neuroradiologic features of dysembryoplastic neurepithelial tumor) and not patients who had amygdala damage in adulthood (their excised amygdala was histopathologically normal) lost the ability to remember better emotionally arousing over nonarousing information. This finding led these authors to suggest the existence of a critical period in the development of amygdala functions.

Because the enhancement of memory in emotionally arousing situations has been found to differ for gist and detail information (enhancement for gist and suppression for detail) (Burke, Heuer, & Reisberg, 1992; Christianson & Loftus, 1987, 1991), it has 63 been hypothesized that the amygdala also plays a mediating role in gist memory. Two groups investigated this question by asking a subject (SM) with bilateral amygdala lesions and patients with unilateral amygdala damage to incidentally encode pictures accompanied by a narrative. The memory test took place the following day and it included questions about gist and detail information related to each of the previously seen pictures. In the first study (Adolphs, Denburg, & Tranel, 2001), it was found that all subjects except SM displayed better gist memory for aversive than for neutral pictures. In the second study Adolphs, Tranel and Buchanan (2005) found that only healthy or brain damaged individuals (damage not including the amygdala) and not patients with amygdala damage (SM and left or right unilateral medial temporal lobe resection) had superior gist memory for emotional pictures. In fact, patients with amygdala damage showed the reversed pattern of memory: they were more accurate in gist memory of neutral than emotional information. Additionally, a correlation between gist memory and amygdala volume was found but the correlation between gist and the hippocampus volume was not significant.

Most of the previous investigations about the amygdala's influence in the enhancement of emotionally arousing stimuli have been consistent with a modulating role during memory consolidation. However, it is clear that episodic memory performance can be affected in any of its three components: encoding, consolidation or retrieval. The preceding work showing specific memory impairment of an emotional event's gist suggests that the amygdala is involved in the narrowing of attention when encoding an emotional event (Phelps, 2006). Earlier work conducted in another patient

(SP) with bilateral amygdala damage and in patients with unilateral damage suggests 64 that the amygdala is involved in perceptual encoding by allowing emotional events to reach awareness. During an-attentional blink paradigm8, Anderson and Phelps (2001) found that SP and patients with left amygdala damage did not show enhanced identification of negative relative to neutral words.

Finally, the work of Richardson, Strange and Dolan (2004) (which LaBar and

Cabeza (2006) termed an "experimental tour de force") must be mentioned. Richardson,

Strange and Dolan (2004) showed that encoding of emotional memories depends both on the amygdala and hippocampus and on their interactions. They asked patients with left temporal epilepsy (none had resection) to encode neutral and arousing words during functional magnetic resonance imaging (fMRI). The encoding was incidental for each word subjects had to indicate whether it represented a living or nonliving entity. Word recognition was tested 90 minutes later outside the scanner. First, pathology of the left amygdala (according to structural MRI) predicted worse memory for arousing words, less activity in the left hippocampus, but more activity in the right hippocampus.

Second, memory for the neutral words was related only to the degree of hippocampal pathology. Third, pathology of the left hippocampus predicted less activity in the left amygdala but more activity in the right amygdala. This suggests a mutual dependence, or a compensatory shift, between amygdala and hippocampus when remembering arousing words.

After a target is identified, there is a transient impairment in awareness for targets presented subsequently. This impairment in awareness is called the attentional blink. The attentional blink is attenuated for aversive words. Compared with neutral words, aversive words are easier to perceive during the attentional blink (Raymond, Shapiro, & Arnell, 1992). 65

Brain Imaging Studies in Healthy Subjects

Studies with brain damaged patients suggest a clear implication of the amygdala in enhancing memory for emotionally arousing information. However, it is still ambiguous whether these deficits are caused by a lack of modulation from the amygdala to other medial temporal lobe structures important in episodic memory (e.g., hippocampus and parahippocampal gyrus) or to damage of the medial temporal lobe structures surrounding the amygdala (e.g., entorhinal and perirhinal gyri). Functional imaging investigations with healthy subjects are also useful to understand how brain regions interact in processing emotional memories. Now, I will review the neuroimaging findings in healthy subjects related to encoding of emotional information, then I will introduce the findings indicating a gender difference in the processing of emotional memories and finally I will present findings related to retrieval of emotional information.

Encoding of Emotional Memory

The first neuroimaging investigation of enhanced declarative memory for emotional information used positron emission tomography (PET). Cahill et al. (1996) scanned subjects while they were incidentally encoding a series of emotionally arousing

(more unpleasant) or neutral short movies. Subjects' memory was tested with a free recall test three weeks later. Researchers found that right amygdala activation when subjects viewed the arousing films was highly correlated with the number of arousing films remembered. However, no correlation was found between amygdala activation when viewing nonarousing films and their subsequent delayed recall (Figure 6). Further, 66 when amygdala activation to emotional clips was compared (by subtraction) to the activation to neutral movies, no difference was found.

Emotional Film Session B Neutral Film Session 12"

10- r«0.33 (n,s.) 8-

6- M 4- • • • 2*

0- • • —1 » i • i 0,8 0.4 0.8 0.8 1.0 Bight amygdala glucose Eight amygdala glucose

Figure 6. Amygdala activity while watching emotionally arousing films correlates with long-term recall of the films. No correlation is found between amygdala activity when viewing nonemotionally arousing films (neutral) and their long-term recall. From "Amygdala activity at encoding correlated with long-term, free recall of emotional information", by L. Cahill, R. J. Haier, J. Fallon, M. T. Alkire, C. Tang, D. Keator, J. Wu, and J. L. McGaugh, 1996, PNAS, 93, p. 8019. Copyright by L. Cahill. Adapted with permission.

In the next PET study of this effect, Hamann, Ely, Grafton and Kilts (1999) scanned subjects during incidental encoding of pleasant, unpleasant, interesting and neutral pictures. They found that recognition memory, tested four weeks after encoding, was enhanced for pleasant, unpleasant and interesting pictures relative to neutral pictures. Importantly, they found that bilateral amygdala activity during encoding of pleasant and unpleasant pictures was positively correlated with their enhanced recognition. No relation was found between amygdala activity during encoding of neutral and interesting items and their subsequent memory. This study extended Cahill et al.'s (1996) findings by demonstrating that amygdala activation can enhance memory for arousing information of positive and negative valence. 67

Further support in favor of the memory modulating role of the amygdala was found in subsequent fMRI studies. Canli, Zhao, Desmond, Glover, & Gabrieli (1999) found that greater activity of the left amygdala during encoding was associated with enhanced memory (tested 2 to 14 months later) for negative pictures. In an event-related fMRI study, Canli, Zhao, Brewer, Gabrieli and Cahill (2000) then showed that subjective rating regarding how emotional subjects found each picture during encoding is important. Activation of the left amygdala during encoding predicted memory for the pictures (that could be either positive or negative) rated as more emotional. The more emotional a picture was rated, the more important was the correlation between left amygdala activity and recognition performance 3 weeks later.

According to Dolcos, LaBar and Cabeza (2004a; 2004b) the previous studies do not tell us why emotionally arousing items are remembered better than nonarousing information. A more informative analysis would be to examine brain activity according to the "subsequent memory paradigm" (Paller & Wagner, 2002). In this paradigm, brain activity during encoding is analyzed according to whether items are forgotten or remembered in a subsequent memory test. Larger brain activity detected for remembered than for forgotten items is known as the DM effect (difference due to memory; hits- misses). Dolcos, LaBar and Cabeza (2004a; 2004b) compared the DM for emotional pictures (positive and negative) to the DM for neutral pictures to see which brain regions were more involved in the successful encoding of emotional pictures. They found that the emotional DM was greater than the neutral DM in the amygdala bilaterally, in the hippocampus head and in the entorhinal cortex. Moreover, they found evidence of a double dissociation along the axis of the medial temporal lobe. The emotional DM was 68 more important in the anterior portion of the medial temporal lobe (hippocampus head and entorhinal cortex) and, conversely, the neutral DM was more important in the posterior portion of the medial temporal lobe (hippocampus tail and parahippocampal gyrus). This is consistent with anatomical reports of rich interconnection between the amygdala and the anterior hippocampus and entorhinal cortex (Amaral, Price, Pitkanen,

&Carmichael, 1992).

It is clear that the amygdala and the medial temporal lobe do not function in isolation. The prefrontal cortex plays an important role in emotional evaluation of stimuli (Davidson & Irwin, 1999; Phan, Wager, Taylor, & Liberzon, 2002), and more important DM to arousing than to neutral pictures has been found in the left dorsolateral and ventrolateral prefrontal cortex (Dolcos, LaBar, & Cabeza, 2004a). Submitting the data of Cahill et al. (1996) to structural equation modelling, Kilpatrick and Cahill (2003) found increased influences (functional connectivity) of the amygdala in the ipsilateral parahippocampal gyrus and in the ventrolateral prefrontal cortex during the emotional relative to the neutral movies (I point out that no difference in amygdala activation was found after subtraction of neutral movies from the emotional condition in the original

Cahill et al. (1996) study). In an fMRI experiment where subjects had to encode and retrieve neutral, negative nonarousing or negative arousing words, Kensinger and Corkin

(2004) found distinct neural networks for the enhancement of memory for words that differed in arousal. The memory advantage for arousing words was supported by increased activity in the left amygdala and left hippocampus whereas the memory boost for nonarousing negative words involved the left hippocampus and the left ventrolateral prefrontal cortex. 69

Gender Differences in Encoding of Emotional Memory

Researchers have been puzzled by the initial findings of enhanced amygdala activity to successfully remembered emotional items. Some studies reported increased activity of the right amygdala (Cahill et al., 1996; Kilpatrick & Cahill, 2003) and others of the left amygdala (Canli, Zhao, Brewer, Gabrieli, & Cahill, 2000; Canli, Zhao,

Desmond, Glover, & Gabrieli, 1999). It was proposed and demonstrated that this hemispheric difference in the amygdala activation was a function of subject gender.

With PET and fMRI investigations it was revealed that even if men and women's memory for emotional information is usually equivalent, the activity measured in their

amygdala is not. These studies indicate a preferential implication of the left amygdala in women and a preferential involvement of the right amygdala in men for memory of

emotionally arousing information (Cahill et al., 2001; Cahill, Uncapher, Kilpatrick,

Alkire, & Turner, 2004; Canli, Desmond, Zhao, & Gabrieli, 2002). This difference might be explained with the finding of a differential functional connectivity of men and

women's amygdala in a resting condition. Kilpatrick, Zald, Pardo and Cahill (2006)

analyzed amygdala activation of men and women in the resting condition of multiple

PET experiments. They found that men's right amygdala was associated with a greater

functional connectivity than women's right amygdala but that women's left amygdala

was associated with more functional connectivity than men's left amygdala. Moreover,

the areas showing more connectivity with men's right amygdala (sensorimotor cortex,

striatum, pulvinar) and women's left amygdala (subgenual cortex, hypothalamus) were

not the same. .70

Retrieval of Emotional Memory

Because the amygdala has classically been seen as playing a role in encoding and consolidation, research about its implication during retrieval of emotional information is relatively new.

The first neuroimaging investigation of emotional memory retrieval was conducted in patients suffering from post-traumatic stress disorder (PTSD). Rauch et al.

(1996) scanned patients with PTSD while they were presented with audiotaped scripts describing autobiographic everyday or traumatic experiences. Increased activation in the right amygdala and in the anterior cingulate was found during the presentation of the traumatic compared to the everyday experiences. However, because subjects were only told to imagine what the script was describing, implication of retrieval mechanisms in this task is questionable. Further, the activation obtained in a psychiatric sample is likely to differ significantly from that of healthy subjects and may not be generalizable to healthy subjects.

The first three neuroimaging studies of emotional memory retrieval in healthy subjects made use of a "blocked design"9, and two of them obtained negative findings in the region of interest (medial temporal lobe) (Tabert et al., 2001; Taylor et al., 1998).

Dolan, Lane, Chua and Fletcher (2000) scanned subjects during intentional and incidental recognition of unpleasant and pleasant pictures. Activation of the left amygdala was found after subtraction of incidental recognition from activation during intentional recognition of emotional pictures.

9 PET and early fMRI experiments used a "blocked design" of stimulus presentation, where similar stimuli are presented together, making it difficult to study cognitive processes in which stimuli prediction is important to consider (Buxton, 2002). The temporal resolution of blocked design is too limited to analyze individual stimuli according to subject's emotion rating or memory success or failure. 71

Subsequent studies of retrieval have used event-related designs and can thus answer more specific questions. To investigate successful emotional memory retrieval while controlling for the influence of emotion on perception, a "contextual paradigm" has been used. In this paradigm, neutral targets are encoded in a neutral or in an emotional context (i.e., target= corn, in neutral context= The farm labourers began harvesting the corn: in positive context= The farmer was overjoyed with his bountiful crop of corn; in negative context= The farmer was shredded when he fell into the corn grinder) and at test the neutral targets are presented for recognition. With this paradigm, used with words or pictures, activation to items successfully retrieved from emotional context was found in the amygdala, the insula, the cingulate and other regions in the temporal and frontal neocortex (Kensinger & Schacter, 2005; Maratos, Dolan, Morris,

Henson, & Rugg, 2001; Smith, Henson, Dolan, & Rugg, 2004; Smith, Dolan, & Rugg,

2004).

Emotions not only have an influence on the probability that a target will be remembered, they can also influence the subjective sense of remembering. Recent studies have shown that the feeling of remembering and recollection are enhanced with emotions (Ochsner, 2000; Talarico & Rubin, 2003). Recollection, with familiarity, is one of the two distinct processes underlying recognition according to the dual process theory of recognition (Yonelinas, 2002). This process is typically measured in recognition paradigms by asking subjects to state if they remember or know a recognized item. According to Tulving (1985b), recollection underlies "remembering" answers (in which the remembered stimuli evoke a specific memory linked to a specific spatio-temporal context) and familiarity underlies "knowing" answers (in which stimuli 72 are "known" to have been experienced earlier, without specific contextual information attached to its memory).

Because recollection and familiarity necessitate different cognitive and neural mechanisms (Yonelinas, Otten, Shaw, & Rugg, 2005), researchers have begun to investigate whether the subjective feeling of remembering varies for emotional and neutral memory targets. Sharot, Delgado and Phelps (2004) have scanned subjects one hour after encoding of neutral and emotional pictures and have asked them to make

"remembering" or "knowing" specification during recognition. Dolcos, LaBar and

Cabeza (2005) used a similar experimental paradigm but with a longer retention interval; recognition took place approximately one year after encoding. Both studies reported a larger number of "remembering" responses for recognized emotional pictures. They also reported more right amygdala activation for "remembering" emotional pictures as compared to the other possibilities (emotional "knowing", neutral "remembering" or neutral "knowing"). Interestingly in the Sharot, Delgado and Phelps (2004) experiment,

"remembering" answers to neutral pictures were specifically associated with increased activity in the right parahippocampus. As they explain it, when an individual is making a

"remembering" response to a neutral picture, he or she may rely on the picture's perceptual details to answer, which has been associated with parahippocampal activity

(Cabeza, Rao, Wagner, Mayer, & Schacter, 2001). Conversely, when an individual makes a "remembering" response to an emotional target, he or she relies more on the feeling of arousal that has been linked numerous times to the amygdala (Hamann, 2001;

LaBar & Cabeza, 2006; Phelps, 2004). 73

The neuroimaging findings are not straightforward: some studies find amygdala activation during encoding and others do not, some find amygdala activation during recognition of emotional information and others not. Sergerie, Lepage and Armony

(2006) propose an explanation for this discrepancy. They carried out an event-related fMRI experiment in which subjects were scanned during encoding and retrieval of faces with happy, neutral or fearful expressions. By comparing encoding and retrieval, they uncovered a hemispheric dissociation of amygdala involvement in the different memory stages. Specifically, they found that the right amygdala was more involved in the encoding of emotional information and that the left amygdala was more implicated in its retrieval. However interesting, these results cannot reconcile the previous research because the task they used differed in important ways from the usual experimental paradigm, explaining the different activation they found. For example their encoding was intentional, memory was tested immediately after encoding and the stimuli they used (faces with different expressions) are known to activate the amygdala whether perceived consciously or not (Dolan & Vuilleumeir, 2003; Whalen et al., 1998; Zald,

2003).

Conclusion

Neuropsychological studies of how humans process information have traditionally excluded emotions, as emotions were believed to be the domain of social and clinical psychologists (G. Miller, 2003). There is now increasing evidence that emotions have a powerful influence on cognition and that examining cognition without considering the emotional context will, at best, give limited results (Phelps, 2006). The pivotal role of 74 the amygdala and of stress hormones in enhancing emotional memory found in animal studies has been convincingly shown in humans. However, the question of the role of the amygdala's diverse nuclei is still not established in human emotional memory. Many other questions remain to be answered. Future research should investigate further the influence of emotions on other memory systems (e.g., , procedural) and type of memory information (e.g., nothing is known yet about the influence of emotional arousal on odor memory) and much work is to be done on integrating data obtained with different experimental methodologies into a comprehensive model of emotional memory. 75

3. ODOR MEMORY, AFFECTIVE INFLUENCES AND ITS NEUROANATOMICAL SUBSTRATES

« Mais, quand d'un passe ancien rien ne subsiste. apres la mort des etres, apres la destruction des choses, seules, plus freles mais plus vivaces, plus immaterielles, plus persistantes, plus fideles, l'odeur et la saveur restent encore longtemps, comme des arnes, a se rappeler, a attendre, a esperer, sur la ruine de tout le reste, a porter sans flechir, sur leur gouttelette presque impalpable, l'edifice immense du souvenir. »

- Marcel Proust, A la recherche du temps perdu, (1913)

In the previous sections of this literature review, I have presented cognitive and neurobiological evidence that emotionally arousing stimuli are remembered differentially, most often better, than nonarousing stimuli. According to Marcel Proust, odors are intimately tied to memories, maybe especially so to powerful and emotional ones. For Proust, it was the taste and smell of a little madeleine (a shell-shaped small cake) that resuscitated his childhood memories. Although few among us have written a seven volume book after having had an olfactory triggered memory, most of us have experienced a similar reoccurrence of vivid, emotional and seemingly unforgettable memories; e.g., when unexpectedly smelling the perfume of a parent or a loved one. In the following section, I will offer a comprehensive overview of the current knowledge on odor memory and its relation to affect. First, I will show that multiple memory systems are appropriate to understand the nature of olfactory memory. Second, I will show how odor memory can be influenced by affective factors such as mood, and I will review the literature surrounding the "Proust effect" or how odors can cue emotional declarative memories. To conclude, I will summarize the neurobiological substrates of odor hedonics and memory. 76

Memory Systems and Olfactory Information

Despite the seemingly extraordinary ability of odors to remind us of personal events, the study of odor memory has been neglected compared to memory for visual or auditory information (Richardson & Zucco, 1989). One reason for this relative neglect may be the common misperception that odors are less important to people than sights or sounds (Engen & Hunter, 1982). Nevertheless, there is now an ever-growing number of cognitive experiments on odor memory (Herz & Engen, 1996; Schab & Crowder,

1995b; White, 1998) and, although the question of whether olfactory memory is a separate memory system remains unanswered, odor memory could very well be understood under the multiple memory systems framework (Larsson, 2002). However, according to Stevenson and Case (2005) dissociable memory systems might not be necessary in olfaction. They believe that the current evidence can be understood within a single memory system in which the olfactory memorandum is activated and then slowly decays.

Memory is an indispensable cognitive faculty but not an indissociable one. It is now accepted that memory is constituted of various systems differing in the kind of information they process, the principles by which they function and the neuroanatomical structures supporting them (Squire, 2004). Tulving (1985a) introduced one of the main distinctions within human memory systems; nondeclarative vs. declarative memory.

Whereas declarative memory gives us the capacity of consciously recollecting facts and events, nondeclarative memory is characterized by learning without awareness and manifests itself through changes in performance. Moreover, declarative memory depends on the integrity of medial temporal lobe and diencephalic structures whereas nondeclarative memory depends on the integrity of other brain areas (striatum, 77 neocortex, amygdala; depending on the type of memory) (Schacter & Tulving, 1994;

Squire, 2004). Nondeclarative and declarative memory systems comprise other systems that I will present in the context of odor memory (Figure 7).

declarative

procedural semantic episodic short-term

Odor conditioning Odor priming ; j Odor identification j j Odor recognition : 1 Odor discrimination

Figure 7. Memory systems and examples of corresponding olfactory mnesic tasks; prs is perceptual representation system.

Odors and Nondeclarative Memory

The nondeclarative branch of memory is believed to have appeared earlier in phylogenetic (development of species) and ontogenetic (development of an organism) evolution (Schacter & Tulving, 1994) and to be less sensitive to aging and health disturbances than the declarative memory system. The nondeclarative system is often subdivided into procedural memory and the perceptual representation system.

Odors and Procedural Memory

Procedural memory manifests itself by action. Procedural memory underlies the acquisition of skills, classical conditioning and nonassociative learning such as habituation.

Classical conditioning is observed when a previously neutral item [the conditioned stimulus (CS+)] becomes predictive of a meaningful one (most of the time it 78 is also emotional) [the unconditioned stimulus (UCS)]. Because odors have an important hedonic dimension (Schiffman, 1974), they easily act as UCS in conditioning paradigms. For example, odors as appetitive or aversive UCS have been paired with pictures of faces (CS+) and in consequence, the faces led to physiological reactions previously associated with smelling the odors alone (UCS) (Hermann, Ziegler,

Birbaumer, & Flor, 2000; Todrank, Byrnes, Wrzesniewski, & Rozin, 1995). Also, therapeutic virtues of odor conditioning have been tried as a "cure" for overeaters; to make them less appetitive, target food such as desserts or french fries were paired on multiple occasions with a disagreeable odor (Cole & Bond, 1983; Frohwirth & Foreyt,

1978). This "cure" had moderate success, after 8 weeks of treatment, subjects had lost some weight, but 8 weeks after the end of the treatment all the weight was regained.

Unfortunately, odor conditioning can have unwanted consequences. Kirk-Smith, Van

Toller and Dodd (1983) have shown that if an ambient odor is associated with a stressful situation (such as completing WAIS block patterns under time limitations), this odor can lead to increased anxiety when present in subsequent situations. Robin and collaborators

(1998; 1999) have found that the odor eugenol 10 was coupled with a higher skin conductance and with more negative emotions (fear, anger, disgust) in subjects who were afraid of the dentist than in subjects who were not fearful. For nonfearful subjects, eugenol was rather associated with happiness and surprise. It was also shown that in some Vietnam war veterans, initiation of post-traumatic stress disorder physiological and psychological symptoms were triggered when veterans encountered odors associated

Eugenol is present in eugenates cement that is used by dentists. It is often the typical smell of the dental office. 79 with combat (Kline & Rausch, 1985; McCaffrey, Lorig, Pendrey, McCutcheon, &

Garrett, 1993).

One of the most potent manifestations of classical conditioning in olfaction is the development of odor and taste aversion. Developing taste and smell aversions to the odor of a substance that when ingested led to sickness is protective and makes sense in an evolutionary perspective (Borison, 1989). However, aversions can also cause serious health problems, such as in patients undergoing cancer treatment. Indeed, it is often the case that patients are nauseated and vomit in consequence of their treatment. Patients can develop taste/odor aversions to oral medication or food consumed during the treatment that are hard to extinguish (Andrews & Sanger, 1993; Bernstein, 1978; Garcia,

Laister, Bermudez-Rattoni, & Deems, 1985; Hursti et al., 1992).

Another form of procedural memory concerning odorants is habituation.

Habituation is the progressive diminution of the probability of a behavior with repeated presentation of a stimulus. Using an odor detection test, Jacob, Fraser, Wang, Walker and O'Connor (2003) showed that people adapt/habituate more rapidly to bad (valeric acid, skatol, butyric acid) than to good smells (amyl acetate, cis-3-hexenol, linalool).

The amount of adaptation was also inversely proportional to odor intensity. Jacob and collaborators (2003) interpreted their findings as an indication that the olfactory system is well tuned to changes in potential warning odors. Measuring event-related potentials

(ERPs), Nordin, Lotsch, Murphy, Hummel, and Kobal (2003) found an electrophysiological correlate of habituation. After multiple presentations of hydrogen sulfide (rotten egg smell), the amplitude of ERPs decreased and their latencies increased. 80

Odor and the Perceptual Representation System

The perceptual representation system (PRS) operates at a pre-semantic level, emerges early in development and is less flexible than other cognitive systems.

Perceptual priming is the expression of the PRS and is reflected in the unconscious facilitation of performance after earlier exposure to a target stimulus. Compared to perceptual priming, conceptual priming would be based more on the operations of semantic memory (Tulving & Schacter, 1990). In olfaction, there is not much evidence for perceptual priming, which could be observed as lower detection thresholds (Schab &

Crowder, 1995a), but there is some support for the existence of olfactory conceptual priming. For example, previous exposure to odorants is reported to improve later identification (Olsson & Cain, 2003; Schab & Crowder, 1995a) and to facilitate judgments of edibility (Koenig, Bourron, & Royet, 2000; Olsson & Friden, 2001).

Odors and Declarative Memory

In day-to-day language, when people refer to how good or bad their memory is, they are talking about their declarative memory. The main distinction that is drawn for declarative memory is the one between semantic and episodic memory. Semantic memory refers to general knowledge or to facts whereas episodic memory refers to the acquisition and retrieval of information having a spatiotemporal context or to events

(Tulving, 1983). Another system that could be nested under the wings of declarative memory is short-term memory. Working memory and primary memory are sometimes presented as the active and passive divisions of short-term memory (Baddeley, 1986).

Olfactory representations can occur in each of these three declarative memory systems. 81

Odors and Semantic Memory

In olfaction, semantic memory concerns the knowledge an individual has about the hedonic dimension of odors or how pleasant one finds an odorant, and also concerns the names or identification of odors (Larsson, 2002).

Hedonic value of odors

The hedonic value of odors, or their perceived pleasantness, is recognized as the most salient characteristic of odors (Harper, Smith, & Land, 1968; Land, 1979;

Moncrieff, 1966; Schiffman, 1974). It is not clear yet whether the hedonic value of odors is learned after birth or if odors are inherently pleasant or unpleasant. Engen (1982) suggested that the hedonic value of odors was learned after five years of age because until that age children have odor preferences that are different from those of adults. For example, it was found that four year-old children like the smell of amyl acetate

(candy/banana smelling substance) as much as they like the smell of artificial sweat and feces (Stein, Ottenberg, & Roulet, 1958). In opposition to Engen's (1982) suggestion, others have shown that infants exhibit congruent affective reactions to odors (i.e., they find pleasant or unpleasant odors that adults also find pleasant or unpleasant), indicating that some odorants may have an inherent hedonic value (Steiner, 1979; Strickland,

Jessee, & Filsinger, 1988).

Odor identification

Asking a subject to name the odorant that is inside a featureless experimental bottle is hardly an ecologically valid task. Indeed, the function of olfaction is more to identify the source of an odor (e.g., the desired morning coffee), than the odor itself

(e.g., the caffeine molecule) (Richardson & Zucco, 1989). Given this, it might not be surprising to learn that despite being able to distinguish a vast number of odorants 82

(around 10 000), humans are poor at naming odorants that are presented out of context

(Cain, 1979; Chobor, 1992). Giving multiple choices of possible names, such as in a multiple choice test, considerably improves odor identification (Doty, Shaman,

Kimmelman, & Dann, 1984; Larsson et al., 1999). Larsson (2002) has suggested that subjects perform better in multiple choice paradigms than in free identification because of a reduction in cognitive demands. When labels are offered, subjects do not need to generate them; they can reduce the task to recognizing the name that matches their olfactory sensation. Although initially poor, odor identification can be improved with practice (Desor & Beauchamp, 1974; Engen & Pfaffman, 1959) or by providing nonolfactory cues such as a word or a color on a card (Davis, 1981).

A frequent occurrence when trying to identify an odorant is the "tip-of-the-nose" phenomenon. This phenomenon, first described by Lawless and Engen (1977), is the olfactory cousin of the "tip-of-the-tongue" experience (Brown & McNeil). A "tip-of-the- nose" event occurs when one recognizes a smell but is unable to name it. Whereas subjects in "tip-of-the-nose" states can answer questions about the word they are looking for, such as its first letter, subjects in "tip-of-the-nose" state cannot, but they can speak about the category of the odor (e. g., if it is fruity or floral) and about objects associated with this odor (Lawless & Engen, 1977). The relatively frequent occurrence of "tip-of- the-nose" experiences may be related to the fact that odor language is poor and idiosyncratic (Engen & Hunter, 1982). After analysing the mistakes subjects made when identifying series of odors (in free identification and in multiple choice), Engen (1987) concluded that subjects did not identify odors based on their phenomenological properties. Rather, their identification was idiosyncratic. 83

Individual differences are important in odor identification. First, there is a gender difference; women are typically more accurate in naming odors than are men (Cain,

1982). This superiority of women has been attributed to hormonal factors and to differences in verbal ability (Engen, 1987), and some have dared to link this advantage to the increased familiarity of women with domestic odors (Engen & Berson, 1975).

Second, aging has an adverse effect on odor identification (Larsson & Backman, 1993;

Lehrner, Walla, Laska, & Deecke, 1999). A progressive loss of olfactory acuity, called presbyosmia, occurs with advancing age (Van Toller & Dodd, 1987; Van Toller, Dodd,

& Billing, 1985). But it has been shown that the deficit older adults have for odor identification is attributable not only to reduced olfactory acuity, but also to a deficit in verbal label usage (Schemper, Voss, & Cain, 1981) and to performance on other semantic memory tasks such as vocabulary and information (Larsson, Finkel, &

Pedersen, 2000).

Odors and Episodic Memory

Because we seldom try to remember odors encountered in daily life, laboratory tests of episodic odor memory, like tests of semantic odor memory, do not seem highly ecologically valid (Issanchou, Valentin, Sulmont, Degel, & Koster, 2002; Neisser,

1976). In everyday life, we learn odors incidentally. Laboratory tests of odor memory are made somewhat more legitimate by the finding that odor memory is equivalent after incidental (subject is not aware that he must memorize the targets and that his memory will be tested) or intentional (subject is aware that his memory will be tested) learning instructions (Ayabe-Kanamura, Kikuchi, & Saito, 1997; Engen & Ross, 1973).

In the laboratory, episodic memory is usually tested with recall or recognition tests.

In olfaction, tests of recall memory are seldom used. One reason for this is that asking 84 subjects to recreate the odors they have encountered during encoding seems like an immensely difficult task if one is not a professional perfumer, or Jean-Baptiste

Grenouille the hero/murderer with an absolute sense of smell in Patrick Suskind's (1985

) novel Perfume. But it is of interest that such a "real" recall test was used with the other chemical sense, taste. In that recall test, subjects had to mix proportions of a tasteless substance with a concentrated taste to reproduce the intensity of a solution they had just tasted (Tuorila, Theunissen, & Ahlstrom, 1996; Vanne, Tuorila, & Laurinen, 1998). The other reason why recall tests are not recommended in olfaction is that they require subjects to recall, and possibly to encode, odor names (Schab & Crowder, 1995c), confounding odor memory and memory for odor names. This explains why episodic odor memory is preferentially tested with recognition tasks. In olfaction, recognition tests can have at least two formats: for example, two-alternative forced choice or yes/no recognition (but see White and Treisman (1997) for recognition tests related to the order in which the odors were presented). In the two-alternative forced choice paradigm, subjects are presented with pairs constituted of a previously presented odorant and a new odorant and subjects must identify the odorant previously encountered. In the yes/no recognition paradigm, subjects are presented with individual, new and old, odorants and for each one, they must state whether it was presented earlier.

Some elements have been found to influence episodic odor memory. Of these, verbal elaboration and the formation of odor imagery during encoding have been found to improve odor recognition (Larsson & Backman, 1993; Lyman & McDaniel, 1990).

Many teams also report that accurately naming odors at encoding increased odor memory (Jehl, Royet, & Holley, 1992; Lehrner, 1993; Lehrner, Gluck, & Laska, 1999;

Lesschaeve & Issanchou, 1996; Lyman & McDaniel, 1986, 1990; Rabin & Cain, 1984) 85 but see (Engen & Ross, 1973; Lawless & Cain, 1975). A probable reason why naming odors enhances memory is that naming allows odors to be dually encoded (Paivio,

1986). To test the influence of dual encoding in olfaction, Perkins and Cook (1990) asked their subjects to learn a series of odors while at the same time doing a task that would prevent verbal encoding (suppression paradigm; e.g., to repeat a sequence of numbers or to play a computer game while trying to encode other information). They found that verbal suppression decreased odor memory, suggesting that dual encoding does take place when memorizing odorants. However, Zucco and Tressoldi (1988) and

White and collaborators (1998) still believe that verbal encoding has a minimal influence in odor memory.

Odors and Short-Term Memory

Odor memory was long believed to consist solely of a long-term component

(Engen, 1991; Engen & Hunter, 1982). However, many factors are not consistent with this belief. First, day-to-day experience makes it clear that we carry out short-term memory processes with olfactory information (e.g., when cooking, grocery shopping, or even more pleasant, tasting wines). Second, the experimental tasks of odor discrimination and odor matching clearly tap into working memory. To succeed in these tasks, it is necessary that subjects form transient representation of odors (Larsson, 2002).

Third, the idea that olfactory information could be processed without short-term memory conflicts with the current cognitive view of memory organization (Baddeley, 1994;

Nyberg & Tulving, 1996). Finally, there is more and more experimental evidence in favor of olfactory short-term memory (White, 1998).

As described previously, working memory and primary memory are sometimes presented as the active and passive divisions of short-term memory (Baddeley, 1994). 86

Short-term memory differs in many ways from longer term memory; among these are differences in capacity and in coding. If short-term odor memory exists, these differences should also be found in olfaction.

Concerning the capacity differences, the number of items that can be retained in short-term memory is smaller than in long-term memory. Consequently, performance in short-term odor memory tasks should be better when fewer odors need to be remembered, and performance in long-term memory tasks should involve a larger number of odors. Indeed, it was shown that short-term odor memory is better when there are fewer odors to remember (Engen, Kuisma, & Eimas, 1973; Jones, Roberts, &

Holman, 1978) and that a much larger number of odors (up to 70% of 48 targets odors) can be remembered over a long-term of one to four months (Engen & Ross, 1973;

Lawless, 1978; Lawless & Cain, 1975).

Concerning the coding differences, it was shown that information is not represented the same way in short- and in long-term memory. For example, it was demonstrated that to encode words in long-term memory, meaning was important, whereas to encode the same words in short-term memory, rehearsal was more beneficial

(Baddeley, 1966). With odor memory, this coding might differ too. It seems that for short-term odor memory, perceptual similarity is more important than semantic factors, such as odor familiarity and the ability to identify odorants, but the reverse is true for efficiently coding odors in long-term memory (Jehl, Royet, & Holley, 1997; Schab,

DeWijk, & Cain, 1991; White, Hornung, Kurtz, Treisman, & Sheehe, 1998).

Finally, a robust phenomenon in short-term memory, serial position effects, must be discussed for olfaction. When serial position effects occur, items presented at the beginning (primacy) and at the end (recency) of a list are remembered better than items 87 presented in the middle. Because of the results of two studies that were not designed to investigate serial position effects in olfaction (Gabassi & Zanuttini, 1983; Lawless &

Cain, 1975), it was long believed that there was no serial position effect with odors in humans. Later, it was demonstrated that the serial position effect with odors existed, but that it was different from the effect usually associated with words. With lists of odors presented in a short-term memory paradigm, there is a recency effect, but there is not much evidence for a primacy effect (Annett & Lorimer, 1995; White & Treisman,

1997). The primacy effect has been associated with greater rehearsal (Waugh &

Norman, 1965), and rehearsal may not be as efficient with odors.

Declarative Odor Memory and Affective Influences

I believed that starting the last section of this literature review with an evocative quote from Marcel Proust about odors and ancient memories was appropriate because what most investigations on odors, memory and emotions are trying to do now is to understand the "Proust effect"(Chu & Downes, 2000b; Herz, 2002). The "Proust effect" has been described as the special ability of odors to cue retrieval of very old, vivid and emotional autobiographical events. It was given this name because in "A la recherche du temps perdu", Marcel Proust (1913) describes a particularly vivid and emotional triggered by a bite of a tea-soaked piece of cake. The "Proust effect" may be experienced by the majority of people at least once in their life. In fact, in what is probably the first survey on odor and memory, Laird (1935) wrote that more than 80% of 254 "living men and women of eminence" reported having had smell-revived memories. Of these, only 7 % of the women and 16% of men said that these smell- revived memories were neutral. In another survey, more famous and larger (26 200 88 subjects randomly selected from over 1.5 million responses), the National Geographic

Smell Survey (Gilbert & Wysocki, 1987), about 55% of respondents in their 20s reported that they had had at least one memory cued by one of the six odors of the survey11, and in older respondents (in their 80s) this percentage was 30%.

From these surveys, it seems that odor cued memories are not at all uncommon and this may be related to the fact that odor memories can be acquired during the earliest stages of life. For example, it was shown that the olfactory system is functional after only 12 weeks of gestation (Schaal, Marlier, & Soussignan, 1998; Winberg & Porter,

1998) and there is evidence that some odors found in the mother's amniotic fluid are learned by the foetus during gestation (Marlier, Schaal, & Soussignan, 1998; Schaal,

Marlier, & Soussignan, 1998; Schaal & Rouby, 1990; Schaal, Soussignan, & Marlier,

2002; Winberg & Porter, 1998).

Going back to the "Proust effect", two main avenues have been taken trying to understand it: studies of paired-associate learning, in which odors are each associated to a distinct item or in which an odor served as ambient context, and studies of autobiographical memories triggered by odors. Now, I will describe the findings of these studies and some factors that have been proposed as potential explanations for the

"Proust effect".

Odor-Cued Memory: Paired-Associate Learning

The results from the first experiments investigating the efficiency of odors to cue memories were not too promising. Initially, it was found that odors were inferior to words or shapes in cuing the recall of digits or odor names in paired-associate learning

11 Six odors were presented to readers of the National Geographic magazine on a "scratch-and-sniff' card included in the magazine. They were: androstenone (sweat), amyl acetate (banana), Galaxolide™ (musk), eugenol (cloves), mercaptans (gas), and rose. 89 paradigms (Davis, 1975, 1977; Eich, 1978). Herz & Cupchik (1995) were not discouraged by these results and asked subjects to associate emotionally evocative paintings with either odors or odor labels. At test, odors and labels were presented again and subjects had to recall and describe the painting that was associated with each one.

The authors found that the descriptions cued by odors were more emotionally loaded, but not more accurate than memories retrieved with labels. Later, Herz (1996) tested memory for pictures associated with cues that were presented in olfactory, tactile, or visual form (such as the smell of an apple, the feel of an apple, or the sight of an apple).

Again, it was found that odors led to recollection that was more emotionally toned, but not more accurate than memories cued by visual or tactile cues.

In the next type of odor paired-associate experiments, the physical context/environment was manipulated by the presence or the absence of an odor in the experimental room. Typically, subjects had to learn stimuli (e.g., faces or list of words) incidentally in a room that was perfumed with an ambient aroma (e.g., flowers, ammonium sulphide, chocolate, violet leaf) and better performance was observed when memory was tested in the same olfactory environment (Cann & Ross, 1989; Herz, 1997;

Schab, 1990). The method adopted by those studies is more ecological, and closer to

Proustian retrieval than standard paired-associate paradigms. In reality, subjects rarely have to remember lists of associations between an odor and another stimulus, and the

"Proust effect" refers to retrieval cued by an odor that was learned incidentally, without the subject trying to.

Odors as Cues to Autobiographic Events

Studies involving personal memories can be challenging because it is often impossible to assess the exactitude of subjects' autobiographical recall. However, 90 because the "Proust effect" involves personal memories, researchers had to develop experimental questions that circumvent this exactitude problem and that allow one to learn about olfactory triggered autobiographical memories.

The first experimental study of odor-evoked personal memories compared subjects' recall when presented with odors, words or pictures of common objects

(Rubin, Groth, & Goldsmith, 1984). Subjects were also asked to rate their memories on vividness and pleasantness, to date each one and to state how often they thought or talked about it. The only significant finding was that odor-evoked memories were thought of and talked about less often than memories cued by words or pictures. The second study of autobiographic memory cued by odors was conducted by Ehrlichman and Halpern (1988). They asked college women to recall a personal event related to neutral words while they were in a room perfumed with a pleasant odor (almond extract), an unpleasant odor (pyridine) or no odor. Women in the pleasantly scented room recalled more happy memories than women in the odor-free or malodorous room.

Proustian memories are supposed to be especially accurate. Aggleton and

Waskett (1999) found a clever manner to verify this claim about the accuracy of odor- cued autobiographical memories. They took advantage of the fact that their subjects had all visited the Jorvik Viking Centre (York, UK), years before (average of six years). This museum seeks to recreate the city of York during Viking occupation and, to make the experience more realistic, the exhibition is laden with numerous smells (e.g., burnt wood, apples, fish market). Aggleton and Waskett asked subjects to answer questions about elements of the museum exhibition in the presence of the museum odors, in their absence or in the presence of odors that were not part of the original exhibition. It was 91 found that subjects' recall was more accurate in the presence of the Jorvik odors, demonstrating the potency of odors as cues.

Two other important defining characteristics of the "Proust effect" are that odors, compared to other types of sensory information (auditory, tactual, visual), are cues believed to produce memories that are more emotional and older. In numerous cross- modal experiments, Herz and colleagues demonstrated that even if memories evoked by various cues did not differ in vividness or specificity, odor-cued memories were significantly more emotional (according to subjects' rating of their memory and content)

(Herz, 2004; Herz & Cupchik, 1992, 1995; Herz & Schooler, 2002). Relative to the claim that Proustian memories are older, Chu & Downes (2000a) examined the distribution of autobiographical memories cued by odors or by words, as a function of age of the memory, in subjects in their late 60s and early 70s. They demonstrated that the "reminiscence bump", a peak in the time distribution of autobiographic memories

(Rubin, Wetzler, & Nebes, 1986) was earlier for odor-cued memories than for word-

cued memories, indicating that odor-cued memories were older than verbally cued

episodes. The majority of word-cued memories happened between the ages of 11 and 25,

whereas most odor-cued memories happened between the ages of 6 and 10.

Some Explanations for the "Proust effect"

Several experimental findings are in accordance with the layman's intuition and

the Proustian proposition claiming that odors are potent cues to autobiographical

memories (Aggleton & Waskett, 1999), that odors trigger the recall of events that are

more emotional (Herz, 2004; Herz & Cupchik, 1992, 1995; Herz & Schooler, 2002) and

that they are older (Chu & Downes, 2000a) than personal events retrieved with other 92 types of cue. Now, I will present some of the many factors that have been proposed to account for these Proustian effects.

Because odors are known to elicit affective reactions (Hinton & Henley, 1993), it was suggested that mood-congruent phenomena (Bower, 1981) could explain the

"Proust effect". The findings of Ehrlichman and Halpern (1988), in which the presence of a pleasant odor biased subjects' recall towards hedonically congruent information

(happy events), are consistent with this hypothesis. However, the study of Cann and

Ross (1989), in which subjects' memory for faces was better when tested within the same olfactory environment, but in which the olfactory environment did not influence subjects' mood, does not support the mood-congruent hypothesis.

Emotional arousal has a strong influence on memory (Christianson, 1992), and it was proposed that as odors are affectively arousing, they may be especially efficient retrieval cues (Aggleton & Waskett, 1999; Herz, 1997). How emotional arousal influences odor episodic memory is unknown because this topic has never been investigated empirically. However, the influence of emotional arousal on odor semantic memory (naming) has been examined by Jonsson, Olsson, and Olsson (2005). They found that the more arousing the odor, the more subjects were confident in the accuracy of the label they gave that odor, but subjects were not more accurate. Clearly, even if the hypothesis that the arousing properties of odors makes them highly potent memory cues seems promising, researchers need to tackle this question empirically.

If the distinctive quality of the "Proust effect" is that odors are good memory reminders, then the encoding specificity hypothesis (Tulving & Thompson, 1973) may provide a satisfactory explanation. According to this hypothesis, elements present during learning (context) are encoded with the target information. At recall, if this contextual 93 information is reinstated, it will serve as a powerful retrieval cue. Many experiments in which the ambient odor (olfactory context) is reinstated at retrieval, and in which memory is improved, are consistent with the encoding specificity hypothesis (Aggleton

& Waskett, 1999; Cann & Ross, 1989; Herz, 1997; Schab, 1990).

However, if the distinctive quality of Proustian memories is that odors are special in that they are better cues (than other type of sensory information), the encoding specificity hypothesis is unhelpful. Indeed, one assumption of the encoding specificity hypothesis is that once the context is encoded and consolidated, all its elements are of equivalent value in helping retrieval. Chu and Downes (2000b;, 2002) have proposed the "differential cue affordance value" hypothesis in which olfactory cues are assumed to have a higher value in retrieval of autobiographical information. To justify their proposition, Chu and Downes (2002) remind us that autobiographical memories are complex, and that complex representations are more likely to include peripheral information. Odors can be considered as peripheral information because usually they do not modify the meaning of an event. Consequently, and importantly, odors will cue the retrieval of richer autobiographical events compared to other, nonperipheral, cues. To provide evidence in favor of their differential cue hypothesis, Chu and Downes (2002) compared the efficiency of different cues in retrieving information related to an individual event. Subjects had to retrieve one autobiographical episode when presented with a label (an odor name); next they were presented with a second cue (either the label a second time, a picture, the odor corresponding to the label, or a different odor) and they had to extend retrieval of the autobiographical episode retrieved to the first cue. It was found that the vividness and the number of details reported were greater, compared with retrieval to the first label, when the second retrieval cue was the odor that matched 94 the label, than in the three other conditions. Because the presentation of a different odor as second cue did not influence the vividness or the number of details of the described autobiographical events, the effect of odor as a cue cannot be due to a modification of the subject's emotional state; i.e., a mood-congruent phenomenon. Moreover, because only the congruent odor condition (not the label, the picture or the mismatching odor) increased details and vividness of the memory, this research does support the differential cue hypothesis; i.e., that odors are especially potent cues to the retrieval of autobiographical events. However, if the underlying logic is true, any other peripheral information has the potential to become a powerful retrieval cue, a surprising proposition that needs to be demonstrated.

Finally, the unique characteristics of the "Proust effect" may have a neuroanatomical basis. Brain areas mediating olfactory, affective and mnesic processes are all in the vicinity of each other and have numerous reciprocal projections. This will be the topic of the next section.

Neuroanatomical Substrates of Odor Hedonics and Odor Memory

As little as 20 years ago, most knowledge about the neural substrates of olfaction was extrapolated from experiments carried out in rodents and nonhuman primates

(Zatorre & Jones-Gorman, 2000). However, noninvasive research techniques have progressed exponentially in the last 15 years, allowing researchers to gain key insight into human olfaction. I will now provide an anatomical overview of the olfactory system, both at the peripheral and central level. Next, I will present the current knowledge regarding the neural basis of the intimate link between olfaction and affect.

Finally, I will discuss the of odor memory with findings from 95 neuroimaging (in healthy subjects) and lesion (primarily in epilepsy patients who underwent a unilateral resection from the temporal lobe) studies.

Anatomical Overview of the Olfactory System

To experience smell, volatile molecules of odorants must reach the olfactory receptors. The olfactory receptors are in the olfactory epithelium located at the roof of the nasal cavities. In humans, the olfactory epithelium measures approximately 5 cm2 and contains about 10 million receptors (Engen & Hunter, 1982) . To reach the epithelium, odorants may take one of two possible routes: either orthonasally, through the nostrils, or retronasally, through the nasopharynx, behind the soft palate (Heilmann

& Hummel, 2004). To bind with olfactory receptors, it is necessary that odorants cross the olfactory mucosa covering the epithelium. Each olfactory sensory neuron is a bipolar cell expressing a single olfactory receptor (Buck & Axel, 1991), and different odorants are detected by different olfactory receptors (one or a combination) (Kajiya et al., 2001; Malnic, Hirono, Sato, & Buck, 1999). Olfactory sensory neurons send their unmyelinated (making olfaction a relatively slow sense) axons through the cribriform plate to the olfactory bulb and form the olfactory tract, the first cranial nerve, which will project olfactory information to the primary olfactory cortex. In the olfactory system, projections are primarily ipsilateral.

Because most inputs from the olfactory bulb converge upon the piriform cortex

(situated near the junction of the frontal and temporal lobes), this structure was initially considered to be the primary olfactory cortex (POC) (Djordjevic & Jones-Gotman,

2006). However, a series of structures that are densely interconnected are now believed

It is interesting to note that dogs, assumed to have greater olfactory sensitivity than humans, have over 200 million olfactory receptors (Engen & Hunter, 1982). 96 to form the POC (Zatorre & Jones-Gotman, 2000). According to Carmichael, Clugnet and Price (1994), the macaque POC (but the same may be assumed in humans) includes not only the piriform cortex, but also the olfactory tubercle (also called the anterior perforated substance), the anterior olfactory nucleus, the ventral taenia tecta, the anterior cortical nucleus of the amygdala, the nucleus of the lateral olfactory tract of the amygdala, the periamygdaloid complex and the rostral entorhinal cortex.

The POC structures project on another series of structures, the secondary olfactory cortex (SOC) (Djordjevic & Jones-Gotman, 2006; Zatorre & Jones-Gotman,

2000). The SOC is believed to include the posterior orbitofrontal cortex, the medial and subcallosal prefrontal cortex and the agranular insular cortex (Carmichael, Clugnet, &

Price, 1994). The POC also send projections to the hippocampus, the ventral striatum and pallidum, the thalamus and the hypothalamus (Price, 1990).

Earlier in this review, it was suggested that the unique characteristics of the

"Proust effect" had a neural basis. This proposition may prove relevant because, among the sensory systems, the olfactory system has many distinctive neuroanatomical features.

For example, unlike primary and secondary areas in the visual, auditory or somatosensory modalities, the primary and secondary olfactory areas are not neocortical.

While the POC structures are allocortical, they contain three layers of neurons instead of the six found in the neocortex (Carmichael et al. 1994; Price, 1990); the SOC structures belong to the agranular/dysgranular cortex that is generally missing layer IV

(Carmichael & Price, 1994). Another distinguishing neuroanatomical feature of the olfactory system is that olfactory information passes directly from the olfactory bulbs to the POC. Other senses have an obligatory thalamic relay between receptors and the primary sensory area (Djordjevic & Jones-Gotman, 2006). Finally, the especially 97 intimate link that the olfactory system shares with the limbic system may very well tip the scale in favour of the "Proust effect". For example, the POC includes parts of the amygdala, a structure well known for its affective role (e.g., Aggleton, 1992), which projects to the subiculum (a component of the hippocampal formation), a structure involved in memory formation (e.g., O'Mara, 2006).

Affective Dimensions of Olfaction

An ever increasing number of studies is being undertaken to understand what neural structures underlie the ability of smell to elicit a strong affective response (for reviews: Djordjevic & Jones-Gotman, 2006; Rouby & Bensafi, 2002; Zatorre, 2002).

Different research techniques have been used, but there is no consensus yet as to the structures implicated in the processing of affective odors and as to whether there is hemispheric specialization, or not, in the judgment of odor pleasantness. Nonetheless, now I will present some of the findings obtained in healthy subjects, in patients who underwent a resection from the temporal lobe for the relief of epileptic seizures and with functional neuroimaging.

In healthy participants, Kobal, Hummel, and Van Toller (1992) found that olfactory evoked potentials had smaller amplitudes and shorter latencies when unpleasant odors were smelled through the left nostril, and when pleasant odors were perceived through the right nostril. They believed that this difference was evidence in favor of a relative specialisation of the left hemisphere for positive emotions and of the right hemisphere for negative emotions. With another method, Bensafi, et al. (2003) reached a similar conclusion. They asked subjects to judge the pleasantness of an odor, presented to one nostril or the other, as fast as possible. Because subjects' reaction times were shorter when they rated unpleasant odors presented to the right nostril, it was 98 suggested that the right hemisphere had an advantage in processing unpleasant odorants.

However, Herz, McCall and Cahill (1999) found that subjects rated odors as more pleasant when they were smelled through the right nostril, and interpreted this as an indication of right hemisphere superiority in processing pleasantness.

Lesion Studies

Given that surgical resections from the medial temporal lobe (MTLR) typically sacrifice some essential olfactory structures (Dade, Zatorre, & Jones-Gotman, 2002), experiments conducted in patients with MTLR could reveal crucial information regarding olfaction and affect. Despite their potentially revealing nature, I was able to find only four studies about odor pleasantness in individuals with MTLR or hippocampal damage.

In the first one, Hughes and Andy (1979) trained patients to make pleasantness judgments to a set of seven odors, prior to amygdalar resection. Following surgery, patients were asked on many occasions (once every day for a few weeks, then once every week for up to 1.5 year) to rate the pleasantness of the same odors. Hughes and

Andy reported that judgements of odor pleasantness were temporarily changed (they judged more odors to be unpleasant) after lesions of the right amygdala (but in that study, no patient had a removal from the left amygdala). In the second one, Duerden,

Jones-Gotman, and Zatorre (1990) found that patients with either left or right MTLR were more variable in their ratings of odor pleasantness than were healthy subjects. In the third one, when pleasantness was assessed by asking subjects to compare pairs of odorants, MTLR patients were again found to have ratings that were more variable than those of healthy subjects (Rouby, Zatorre, Jones-Gotman, & Forster, 1997). Moreover, in that study only patients with right MTLR were impaired. Finally, in a study of odor memory in which patients with hippocampal damage (due to cerebral anoxia) had to rate 99 odors for pleasantness at encoding, Levy, Ramona and Squire (2004) found no difference between the ratings of patients and of healthy control subjects.

Neuroimaging Studies

Numerous scientists have understood that neuroimaging techniques are powerful and relatively noninvasive methods to investigate the affective dimension of olfaction.

Fulbright et al. (1998) conducted one of the first neuroimaging studies of pleasantness in olfaction. They presented subjects with the odor of Clementine, isovaleric acid or clean air and asked them to rate the intensity and pleasantness of each one. They report activation to these odors in the dorsal prefrontal cortex but none in the orbitofrontal cortex or medial temporal lobe. Subsequent studies have not replicated this finding.

Rather, others have shown activation of the left orbitofrontal cortex and bilateral amygdala when smelling very unpleasant odors (a sulphide "cocktail") (Zald & Pardo,

1997); activation in the left orbitofrontal cortex, the left temporal pole, the left superior frontal gyrus, the hypothalamus, the subcallosal gyrus and the amygdala bilaterally

(Royet et al., 2000) and activation in the right orbitofrontal cortex and hypothalamus when making pleasantness judgments to pleasant and unpleasant odors (Zatorre, Jones-

Gotman, & Rouby, 2000). Wicker et al. (2003) have shown that pleasant and unpleasant odors could produce equal activation in the amygdala, but activations differed in the insula. The anterior portion of the insula was activated bilaterally by disgusting odorants and the posterior portion of the right insula by pleasant odorants.

Gottfried and collaborators have conducted many experiments of associative memory in which odors are paired with visual information (Gottfried, Deichmann,

Winston, & Dolan, 2002; Gottfried & Dolan, 2003,2004; Gottfried, O'Doherty, & Dolan,

2002,2003; Gottfried, Smith, Rugg, & Dolan, 2004). Their findings are related not only to 100 the mnemonic dimension of the task, but also to the affective component of odors. For example, they found that the posterior piriform cortex and the left amygdala were activated by all odors but that this was not the case for the anterior piriform cortex. The anterior piriform was activated only by pleasant and unpleasant but not neutral odors (Gottfried,

Deichmann, Winston, & Dolan, 2002; Gottfried & Dolan, 2003). Moreover, they report that the anterior piriform cortex displays a differential temporal response to pleasant and unpleasant odors: the response to pleasant odors is stable over time but the one to unpleasant odors decreases.

In another comparison of pleasant and unpleasant odors that were matched on intensity, Royet, Plailly, Delon-Martin, Kareken, & Segebarth (2003) found different activation to odor pleasantness as a function of subjects' handedness. Unpleasant odors activated the left ventral insula in right handers and the right ventral insula in left handers. They also found that the amygdala activition was stronger to unpleasant odors.

Because in that experiment unpleasant odors also led to larger skin conductance, it was suggested that the amygdala was tuned preferentially to the arousal dimension of olfaction; i.e., the intensity of the emotional reaction caused by the odorant.

It has long been known that pleasantness is not the sole fundamental dimension of emotion; arousal is equally important (Lang, Bradley, & Cuthbert, 1990; Russel,

1980). For Anderson et al. (2003) the perceptual intensity of odorants corresponds with, or is a potential index of the arousal dimension. They presented subjects with pleasant

(citral—lemon like) and unpleasant (valeric acid—putrid, fecal) odorants at a weak or strong intensity (low or high concentration). They found evidence that the neural representation of intensity (arousal) was dissociated from the representation of pleasantness. Activity in the amygdala was uniquely associated with odor intensity and 101 activity in orbitofrontal regions was associated, uniquely also, with odor pleasantness.

Consistent with these results are the findings of Rolls, Kringelbach and de Araujo (2003) who uncovered activity in the medial temporal lobe in association with the intensity, and not with the pleasantness of odors. Also, pleasant odors activated a medial portion of the orbitofrontal cortex and unpleasant odors were associated with activity in the lateral orbitofrontal cortex. However, in a recent fMRI study, Winston, Gottfried, Kilner and

Dolan (2005) showed that the amygdala was activated in response to intense pleasant

(citral) and intense unpleasant (valeric acid) odors, but not to intense neutral (anisol:

"phenolic, gasoline, ethereal"; 2-heptanol: "earthy, oily") odors. Thus, they suggested that the amygdala codes for a combination of intensity and pleasantness, that is for the overall emotional value of odorants. This concept is closer to the emotional arousal dimension than to concentration of odorant or perceptual intensity.

Odor Memory

Lesion Studies

Because most studies of patients with MTLR reveal normal detection thresholds

(Eskenazi, Cain, Novelly, & Friend, 1983; Eskenazi, Cain, Novelly, & Mattson, 1986;

Henkin, Comiter, Fedio, & O'Doherty, 1977; Jones-Gotman & Zatorre, 1988; Martinez et al., 1993; Rausch & Serafetinides, 1975), any observed odor recognition deficits in these patients are more likely to be caused by deficient odor memory processes than by poor odor perception. However, this may be less true for patients with resection from the orbitofrontal cortex, as they exhibit a severe impairment in odor discrimination (Jones-

Gotman & Zatorre, 1988, 1993; Zatorre & Jones-Gotman, 1991). If an individual demonstrates odor discrimination difficulty, he is likely to be impaired on odor tasks of a higher cognitive level (e.g., odor memory and odor identification). 102

Patients with MTLR are found consistently to have odor recognition memory deficits. Resections from the right hemisphere are believed to produce bigger impairments (Abraham & Mathai, 1983; Carroll, Richardson, & Thompson, 1993;

Eskenazi, Cain, Novelly, & Friend, 1983; Jones-Gotman & Zatorre, 1993; Martinez et al.,

1993; Rausch, Serafetinides, & Crandall, 1977). However, larger odor recognition deficits have been observed in patients with left MTLR (Henkin, Comiter, Fedio, & O'Doherty,

1977), and some report equal impairment irrespective of side of resection (Dade, Zatorre,

& Jones-Gotman, 2002).

Interestingly, patients with bilateral hippocampal atrophy (due to anoxic episodes) also show impaired odor recognition (Levy, Hopkins, & Squire, 2004). Moreover these patients are worse than healthy control subjects in an "odor span" task (Levy et al., 2004).

I must also point out that in another study of odor recognition memory, patients with

MTLR were impaired in recognizing the names of odors they had previously smelled but not in odor recognition per se (Buchanan, Tranel, & Adolphs, 2003). Finally, patients with temporal- or frontal-lobe resection have been shown to have an odor identification deficit when the odor is smelled through both nostrils (Jones-Gotman & Zatorre, 1988). It is interesting to note that the extent of hippocampal resection did not matter; i.e., patients with larger hippocampal removal were not more impaired in odor identification than patients with smaller removal. Also, patients with MTLR (left or right) have been shown to be impaired in odor identification when odors are presented to the nostril ipsilateral to their resection (Jones-Gotman et al., 1997). These studies suggests that temporal lobe structures

13 On the first trial, subjects are presented with one of 14 odorants. On the second trial, subjects are presented with two odors that are positioned randomly on an odor-bottle holder. On each trial, subjects' task is to identify the new odorant, and they can smell the odors in the order they want. Trials continue this way until all 14 odors are presented in the odor-bottle holder. 103 are involved in a range of odor memory tasks: semantic (identification), episodic

(recognition) and working (odor span) memory tasks.

Neuroimaging Studies

In a positron emission tomography (PET) experiment - the first neuroimaging study of odor memory - activations similar to those seen during odor perception were reported (piriform bilaterally and right orbitofrontal cortex), but the right posterior hippocampus was also activated (Jones-Gotman, Zatorre, Evans, & Meyer, 1993;

Zatorre & Jones-Gotman, 2000). Dade and collaborators (Dade, Jones-Gotman, Zatorre,

& Evans, 1998; Dade, Zatorre, & Jones-Gotman, 2002) scanned subjects during odor encoding and during immediate and delayed recognition. Activity in the piriform and right orbitofrontal cortex was revealed during both recognition tests. During encoding, regional cerebral blood flow (rCBF) increased in the superior and medial frontal gyri bilaterally and in the left precentral gyrus. Savic, Gulyas, Larsson and Roland (2000) report increased activation in the right temporal cortex, the parietal lobe bilaterally, the left cerebellum, the piriform, the cingulate, the orbitofrontal cortex and in the amygdala during an odor recognition task. Dade, Zatorre, Evans & Jones-Gotman (2001) scanned subjects during a working memory task in which subjects had to indicate whether the odor they were currently smelling was the same as or different from the odor smelled two trials before. Their finding of increased rCBF in the right mid-dorsolateral frontal cortex is consistent with working memory studies in other modalities (Cabeza &

Nyberg, 2000; Petrides, Alivisatos, & Evans, 1993; Petrides, Alivisatos, Evans, &

Meyer, 1993). It is interesting to note that except for Jones-Gotman, Zatorre, Evans and

Meyer (1993), none of these odor-memory studies found hippocampal activation. 104

Another interesting negative finding is the lack of piriform activation during the encoding portion of Dade's studies (1998; 2002). This may seem surprising given that subjects had a good odor memory performance (odors had to be well perceived!).

However, inconsistent activation in the piriform cortex when perceiving odorants is almost a trademark of the field. Different hypotheses may explain these inconsistencies:

PET scans are not powerful enough to detect weak but real activity (Zatorre & Jones-

Gotman, 2000), the piriform habituates rapidly (Poellinger et al., 2001; Sobel et al.,

2000), or the piriform is involved even when the subject is just sniffing plain air (in the control condition) (Sobel et al., 1998).

Going back to the "Proust effect", Herz, Eliassen, Beland and Souza (2004) have compared brain activation when subjects' aubiographical memory was cued by an odor or by a picture. They found greater activation in the amygdala and hippocampal area when recall was cued by a personally significant odor than by any other cue. No activation was reported in the orbitofrontal cortex because their region of interest was within the medial temporal lobe. Finally, in a series of cross-modal recognition experiments, Gottfried and collaborators (Gottfried, Deichmann, Winston, & Dolan,

2002; Gottfried & Dolan, 2003; Gottfried, O'Doherty, & Dolan, 2002, 2003; Gottfried,

Smith, Rugg, & Dolan, 2004) investigated the neural correlates of visual-olfactory associations. Of their numerous interesting findings, I will report two. During appetitive but not during aversive olfactory learning, activation in the anterior hippocampus bilaterally decreased over time (Gottfried, O'Doherty, & Dolan, 2002). Also, assuming they were previously paired with odors during encoding, visual stimuli presented alone

elicited activation in the right posterior piriform and the right hippocampus. Because no odor was presented and significant piriform activity was observed, this experiment 105 strongly suggests that the piriform is a storage locus of olfactory information (Gottfried,

Smith, Rugg, & Dolan, 2004).

Conclusion

As we have seen, the "Proust effect" is more than nice prose. Memory, odors and emotions have, indeed, a special relationship. In this last section, I have tried to provide a comprehensive review of the empirical evidence that could help explain this relationship. This specificity may very well be related to the fact that among all the sensory systems, olfaction has the closest neuroanatomical connections with the neural substrates of emotion and memory. However, we also know that pleasantness is not the sole component of emotions, arousal is there too. And we also know that arousal can have a powerful influence on memory. It is therefore surprising that the memory enhancing effect of emotional arousal has never been investigated with odors. In fact, despite the popular belief that odors have a special ability to evoke emotional memories, the relation between memory, odors and emotions still is a vastly uncharted territory.

Clearly, a lot of work still needs to be done by chemosensory experimental psychologists and neuroscientists. 106

CHAPTER 3. PRELIMINARY STUDY 107

PRELIMINARY STUDY

Introduction

I undertook this preliminary study with two goals in mind. One goal was to select odorants that varied in perceived pleasantness, arousal, intensity and familiarity, in order to generate two equivalent odor sets for future odor recognition memory experiments.

The other goal, necessary for the previous, was to adapt to odorants a scale that could assess the subjective appraisal of those four attributes. Additionally, the scale should be useable regardless of participants' language and should be easy to administer.

For this purpose, I chose to adapt the Self-Assessment Manikin (SAM) (Hodes,

Cook, & Lang, 1985) because SAM is a reliable instrument for evaluation of emotional reactions (of valence and arousal) that has been used with many stimuli and with diverse populations. Many investigators agree that arousal and valence are parameters at the basis of emotion (eg., Bradley & Lang, 2000). Valence is described as a continuous dimension ranging from unpleasantness (unhappy, annoyed...) to pleasantness (happy, pleased...). Arousal is described as ranging from an unaroused state (lethargic, relaxed, sleepy...) to a highly aroused state (alert, excited, wide awake). As arousal increases, the probability of falling asleep diminishes (Corcoran, 1965, 1981). Whereas valence seems to correspond to the direction of the emotional state, arousal seems to correspond to its intensity.

Although SAM has never been used with odorants, it is effective for measuring emotional reactions to pictures (Greenwald, Cook, & Lang, 1989; Lang, Greenwald,

Bradley, & Hamm, 1993), to sounds (Bradley & Lang, 1999b), to words (Bradley &

Lang, 1999a), to mental imagery (Miller et al., 1987) and even to painful stimuli

(McNeil & Brunetti, 1992). SAM has been used not only with healthy adults, but also 108 with children (Greenbaum, Turner, Cook, & Melamed, 1990), with anxiety patients

(Cook, Melamed, Cuthbert, McNeil, & Lang, 1988), with temporal lobectomy patients

(Morris, Bradley, Bowers, Lang, & Heilman, 1991) and with psychopaths (Patrick,

Bradley, & Lang, 1993). Moreover, SAM is a subjective instrument that accurately reflects physiological reactions to affective stimuli. Among others, meaningful covariations have been described between SAM ratings of unpleasantness and contraction of the corrugator muscles (contraction of the brows) (Lang, Greenwald,

Bradley, & Hamm, 1993), between SAM pleasantness ratings and contraction of the zygomatic muscle (smile muscle) (Schwartz, Brown, & Ahern, 1980) and between SAM ratings of arousal and skin conductance (Lang, Greenwald, Bradley, & Hamm, 1993).

Hand sweating is often measured as a means to assess autonomic arousal: skin- conductance varies as a function of sweat, and sweat glands are thought to be innervated solely by the sympathetic branch of the autonomic nervous system.

Inspired by SAM (Bradley, Greenwald, Petry, & Lang, 1992; Hodes, Cook, &

Lang, 1985; Lang, 1980), my new scale (SAM*SMELL) retains the arousal and pleasantness dimensions of the original scale, but also includes intensity and familiarity dimensions. I implemented an intensity scale because odor intensity is an important component of odor perception (Doty, 1975), and because intensity was found to be highly correlated with subjective and objective measures of arousal (Bensafi et al.,

2002a). A familiarity scale was included because odor familiarity has been shown to influence odor pleasantness (Engen & Ross, 1973; Royet et al., 1999) and odor memory

(Larsson, Oberg, & Backman, 2006; Rabin & Cain, 1984; Schab & Crowder, 1995c).

My two goals of selecting odorants for a memory test and of adapting SAM to odorants were attained in four steps. The first step was to assemble a large number of 109 odorants from which the adapted SAM* SMELL could be validated and from which appropriate odorants could be selected for later memory tests. The second step was to ask subjects to rate all these odorants with SAM*SMELL. The third step was to compare

SAM* SMELL ratings on the dimensions of pleasantness, arousal, intensity and familiarity and determine the pattern of relationships among them as we wished to reproduce previous findings (Rouby & Bensafi, 2002). The fourth and final step was to use these SAM* SMELL ratings to select odorants and to assign them to two different sets equivalent on most dimensions.

1. Assemble Odorants

To increase the chances of including appropriate odorants in the future memory tests and of obtaining meaningful results using SAM* SMELL ratings, a large sample of odorants was tested. I gathered one hundred thirty odorants that were either compounds provided by aroma industries (Bell, Fluka, Givaudan-Roure, International Flavors and

Fragrances) or chemicals provided by chemical societies (Aldrich, Sigma, Sigma-

Aldrich) (Appendix A). Most odorants were diluted to a concentration of 10% (in mineral oil), this resulted in solutions of approximately equal perceptual intensity as judged by the experimenters. It was decided to make this intensity relatively weak to diminish olfactory adaptation during testing.

2. Rating of Odorants with SAM*SMELL

Method

Subjects

Forty-one university students (25 women) between the ages of 19 and 40

(average=22.85) were tested. Three were left-handed and four were smokers.

Francophones were tested in French; all other subjects were tested in English. The 110 maternal language breakdown was: 2 Cantonese, 1 Czech, 1 Dutch, 20 English, 10

French, 2 German, 1 Italian, 1 Japanese, 1 Mandarin, 1 Russian, and 1 Serbian.

Material

Odor ants. The 130 odorants gathered in Step 1 (Appendix A) were used. Odorants were presented in 30 ml amber glass bottles in which a piece of polypropylene was inserted to absorb the odorant, to prevent spilling and to ensure a sufficient exchange with air (Figure 8). Odorants were kept refrigerated when not in use.

Figure 8. Glass bottle used to present odorants (the piece of polypropylene inserted inside is shown on the right side).

SAM*SMELL. This pen and paper rating scale was used to measure subjective responses to diverse dimensions of the odorants (Figure 9). Six SAM* SMELL scales appeared on each page of a rating booklet (8'/2 X 11 paper). Ill

j Intensity % ^> n\ ^ ^ \

as ran rn a Pleasantness

nnnnnnn Familiarity

DWDTOiD Arousal

Figure 9. Adaptation of SAM to SAM*SMELL for olfactory testing. Pleasantness and arousal dimensions are from the original SAM.

For each dimension, ratings were made by checking on or between one of the five figures, producing a nine-point scale. The dimension of pleasantness ranges from a frowning unhappy figure to a smiling, happy one and the dimension of arousal (or of emotional intensity) ranges from a sleepy, relaxed figure to an excited, wide awake one

(Hodes, Cook, & Lang, 1985; Lang, 1980). The odorant intensity dimension of

SAM* SMELL shows figures that range from an indication of no perceived odorant (tiny bottle under a tiny nose) to figures indicating the strongest odorant ever smelled (large bottle under a large nose). The familiarity dimension was described to participants as ranging from having no idea about the odor's identity to being certain of what it was

(naming was not required). The SAM*SMELL figures for this dimension ranged from a manikin with his shoulders up in the air, his eyebrows elevated and a big question mark over his head to a confident looking one with a big light bulb over his head. 112

Procedure

Subjects had to smell the 130 odorants and to rate each one with SAM*SMELL.

After explaining the different dimensions of this rating task, the experimenter presented the odorants in a random order that differed for every subject (see Appendix B for exact instructions). Each odorant bottle was placed approximately 1.5 cm under the subject's nostrils for 3 seconds. Subjects completed SAM*SMELL immediately after smelling each odorant. The time interval between two odorant stimulations was 30 seconds or more, to prevent olfactory adaptation. When subjects had smelled and rated half of the odorants (after the 65 odorant), they were given a 10 minute break.

3. Correlations between SAM* SMELL dimensions

Individual ratings for each odorant were averaged and a correlational analysis between the different dimensions was conducted. The analysis revealed significant

Pearson correlations between ratings of arousal and intensity (r(128)=0.93, /?=.000001), of arousal and familiarity (r(128)=0.78, ^=.000001), familiarity and intensity

(r(128)=0.72,jp=.000001), familiarity and pleasantness (r(128)=0.6,/?=.000001). No significant linear correlation was found between SAM*SMELL ratings of arousal and pleasantness (r(128)=0.15,/?=.09) or of intensity and pleasantness (r(128)=0.01,p=.89).

However, there was a significant quadratic relationship between ratings of arousal and pleasantness (r(128)=0.59, ^=.000001) and of intensity and pleasantness (r(128)=0.41,

^=.000001) (Figure 10).

These correlations are not completely new findings. Most have been described elsewhere, but it is the first time that an adapted version of SAM has been used to assess odors. Bensafi et al. (2002a) asked subjects to rate odorants on intensity, familiarity, 113 arousal and pleasantness, and reported a strong correlation between ratings of arousal and intensity. The fact that they did not uncover any other significant relationship was probably due to the small number of odorants (six) in their experimental paradigm. No other team has ever reported a correlation between arousal and familiarity for odorants.

However, Distel and colleagues (1999) reported a positive correlation between familiarity and "hedonic strength", where "hedonic strength" was defined as absolute ratings of pleasantness, regardless of whether an odorant was rated as pleasant or unpleasant. This "hedonic strength" dimension seems to represent the emotional importance (or emotional intensity) of the stimulus, a definition that is close to my definition of arousal.

I found a positive correlation between SAM* SMELL ratings of familiarity and intensity; this correlation has been observed previously by the teams of Distel et al.

(1999) and of Royet et al. (1999). My finding of a positive correlation between familiarity and pleasantness is also supported by earlier (Distel et al., 1999;

Engen & Ross, 1973; Royet et al, 1999; Sulmont, Issanchou, & Koster, 2002). The relationship existing between pleasantness and intensity is a complex one. Some have reported a negative relationship between pleasantness and intensity (Henion, 1971), some have reported a relationship depending on the odorant (for some odorants the correlation is negative, for others it is positive) (Doty, 1975) and others, no correlation at all (Royet et al., 1999). I found no linear correlation between intensity and pleasantness, but visual inspection of the data suggested a quadratic relationship, which when tested was found to be significant. It indicated that odors that were rated as more pleasant and those rated as more unpleasant were all rated as more intense. I also found a quadratic relationship between SAM* SMELL ratings of arousal and pleasantness. It is the first 114 time that this relationship was observed with odorants, but a similar nonlinear correlation has been reported for pictures. Increases in ratings of picture pleasantness or unpleasantness are correlated with increases in rated arousal (Lang, Ohman, & Vaitl,

1988). ll

/t128)=78, p=.00001 r(128)=.93,p=.00001 /{128)=.72,p=.00001 • # •

7 - 7-

6- 6- 5 " I5" 4 - •• • 3- <»*•• 2 -j it 2 3 4 5 6 7 8 12 3 4 5 6 7 12 3 4 5 6 7 8 familiarity intensity intensity

Linear: r(128)=.15,p=.09 r(128)=.6,p=.00001 Linear: r{128)=.01,p=.89 Quadratic: /{128)=.59, p=.00001 9 - 31 Quadratic:/t128)=.41,p=.00001

7 - • •• /3^ • 7- 6 - 6- 5 •'..< 1 " 5-

4 - 4 . «:. 3 3-

2 - 2

1 — 12 3 4 5 6 7 1 l 5 6 7 12 3 4 5 6 7 pleasantness pleasantness pleasantness

Figure 10. Correlations between SAM*SMELL ratings. 116

4. Selection of Odorants for Odor Memory Tests

Because the correlations obtained were consistent with previous findings, I considered SAM*SMELL to be an appropriate tool to investigate relations existing between affective and perceptual dimensions of odors. Thus, the SAM*SMELL ratings obtained here also provide good empirical data to help in odorant selection for memory testing.

Based on the SAM*SMELL ratings, 42 odorants were selected to use in odor memory testing. These odorants were assigned to two different sets (designated Set A and Set B) designed to be as equivalent as possible (Table 2). Odorants that had obtained minimal ratings of intensity were eliminated. Odorants varying in levels of intensity, familiarity, pleasantness and arousal were distributed homogeneously across sets.

Odorants were also distributed homogeneously across sets as a function of their semantic categories (fruity, floral, household product, chemical, stinky...).

Finally, Mests were conducted to verify that the two odorant sets were equivalent on each SAM* SMELL dimension. There was no difference between odorant Sets A and

B for ratings of intensity (£(40)=0.58, p=.5T), pleasantness (/(40)=0, p=\), familiarity

(t(40)=0.02,p=.9S) or arousal (t(40)=0.64,p=.52).

Conclusion

The goals of this preliminary experiment were attained. One goal was to develop a rating scale adapted to odorants, which would be easy to use and which could be administered regardless of subjects' language. SAM*SMELL seems good for this purpose because it was used without difficulty by participants of diverse linguistic background, and correlations found in the literature were replicated. The other goal was to select odorants for use in memory testing. Two odorant sets equivalent in semantic 117 categories and in ratings of intensity, pleasantness, familiarity and arousal were created.

These odorant sets and the SAM* SMELL scale will be used in the following experiments of this thesis.

Table 2

Selected Odorants and Memory Sets to which They Were Assigned

Mean Rating

Intensity Pleasantness Familiarity Arousal

Set A

Ambrarone 5.17 3.02 4.29 4.44 Anise 5.37 4.56 5.44 4.27 Banana 6.56 5.34 6.71 5.46 Bergamot 5.71 4.88 5.49 4.39 Black Pepper 4.8 4.41 4.8 3.93 Butyric acid 5.07 2.49 4.12 4.39 Cardamon 6.76 3.93 4.83 5.54 Cineole 6.27 5.68 6.39 5.54 Ethy-3-methy-3-phenyglicidate 4.85 6.27 5.66 4.85 Freesia 5.9 6.15 6.6 5.08 Ham 6.93 2.78 5.9 5.75 Lime 6 5.68 6.44 4.98 Methyl 2-methylbutyrate 6.48 4.43 5.08 5.45 Methyl benzoate 5.39 4.76 4.93 3.85 Methyl ionone gamma 4.61 6.07 5.41 4 Mousse de chene 5.46 5.68 5.73 4.32 Peanut butter 6.75 6.43 6.98 6.18 Pyridine 8.1 1.63 3.85 6.9 Styrax essence 6.29 6.29 7.07 5.63 Viridine 4.88 5.2 5.83 4.02 Z-heptanone 6.27 4.24 5.98 4.85

Minimum 4.61 1.63 3.85 3.85 Maximum 8.1 6.43 7.1 6.9 Average 5.89 4.76 5.6 4.94 Mean Rating

Intensity Pleasantness Familiarity Arousal

SetB

Angelica root 5.34 4.66 5.1 4.02 Basil 6.44 4.02 5.51 5.63 Bois de rose 6.44 5.66 6.73 4.98 Carrot 6.85 2.95 4.59 5.49 Citronellyl butyrate 4.66 2.78 3.85 4.41 Coffee 6.12 5.54 6.73 5.54 Eugenol 6.7 5.28 6.65 5.45 Galbanum oil 4.17 4.59 4.49 3.51 Garlic 7.61 3.76 6.49 5.93 Guava 6.05 7.41 7.15 5.51 Mimosa 6.51 6.37 6.8 5.12 Musk ambrette 3.93 6.02 4.83 4.17 Octyl acetate 4.68 4.44 4.41 3.95 Orange 5.59 5.98 6.44 5.1 Patchouly 5.51 4.63 6.02 4.32 Peru balsam 4.83 5.66 6.02 4.39 Pine needles 5.24 4.49 4.8 4.15 Tarragon 4.73 4.49 4.95 3.93 Thymol 6.22 4.41 6.54 4.88 Trans-cinnamyl butyrate 6.2 2.58 4.2 5.05 Verdone 6.35 4.2 5.38 5.13

Minimum 3.93 2.58 3.85 3.51 Maximum 7.61 7.41 7.15 5.93 Average 5.72 4/76 5,6 4J5_ Note. v\v: volumeWolume, w\v: weightWolume 119

CHAPTER 4. STUDY 1

Odors Causing Strong Emotional Reactions are Remembered Better

Pouliot, S., Hudry, J., and Jones-Gotman, M.

Montreal Neurological Institute, McGill University, Quebec, Canada

This work has been submitted for publication and the revision is currently under review at Cognition & Emotion. 120

Abstract

We measured emotional reactions to odors with self-reports and physiological monitoring, and assessed odor memory one week later. We found that magnitude of phasic skin conductance was greater for odorants rated as more emotionally arousing than for odors rated as eliciting smaller reactions. Odorants rated as more arousing were also remembered better than odorants rated as less arousing. Odor pleasantness did not affect odor memory. In a second experiment, we found that odors rated as more intense and as unpleasant were remembered better but the enhancing effect of emotional arousal on odor memory did not reach significance. Strong emotional reaction to an odorant seems to enhance odor recognition memory without influencing response bias. Given that very specific conditions are needed for emotional arousal to enhance memory for pictures and words, our findings suggest that the enhancing, but capricious and demanding, effect of emotional arousal on memory may not be modality specific. 121

Introduction

Why do we remember easily the perfume of our first love but not so well the one of our first lab mate in Chemistry 101? One could answer that it is because information associated with strong emotional reactions is remembered better than information that is less emotional (Christianson, 1992; Craik & Blankstein, 1975; Phelps, 2004). An illuminating illustration of this relationship is the "flashbulb memory" phenomenon in which a highly emotional (or arousing) event (for example: the attack on the World

Trade Center, Challenger's explosion or President Kennedy's shooting) would be remembered as clearly as if it were perceived again (Brown & Kulik, 1977; Winograd &

Killinger, 1983; Yarney & Bull, 1978) (but see McCloskey, Wible, & Cohen, 1988).

In the olfactory world, a similar phenomenon is often cited, namely the "Proust effect" (Chu & Downes, 2000b, 2002), in which smelling an odor leads to the retrieval of a personal memory that is especially vivid and strongly emotional. Trying to understand this "Proust effect", researchers have found that odors compared to other types of sensory information are remembered longer (Engen & Ross, 1973), that they are more evocative autobiographical memory cues (Chu & Downes, 2000b, 2002; Rubin,

Groth, & Goldsmith, 1984) and that they allow the retrieval of information that is more emotional (Herz & Cupchik, 1995; Herz, Eliassen, Beland, & Souza, 2004; Hinton &

Henley, 1993).

In the laboratory, declarative memory is not immune to the effect of emotion either. Matlin and Stang (1978) described the "Pollyanna effect", in which memory is better for pleasant relative to neutral information. However, more frequent are reports of a memory advantage for unpleasant, negative or traumatic information (Christianson &

Loftus, 1987, 1991; Maratos, Allan, & Rugg, 2000; Talmi & Moscovitch, 2004). The 122 more a stimulus is polarized on the pleasantness continuum, the more emotionally arousing it will be (Bradley, Greenwald, Petry, & Lang, 1992). It is generally accepted that emotionally arousing visual and auditory stimuli are better remembered than nonarousing stimuli (Brewer, 1988; Christianson, 1992; Kleinsmith & Kaplan, 1963,

1964). Studies using words have shown that long-term memory performance was better for highly arousing items compared to the less arousing ones (Craik & Blankstein, 1975;

Eysenck, 1976; Sharot & Phelps, 2004). Moreover, Bradley, Greenwald, Petry and Lang

(1992) investigated the specific contribution of pleasantness and arousal to memory for pictures and demonstrated that only emotional arousal had an effect on memory. Highly arousing pictures were better remembered than pictures that were less arousing, regardless of their pleasantness.

Surprisingly, despite the proposed relationships between emotions and odor memory as well as between emotional arousal and memory, the influence of emotional arousal on odor memory has not been studied before. Our hypothesis is that odors associated with larger emotional reactions, or arousal, will be remembered better than less arousing ones.

In the first experiment, we tested whether emotionally arousing odors are remembered better than less arousing ones and this, regardless of their pleasantness. We obtained subjective ratings of arousal and pleasantness as well as objective estimation of emotional reactions through measures of skin conductance during an incidental odor memory task. The recognition test was given a week after incidental encoding because it has been shown that the effect of arousal on memory is easier to capture after a minimum delay of 24 hours (Baddeley, 1982; Craik & Blankstein, 1975; Kleinsmith &

Kaplan, 1963, 1964; Park & Banaji, 1996; Sharot & Phelps, 2004). 123

Experiment 1

Method

Subjects

Thirty undergraduate students (17 women and 13 men, mean age/education=20.5/14.1, range=l 8-29/12-20, 2 women were left handed) participated in this experiment. Exclusion criteria were infection obstructing the upper nasal airways, respiratory allergies, or neurological or psychiatric antecedents. All subjects gave informed consent and none reported to be a regular cigarette smoker.

Material

Odorants. Forty-two odorants were used (Table 3). They were selected from among 130 odorants that had been rated for intensity, pleasantness, familiarity and arousal by 41 subjects in an earlier study (Pouliot, Hudry, & Jones-Gotman, 2003). The

42 odorants were divided into two equivalent sets (A and B) of 21 odorants ranging in ratings of intensity (A: M=5.9 / SD=0.9; B: 5.7 /l), pleasantness (A: 4.8 /1.4; B: 4.8

/1.2), familiarity (A: 5.6 /0.9; B: 5.6 A), and arousal (A: 4.9 /0.8; B: 4.8 /0.7). The set of

21 odorants that was presented at encoding was the memory target set in the recognition test. Odorants from the other set served as foils during recognition. The specific odorant set being presented as targets or foils was counterbalanced across subjects. 124

Table 3 Two Sets ofOdorants Used in the Memory Task

A B

Ambrarone Angelica root Anise Basil Banana Bois de rose Bergamot Carrot Black Pepper Citronellyl butyrate Butyric acid Coffee Cardamon Eugenol Cineole Galbanum oil Ethy-3-methy-3- phenyglicidate Garlic Freesia Guava Ham Mimosa Lime Musk ambrette Methyl 2-methylbutyrate Octyl acetate Methyl benzoate Orange Methyl ionone gamma Patchouly Mousse de chene Peru balsam Peanut butter Pine needles Pyridine Tarragon Styrax essence Thymol Viridine Trans-cinnamyl butyrate 2-heptanone Verdone

All odorants were odor chemicals. With a few exceptions, we diluted odorants to

10 % in 4.5 ml of mineral oil. They were presented in 30 ml amber glass bottles in which a piece of polypropylene was inserted to absorb the odorant, prevent spilling and ensure a better exchange with air. Odorants were kept refrigerated when not in use.

Subjective ratings. A new pen and paper rating scale was used to measure subjective responses to perceptual and affective dimensions of odorants. Inspired by the

Self-Assessment-Manikin (SAM), a well-known rating scale used in emotion research

(Hodes, Cook, & Lang, 1985; Lang, 1980), the new SAM*SMELL scale keeps the arousal (calming-exciting) and pleasantness (unpleasant-pleasant) dimensions of the original scale, but also includes intensity and familiarity dimensions. We implemented 125 an intensity scale because odor intensity is an important component of odor perception

(Doty, 1975) and because intensity was found to be highly correlated with subjective and objective measures of arousal (Bensafi et al., 2002a). We added a familiarity scale because familiar odors are often remembered better than unfamiliar ones (Savic &

Berglund, 2000; Schab & Crowder, 1995c). The pleasantness (valence) and arousal dimensions of the SAM scales have been described elsewhere (Bradley, Greenwald,

Petry, & Lang, 1992; Lang, 1980).

The odor intensity dimension of SAM* SMELL shows figures that range from an indication of no perceived odorant (tiny bottle under a tiny nose) to figures indicating the strongest odorant ever smelled (large bottle under a large nose). The familiarity dimension ranged from having no idea about the odor's identity to being certain of knowing what the odor was (naming was not required). The SAM*SMELL figures for this dimension ranged from a manikin with his shoulders up in the air, his eyebrows elevated and a big question mark over his head to a confident looking one with a big light bulb over his head. For each dimension, ratings were made by checking on or between any of the five figures, producing a nine-point scale. Six SAM*SMELL scales, each comprised of the four dimensions, appeared on each page of a rating booklet.

Psychophysiology. We amplified and recorded skin conductance and breathing with a Power Lab 4 SP system using Chart 5 for Windows software (AD Instruments).

Skin conductance in microsiemens (ja.S) was recorded with bipolar nondisposable electrodes attached with velcro™ straps to the palmar surface of the middle segment of the fore and middle fingers of the nondominant hand. The GSR amplifier was fully isolated and provided a low constant-voltage AC excitation (22 mV at 75Hz) on one of 126 the two electrodes. Changes in breathing were monitored with a pressure transducer

(PTAFlite, Pro-Tech) fitted to a cannula (Pro-Flow, Pro-Tech) placed at the nostrils.

The first important increment in breathing that occurred after presentation of an odor determined when an experimental odor had been sniffed. This increment in sniffing volume corresponded to a positive deflection of the breathing waveform. We examined the different magnitude in phasic skin conductance responses (SCR) during the 10 seconds after which an odor was sniffed. We subtracted the mean skin conductance magnitude, for each odor, during the 3 seconds preceding sniff detection (baseline) from the mean skin conductance magnitude in the subsequent 10 seconds. In a way similar to

Bensafi and collaborators (2002a;, 2002b) our prestimulus and poststimulus intervals differ. We chose a 10 second poststimulus window because SCR is relatively slow to rise and we wanted to be certain the maximal phasic value would be included. The subtraction was done to minimize the influence of the general increase in tonic skin conductance. We normalized these differences in mean phasic skin conductance magnitude with log transformations [logio(SCR+l)] (Dawson, Schell, & Filion, 2000;

Venables & Christie, 1980).

Procedure

The experiment comprised two sessions: one for incidental encoding and a later one for a recognition test. Further, the incidental encoding session was divided into two parts; a first part for skin conductance measurements while smelling odors, and a second part for odor rating. We chose to split the incidental encoding session into two successive parts in order to obtain the psychophysiological measures when an odor is first sniffed uncontaminated by interference from hand movements and other cognitive processes that would occur during odor ratings. 127

In the first part of the incidental encoding session, skin conductance and breathing were recorded while subjects smelled each of the 21odorants. Participants were told that the goal of the experiment was to study their emotional reactions when smelling different odors and that their only task was to sniff when a bottle was placed under their nose. They were also told that they should refrain from talking and moving, sniff each odor in the same way and that they should look straight ahead during this part of the experiment. Right before the recording, participants washed and dried their hands (Venables & Christie, 1973). Next, they put on earplugs, in order to reduce extraneous stimulation. Then they were seated comfortably on a chair with an arm rest, in a quiet testing room, and the skin conductance electrodes and the cannula to monitor breathing were installed. Participants were trained to sniff when the experimenter placed a bottle under their nose. Once participants managed to sniff without moving or looking at the bottle, the experiment began with a three-minute relaxation period. After the relaxation period, the experimenter, who was located beside the participant, began presentation of the 21 odors. Odorants were presented individually in bottles 1cm under the nostrils for three seconds, with an interstimulus interval (ISI) of 45 seconds, in a randomized order. Half of the subjects received odorant set A and the other half odorant setB.

In the second part of the incidental encoding session, after SCR and breathing recordings, participants were freed from the electrodes and the cannula and were asked to move to a desk. Participants were told that they would smell again the odors and that their task was now to judge each odor with SAM* SMELL for intensity, pleasantness, familiarity and the degree to which they found the odors emotionally arousing. Again, the experimenter presented each odorant for 3 seconds and the ISI was at least 45 128 seconds. Also, participants were told that they had to be attentive because they would smell each odorant only once to rate all four dimensions. The future odor recognition test was never mentioned.

A week later, the unexpected recognition memory test took place. Forty-two odorants (21 targets, 21 foils or all odorants from sets A and B) were presented for three seconds each, in a pseudo-randomized order such that no more than three targets or three foils were presented consecutively; ISI was 45 seconds. A yes-no sequential presentation was used; a response was required for every presentation. Finally, in a postexperimental questionnaire, we asked subjects about their experience in the study.

Results

An alpha level of .05 was used for all statistical tests, and when we report post hoc multiple comparisons, the/?-values are based on Bonferroni adjustments. Because no difference was found between men and women, we present data collapsed across gender

(although gender differences are sometimes observed in olfaction, (Brand & Millot,

2001)).

Ratings

To investigate whether there was a relationship between the different odor dimensions, for each subject we conducted a correlational analysis among the

SAM* SMELL ratings given to the 21 odors at encoding. Because of an a priori hypothesis regarding the direction of each correlation, we performed one-tailed tests. We were expecting positive and linear correlations between ratings of intensity and arousal

(Bensafi et al., 2002a) and between ratings of familiarity and pleasantness and ratings of familiarity and intensity (Royet et al., 1999). Because Distel and collaborators (1999) found a positive linear correlation between familiarity and strength of hedonic judgment 129

(a concept close to emotional arousal) we were expecting a positive and linear correlation between familiarity and arousal. Finally, given that a visual inspection of ratings of pleasantness and intensity reported by Royet et al. (1999) strongly suggests a positive quadratic correlation, and given the conceptual similarity between intensity and arousal, we predicted positive quadratic correlations between ratings of pleasantness and intensity and between ratings of pleasantness and arousal. The correlations we observed between our SAM*SMELL ratings are described in Table 4.

Table 4 Pearson Correlations between SAM*SMELL Rating Dimensions for Experiment 1 and Experiment 2. Averaged across Participants, Range, Proportion and Percent of Significant Correlation (p<.05, one-tailed); df=19

Rating dimension Pleasantness Familiarity Arousal

Experiment 1

Intensity r= .48 .37 .67 range =-.11 to .9 -.36 to .84 .23 to .89 proportion significant = 17/30 (56.67%) 27/30 (90%) 12/30 (40%)

Pleasantness .51 .5 .06 to .84 -.15 to .86 23/30 (76.67%) 17/30 (56.67%)

Familiarity .38 -.4 to .93 18/30(60%)

Experiment 2

Intensity r=.23 .3 .52 range = -.56 to .61 -.29 to .77 -.15 to .86 proportion significant = 13/27 (48.15%) 21/27 (77.78%) 15/27 (55.56%)

Pleasantness .46 .31 -.11 to .88 -.28 to .72 16/27 (59.26%) 16/27 (59.26%)

Familiarity .37 -.46 to .79 18/27 (66.67%) 130

For each correlation, we conducted a binomial test (using the normal approximation) to determine whether the proportion of participants with a significant

Pearson's coefficient was different from chance. They were significant in every case (all

/?s<.0001).

We also conducted x2 tests to determine whether the proportion of significant results for the relationship between intensity and arousal differed from other relationships. We found that this one was greater than for any other relationship with the exception of the one between pleasantness and familiarity ratings (all p<.05).

Memory Discrimination and Response Bias: Pleasantness and Arousal.

Experimental groups. To investigate the contribution of pleasantness and arousal to odor memory discrimination and response bias, we rank ordered the 21 target odors by pleasantness ratings for each subject. The ranks for odors given identical ratings were decided on the basis of subjects' mean pleasantness ratings for these odors. The 11 odors with the lowest pleasantness ratings were assigned to the unpleasant group, and the other

10 to the pleasant group. Within each pleasantness group, odors were subsequently ranked by their arousal ratings. Again, ties in ranks were broken on the basis of subjects' mean arousal rating for these odors. The 6 odors with the lowest arousal ratings in the unpleasant group and the lowest 5 in the pleasant group were designated nonarousing odors; the remaining 5 odors in both unpleasant and pleasant groups were considered the arousing odors. These rankings produced for each subject four types of memory target odors: unpleasant nonarousing, unpleasant arousing, pleasant nonarousing and pleasant arousing. The 21 alternate odors presented as foils during the recognition test were rank- ordered in a similar way (in order to calculate the corresponding four types of incorrect 131 recognition/false positive rate); however, average ratings given by subjects who had rated this alternate set at encoding were used.

To determine whether the ranking procedure described pleasantness ratings efficiently across arousal groups, we conducted a repeated-measures ANOVA on mean pleasantness ratings with pleasantness and arousal as within-group factors. The effect of

2 pleasantness was significant (F(l,29)=8037.44, MSE=79.28,/J=.0001, PartialEta =.99), but the effect of arousal was not (F(l,29)=0.3, A/SE=0.003,T?=.86). A significant interaction between pleasantness and arousal (F(l,29)=51.61, M<£Zi=4.27,/>=.0001,

Partial Eta2=.64) indicated that, as expected, ratings of pleasantness were lower in both unpleasant groups compared to the pleasant groups (ps.=.0001) (Figure 11). The post- hoc comparisons revealed that odors in the unpleasant arousing group were rated as less pleasant than odors in the unpleasant nonarousing group (p=.0001); moreover, odors in the pleasant arousing group were rated as more pleasant than odors in the pleasant nonarousing group (p=.0001).

To determine whether this ranking procedure was as efficient in describing arousal ratings across the pleasantness groups, we conducted a similar ANOVA on the mean arousal ratings with odor pleasantness and arousal as within-group factors. The main effect of pleasantness on arousal ratings was not significant (F(l,29)=1.15, MSE-0A7, p-.29), indicating that pleasant and unpleasant odors did not differ in their mean arousal ratings. As expected, a large effect of arousal was found (F(l,29)=1256.3, MSE=6\A5, p=.0001, Partial Eta2=.9S), indicating that odors in the pleasant and unpleasant arousing groups were rated as more arousing than odors in the nonarousing groups. The interaction between pleasantness and arousal on arousal ratings was not significant

(F(l,29)=1.97, MSE=0.\5,p=A7) (Figure 11). 132

9- 8 • arousal • pleasantness 7

6 _ ——' LU 5 CO ^=_ * 4 < CO 3 2 i 1 unpleasant pleasant unpleasant pleasant

norla nDU ;sin g arousing

Figure 11. Mean ratings of pleasantness and arousal in the four pleasantness and arousal odor group combinations. Error bars express standard error of the mean.

d' and C. For each subject, we calculated memory discrimination (d') and response bias (C) indices within each of the four odor groups. The d' is a bias free measure that gives a clear estimate of memory accuracy because it takes into account correct recognitions or hits (responding 'yes it is old' when presented with a target odor) and incorrect recognitions or false positive errors (responding 'yes it is old' to a foil).

The C is a measure of response tendency or bias. It is important to measure bias because abnormal bias is often a significant component of abnormal memory (Snodgrass &

Corwin, 1988) and may differ among odor dimensions. No response bias is present when

C equals 0. A liberal bias, or a tendency to respond "yes it is old" when uncertain, corresponds to a negative C while a conservative bias, or a tendency to answer "no it is not old" when uncertain, corresponds to a positive value.

We conducted two separate 2X2 ANOVAs, one on d' and one on C with pleasantness and arousal as within-subject factors. The analysis conducted on d' 133 revealed no effect of pleasantness (F(l,29)=1.55, MSE=0..55, p=..22), a significant effect of arousal on memory discrimination (F(1,29)=21.52,MS'£'=8.96,/'=.0001, Partial Eta 2

=.43) (Figure 12) and no interaction (F(l,29)=0.44, MSE=0.22,p=.5l). The effect of arousal indicated that odors rated as more arousing were remembered more accurately than less arousing odors. The similar analysis of variance performed on C showed no significant effects of pleasantness (F(l,29)=0.33, MSE=0.05,p=.57), of arousal

(F(l,29)=1.18, MSE=0.I6,p=.29), or interaction between arousal and pleasantness

(F(l,29)=1.18, MSE=0.14,p=.29), suggesting that differences in arousal or pleasantness did not influence subjects' response strategies or tendencies.

• unpleasant • pleasant

nonarousing arousing Figure 12. Mean odor memory discrimination (d') as a function of the rated pleasantness and intensity. There was no effect of pleasantness on odor memory (F(l,29)=1.55, p=.22) but the effect of arousal was significant (F(l,29)=21.52,/?=.0001). Error bars express standard error of the mean.

Memory Discrimination and Response Bias: Pleasantness and Intensity

Experimental groups. Because ratings of arousal and intensity were strongly correlated, we wanted to test whether intensity influenced odor memory as well. To do so, we repeated the rank ordering procedure of the previous analysis, but this time within 134 the pleasantness groups the odors were rank ordered by intensity ratings. To determine how efficient this ordering was in characterizing pleasantness levels across intensity groups, we carried out a repeated-measures ANOVA on mean pleasantness ratings.

There was a main effect of pleasantness (F(l,29)=8042.6, MSE=78.68,p=.000l, Partial

Eta2=.99) and no effect of intensity (F(l,29)=2.31, MSE=0.17,p=A4). A significant interaction between pleasantness and intensity was found (F( 1,29)=18.91, MSE=\.61, jt?=.0001, Partial Eta =.4). Pairwise comparisons indicated that participants rated unpleasant weak and intense odorants as less pleasant than pleasant weak and intense odorants (p=.0001 andp=.0001). They also rated unpleasant intense odorants as less pleasant than unpleasant weak odors (p-.OOl) and pleasant weak odorants as less pleasant than pleasant intense odorants (p=.02).

We carried out a similar ANOVA on mean intensity ratings with odor pleasantness and intensity as within-group factors. There was no main effect of pleasantness on intensity ratings (F(l ,29)=0.26, MSE=0.0S, p=.6l). The effect of intensity was significant (F(l,29)=993.65, MSE=55.55,^=.0001, Partial Eta1=.97). An interaction between pleasantness and intensity was revealed (F(l,29)=14.91, MSE= \.74,p=.0001,

Partial Eta =.34). Pairwise comparisons indicated that unpleasant and pleasant weak odors were rated as less intense than unpleasant and pleasant intense odors (p=.0001 and

/?=.0001). Unpleasant intense odors were rated as more intense than pleasant intense odors (p=.01).

d' and C. For each subject, we calculated memory discrimination (d') and response bias (C) indices for each of the four pleasantness and intensity groups. We conducted two separate 2X2 ANOVAs, one on d' and the other on C with pleasantness and intensity as within-subject factors. The analysis performed on d' revealed no effect 135 of pleasantness (F( 1,29)=1.06, MSE=0.65, p=.3l), a significant effect of intensity

2 (F(l,29)=10.07, MS£=5.57,jp=.004, Partial Eta =.26) and no interaction

(F(l,29)=3.32, MSE=l.37,p=M). The effect of intensity indicated that odors rated as more intense were remembered more accurately. The analysis of C for pleasantness and intensity revealed no effect of pleasantness (F(l,29)=0.77, MSE=0.l l,p=.39), of intensity (F(l,29)=0.15, MSE=0.03,p=J) or interaction between these factors

(F(l,29)=0.26, MSE=0.04,p=.6l).

Memory Discrimination: Intensity versus Arousal

A larger average d' for arousing (M=1.21) compared to intense odors (M=1.14), and a moderate effect size for arousing odors {Partial Eta =.43) compared to a modest one for intense odors {Partial Eta 2 =.26), suggest a memory discrimination advantage for arousing odors over intense odors. To test this, we conducted a paired samples t-test comparing d' for arousing odors and d' to intense odors. The paired t-test did not show a significant discrimination advantage for arousal versus intensity (/(29)=.91,/?=.37).

Psychophysiology

Skin conductance response: pleasantness and arousal. As we did with d' and C, we calculated the mean phasic SCR magnitude within each of the four pleasantness and arousal groups for every subject. We conducted a repeated-measures ANOVA on mean phasic SCR magnitude, with pleasantness and arousal as within-group factors. This analysis revealed no effect of pleasantness (F(l,29)=0.5, MSE=Q.QQA, p=A%), an effect of arousal (F(l,29)=4.67, MSE=0.0\,p=.04, Partial Eta2 =.\ A) and no interaction between pleasantness and arousal (F(l,29)=0.002, MSE=0.00l,p=.96). The effect of arousal showed that odors rated as more arousing led to greater mean phasic SCR magnitude. The mean phasic SCR magnitudes were .23 for unpleasant nonarousing 136 odors, .25 for unpleasant arousing odors, .22 for pleasant nonarousing odors and .24 for pleasant arousing odors. These values may seem alike, but they differ significantly on the arousal dimension. Moreover, it must be kept in mind that they were log transformed and that they represent the mean magnitude difference in SCR between before and after an odor is smelled (hence phasic SCR).

Skin conductance response at encoding: pleasantness and intensity. We recalculated the mean phasic SCR magnitude within each of the four pleasantness and intensity groups and performed an ANOVA with pleasantness and intensity as within- group factors. There was no effect of pleasantness (F(l,29)=0.47, MSE=O.0G&, p=A9), intensity (F(l,29)=1.05, MSE=0.004,p=.3l) or interaction between pleasantness and intensity (F(l,29)=0.93, MSE=0.004,p=34) on the mean phasic SCR magnitude. The mean phasic SCR magnitudes were .24 for unpleasant weak odors, .24 for unpleasant intense odors, .24 for pleasant weak odors and .22 for pleasant intense odors.

Experiment 2

The aim of Experiment 2 was to confirm the findings of better memory for arousing and intense odors with a different sample of subjects. Unlike in Experiment 1, participants were recruited outside the university community. They were also older (the age difference between subjects of Experiment 1 and 2 was significant: F(l,55)=49.04,

/7=.0001; Exp. 1: mean age= 20.5, range= 18-29; Exp. 2: mean age= 33.6, range=T8-53; but there was no difference in years of education: F(l,55)=2.12, p=A5; Exp. 1: mean education=14.07, range=12-20 ; Exp. 2: mean education= 13.52 , range=12-18). A second aim of Experiment 2 was to determine whether the effects of arousal and intensity could be replicated with a reduced exposure to the odorants to be remembered.

This shorter exposure was used because we wanted to determine whether this type of 137 odor memory task could be usefully included in the clinical neuropsychological assessment of epilepsy patients, an assessment which is already time consuming.

Method

Subjects

Subjects were 27 healthy right handed adults (11 women and 16 men, mean age=33.6, range=18-53) recruited from the general population through advertisement in local newspapers and community centers. The exclusion criteria were the same as for

Experiment 1. All participants gave informed consent and none reported to be a regular cigarette smoker.

Material

We used the odorants (Table 3) and rating scale described in Experiment 1. No psychophysiology apparatus was involved.

Procedure

The procedure was identical to that of Experiment 1, except that participants smelled the odorants once (rather than twice) during incidental encoding, the IS I was 30 seconds rather than 45, and no psychophysiology parameter was recorded.

Results

As in Experiment 1, no difference was found between men and women, we present data collapsed for gender and each subject's SAM*SMELL ratings were submitted to a

Pearson correlation and averaged across participants (Table 4). For each correlation, we conducted a binomial test (using the normal approximation) to determine whether the proportion of participants with a significant Pearson's coefficient was different from chance. As in Experiment 1, all proportions were significant. 138

We also conducted x tests to determine whether the proportion of significant results for the relationship between intensity and arousal differed from other relationships. We found that the proportion of significant results for intensity and arousal was greater than one other relationship, intensity and familiarity (p<.05).

Memory Discrimination and Response Bias: Pleasantness and Arousal

Experimental groups. To investigate the contribution of pleasantness and arousal to odor memory discrimination and response bias, we rank ordered the 21 target odorants in the same way as in Experiment 1. Again, we conducted two separate repeated-measures ANOVAs on the pleasantness and arousal ratings with odor pleasantness and arousal as within-group factors. For the pleasantness ratings there was a large effect of pleasantness (F(l,26)=3855.24, MSE=67.2,p=.0O0l, Partial Eta 2

=.99), no effect of arousal (F(l,26)=0.97, MSE=0.12,p=.33) but as in Experiment 1, there was an interaction between pleasantness and arousal (F(l,26)=32.61, MSE=2A\,

/?=.0001, Partial Eta 2 =.56). The post hoc comparisons showed that unpleasant nonarousing odors were rated as less pleasant than pleasant nonarousing odors

(p=.0001), and that unpleasant arousing odors were rated as less pleasant than pleasant arousing odors (p=.0001). Unpleasant nonarousing odors were rated as more pleasant than unpleasant arousing odors (p=.02) and pleasant nonarousing odors were rated as less pleasant than pleasant arousing odors (p=.0001).

For the arousal ratings, there was no effect of pleasantness (F(l,26)=0.37,

MSE=0.2\,p=.55), a large effect of arousal (F(l,26)=1010.42, MS£=49.09,/?=. 0001,

Partial Eta2 =,98), and an interaction between pleasantness and arousal (F(l,26)=6.84,

MSE=0.57, p=.02, Partial Eta =.21). Post hoc comparisons showed that unpleasant nonarousing and pleasant nonarousing odors did not differ on their arousal ratings 139

(p=A3), and the same was true for unpleasant arousing and pleasant arousing odors

(p=J3). As expected, unpleasant nonarousing odors were rated as less arousing than unpleasant arousing odors (p=.0001) and pleasant nonarousing odors were rated as less arousing than pleasant arousing odors (p=.000\).

d' and C. For each subject, memory discrimination (d') and response bias (C) indices were calculated within each of the four groups of odorants differing in ratings of pleasantness and arousal. We carried out two separate ANOVAs, one on d'and the other on C, with pleasantness and arousal levels as within-subject factors. The d' for unpleasant odors (M=.57) was larger than the one for pleasant odors (M=.31),

(F(l,26)=7.45, MSE=l.95,p=.0l, Partial Eta 2'=.22). Even though the d' for arousing odorants was larger (M=0.53) than the one for nonarousing odorants (M=0.35), the effect of arousal was not significant (F(l,26)=1.76, MSE=0.82,p=.l9). There was no interaction of pleasantness and arousal on d* (F(l,26)=2.67, MSE=2.04,p-.l 1). The response bias index did not vary significantly as a function of pleasantness

(F(l,26)=3.49, MSE=0.53,p=.07), arousal (F(l,26)=0.48, MSE=0.07,p=A9) or interaction of pleasantness and arousal (F(l,26)=0.21, MSE=0.02, p=.65).

Memory Discrimination and Response Bias: Pleasantness and Intensity

Experimental groups. We repeated the rank ordering procedure we had carried out in Experiment 1. As with Experiment 1, we conducted two separate repeated- measures ANOVAs on the pleasantness and intensity ratings with odor pleasantness and intensity as within-group factors. The analysis of pleasantness ratings revealed a significant effect of pleasantness (F(l,26)=4122.89, MSE=67.64,p=.000\, Partial Eta 2

=.99). There was no effect of intensity on pleasantness ratings (F(l,26)=2.05,

MSE=0A8,p=A6). However there was a significant interaction between intensity and 140 pleasantness (F(l,26)=17.79, MS£=1.9,/?=.0001, Partial Eta1'=.41). The post hoc comparisons revealed that odors in the unpleasant weak group were rated as less pleasant than odors in the pleasant weak group (p=.0001), that odors in the unpleasant intense group were rated as less pleasant than odors in the pleasant intense group

(p=.0001) and that odors in the unpleasant intense group were rated as less pleasant than odors in the unpleasant weak group (p=.0001). Odors in the pleasant weak group were not rated differently from odors in the pleasant intense group (p=.06).

The analysis of intensity ratings confirmed a difference in intensity but not in pleasantness (no main effect of pleasantness: F(l,26)=3.14, MSE=l .58, p=.09; large effect of intensity F(l,26)=1068.02, MSE=49.9, /?=.0001, Partial Eta 2 =.98; no interaction of pleasantness and intensity on intensity ratings (F(l,26)=3.02, MSE=0.3, p=.09).

d' and C. For each subject, four memory discrimination (d') and response bias (C) indices were calculated, one each for the unpleasant weak, unpleasant intense, pleasant weak and pleasant intense odorant groups. Two separate ANOVAs were conducted, one on d' and one on C, with pleasantness and intensity levels as the within-subject factors.

The analysis carried out on d' revealed an effect of pleasantness (F(l,26)=6.74,

MSE=2.3,p=.02, Partial Eta 2 =21) indicating that unpleasant odors (M=.58) were better remembered than pleasant ones (M=.29). There was also an effect of intensity

(F(l,26)=4.63, MSE=2.66, p=.04, Partial Eta2 =.15) indicating that memory discrimination for intense odorants (M=.59) was better than for weak odorants (M=.28).

There was no interaction between pleasantness and intensity on d' (F(l,26)=1.75,

MS!£=0.86,£>=.2). The C did not differ for pleasant versus unpleasant odorants

(F(l,26)=2.3, MS^O.33,^.14) or for intense versus weak odorants (F(l,26)=0.21, 141

MSE=0.04, p=.65), and there was no interaction between pleasantness and intensity on response bias (F(l,26)=l.69, MSE=0.2l,p=.21).

Memory Discrimination: Intensity versus Arousal

Because the effect size of arousal (Partial Eta 2 =.06) was relatively smaller than the one for intensity {Partial Eta =. 15) we conducted a paired t-test to assess whether the memory advantage given by intense odors was different from the one given by arousing odors. It was not (t(26)=\,p=.33).

Memory Discrimination: Intensity and Arousal versus Pleasantness

To determine whether the memory advantage given by unpleasant odors (Partial

Eta=.2\) was different from the one given by intense (Partial Eta =. 15) or arousing odors (Partial Eta 2 =.06), we conducted two other paired t-tests. No significant difference was uncovered between memory discrimination of intense versus unpleasant odors (Y(26)=0.12,/>=.9) or between that of arousing compared to unpleasant odors

General Discussion

In the first experiment, we have confirmed our hypothesis that emotionally arousing odors, i.e. odors causing strong subjective (measured with SAM*SMELL ratings) or objective (phasic SCR magnitude) emotional reactions, are remembered more accurately (d') than odors causing weaker emotional reactions. Previously, others have shown that odors are good cues for the explicit retrieval of emotional information (Chu

& Downes, 2000b, 2002; Herz & Cupchik, 1995; Herz, Eliassen, Beland, & Souza,

2004; Rubin, Groth, & Goldsmith, 1984) and that odors are efficient stimuli in nondeclarative emotional memory, specifically in classical conditioning paradigms

(Gottfried, O'Doherty, & Dolan, 2002, 2003). We are the first to demonstrate that 142 emotional arousal can enhance episodic odor memory. This finding is consistent with reports of the facilitating role of emotional arousal on memory for other types of memoranda (Cahill & McGaugh, 1998; Sharot & Phelps, 2004). This effect cannot be explained as subjects using different response strategies for arousing odors, as there was no difference between response bias indices (C) for arousing and nonarousing odors.

However, we did not replicate the effect of emotional arousal on a different population sample and with a slightly different paradigm. In this second experiment, pleasantness and intensity influenced memory accuracy: intense and unpleasant odors were remembered better than weak and pleasant odors.

Only in Experiment 1 were odors that had been rated as more arousing remembered better than odors rated as less arousing, as shown by a higher discrimination index (d'). In Experiment 2, memory discrimination was marginally higher for arousing compared to nonarousing odors, but this difference was not significant. In both experiments, intense odors were remembered better than weaker ones. In the first experiment, relatively more variation in memory discrimination was accounted for by arousal (Partial Eta =.43) than when the same data were partitioned according to intensity {Partial Eta2=.,26). However, a direct comparison of the two did not show a significant difference. In contrast, in the second experiment the variation accounted for by intensity {Partial Eta2=.\5) appeared to be more important than that by arousal {Partial Eta2=.06), but this difference was also not significant. Moreover, we found that in 90 % of the participants in Experiment 1 and in 78% in Experiment 2, ratings of intensity and of emotional arousal were significantly and positively correlated.

Thus the effect that arousal has on memory discrimination may simply be an effect of intensity or vice versa; basically, intensity and arousal may be the same thing. Bensafi et 143 al. (2002a) have also found a strong positive correlation between ratings of arousal and ratings of intensity. Like them, we are tempted to suggest that in olfaction, intensity and arousal are connected to a similar phenomenon. Judgment of intensity would refer to the intrinsic property of the odorant while judgment of arousal would refer to the effect that the odor has on the subjective and autonomic state.

It has been demonstrated many times that sniffing an odorant modifies skin conductance. For example, some have found that skin conductance varied with odor concentration (Uryvaev, Golubeva, & Nechaev, 1986), with odor pleasantness (Alaoui-

Ismaili, Robin, Rada, Dittmar, & Vernet-Maury, 1997; Alaoui-Ismaili, Vernet-Maury,

Dittmar, Delhomme, & Chanel, 1997; Brauchli, Riiegg, Etzweiler, & Zeier, 1995), or with odor rated arousal (Bensafi et al., 2002a, 2002b). Our findings of increased phasic

SCR amplitude as a function of arousal and not of intensity or pleasantness are consistent with the demonstration of Bensafi and collaborators (2002a, 2002b), who investigated correlations between skin conductance variations and the dimensions of intensity, familiarity, pleasantness and arousal and found that skin conductance variations only correlated significantly with the arousal dimension of odors.

Our results do support the notion of a functional dissociation between intensity and arousal because our objective measure of autonomic arousal (phasic SCR magnitude) differed significantly only between smelling arousing versus nonarousing odors. There was no difference in phasic SCR when smelling odors rated as intense versus weak. This also suggests that the memory superiority that odors rated as arousing had over less arousing ones was driven by an autonomic arousal difference. Whereas the memory superiority for odors rated as more intense was most likely driven by a perceptual one.

Thus emotional arousal and intensity may enhance odor memory to a similar degree, but 144 not through the same processes. On one hand, intense odorants could be remembered better because they are easier to attend to and to be encoded. On the other hand, emotionally arousing odorants may be remembered better because they are efficient at capturing attention, leading to a better encoding. In addition, it has been reported that consolidation is enhanced for arousing stimuli (Cahill & McGaugh, 1998). If this is true for odors, then it should be possible to demonstrate better memory for emotionally arousing odors compared to nonarousing ones only after a certain time delay, while a retention delay would not affect memory for intense odors compared to weaker ones.

However, this hypothesis will be challenging to test because odors that are emotionally arousing also tend to be more intense.

It is a common procedure to ask participants to assess the perceived intensity of an odor on a rating scale. In methods similar to our use of SAM*SMELL, some researchers have asked participants to rate odor intensity with a nine point rating scale

(very weak-very strong) (Bensafi et al., 2002a), with a 10 cm scale labelled with words corresponding to minimal, moderate, medium, strong and maximal (Distel & Hudson,

2001) or with a six-point scale going from not detectable to very strong (Distel et al.,

1999). However, it might be argued that using rating scales to measure perceived intensity is a relatively weak method compared to the most stringent olfactory equivalence procedure (where participants have to assess an odor's intensity in relation to a reference odor). Nevertheless, olfactory equivalence procedures (magnitude estimation) are not without their limitations. For example, if the time between presentation of the test and the reference odors is too long or too short, memory of the reference odor can fade or olfactory adaptation can happen, distorting the participant's intensity evaluation (Doty & Laing, 2003). Moreover, when the variability, reliability 145 and ease of use are compared between more traditional rating scales (nine-point rating scale, line scale, etc.) and olfactory equivalence procedures, rating scales may be superior with untrained subjects (Lawless & Malone, 1986a, 1986b). Thus, given that the olfactory equivalence procedure is not without its disadvantages and given that our experiments involved untrained subjects in an incidental memory task (where there is the necessity of reducing potential interference), we considered that using a rating scale to evaluate perceived intensity was the most appropriate method. However, it could be interesting to use an olfactory equivalence procedure in future experiments investigating the effects of arousal or intensity on odor memory.

Because we did not find different response tendencies (C) as a function of arousal or intensity, our results may seem at odds with recent findings of overconfidence in the accuracy of memory for highly arousing stimuli. Talarico and Rubin (2003) found that subjects incorrectly believed that their memory of an arousing event, September 11th

2001, was more accurate than another memory from the same time period. Also,

Jonsson, Olsson & Olsson (2005) showed that subjects wrongly thought that they were naming odors accurately more often when the odors were more arousing. In the present experiments, overconfidence in memory for arousing odors would have been observed with a more liberal response bias index (increased tendency to respond yes) for arousing odors. However, some important differences between previous studies showing this effect and our investigation need to be considered. First, Talarico and Rubin (2003) measured the effect of emotional arousal on information that was not olfactory, whereas odor memory is believed to represent a unique and separate memory system (Herz &

Engen, 1996; Schab, 1991; Zucco, 2003). Second, with odor naming, Jonsson, Olsson &

Olsson (2005) were measuring knowledge, or semantic odor memory. Because we gave 146 subjects new odors to remember, our task targeted episodic odor memory. It is widely accepted that episodic and semantic memory systems are cognitively and neuroanatomically different (Shimamura & Squire, 1987; Squire, 2004; Tulving, 1989).

Some results of Experiment 2 may seem inconsistent with those of Experiment 1.

Of special interest are the findings of better memory for unpleasant odors and the absence of a significant memory enhancement for arousing compared to nonarousing odors. This first result provides no support for the rare claim that positive or pleasant events are remembered better than neutral or unpleasant ones (Matlin & Stang, 1978;

Wagenaar, 1986) but is consistent with the numerous reports of better memory for unpleasant information (Christianson & Loftus, 1987, 1991; Maratos, Allan, & Rugg,

2000; Talmi & Moscovitch, 2004). Because arousal ratings to sounds and pictures have been found to increase as a function of pleasantness (pleasant and unpleasant extremes)

(Bradley & Lang, 1999b; Lang, Bradley, & Cuthbert, 1999), unpleasant odors could also have been more arousing, suggesting again that arousal plays a role in memory enhancement. In both experiments, we uncovered a quadratic relationship between ratings of arousal and pleasantness (Table 4), meaning that odors rated as more pleasant or more unpleasant were also rated as more arousing. However, in both experiments, unpleasant and pleasant odors were initially partitioned to differ significantly only in their pleasantness ratings and not in their arousal ratings. Moreover, in Experiment 2, a direct comparison of memory discrimination for unpleasant with arousing and intense odors did not show a significant memory advantage for the arousing or the intense odors.

Charles, Mather & Carstensen (2003) have found a memory advantage for negatively valenced (or unpleasant) pictures compared to neutral or positive pictures in younger and not in older participants. Although our experiments were not specifically 147 designed to investigate whether there was an interaction between age and pleasantness on odor memory, our results suggest that the memory advantage of younger adults to unpleasant odors may not exist, or may even be reversed, in older adults. Only the participants of Experiment 2 remembered unpleasant odors better than pleasant ones and the participants of Experiment 2 were significantly older (M=33.6) than those of

Experiment 1 (M=20.5). An optimal use of cognitive resources (Hasher & Zacks, 1988) may explain why older adults show a memory advantage to unpleasant odors and not to unpleasant pictures. Unpleasant odors are more likely than unpleasant pictures to have a life or death consequence in everyday living (smelling spoilt fish versus seeing the picture of a decomposing animal), and arguably it seems more crucial to direct one's limited cognitive resources towards stimuli that can jeopardize life. This relative decline in cognitive resources may also give more impact to the "principle of negative potency" in olfaction. This principle, elaborated by Rozin & Royzman (2001), states that with positive and negative stimuli of equivalent magnitude, negative events are more salient, and consequently easier to remember. However, in Experiment 2, our participants were older but healthy and showed no evidence of declining cognitive resources.

Because arousal and intensity are not independent dimensions, older participants may show a somewhat decreased effect of arousal on odor memory related to the decline in olfactory sensitivity and intensity perception that accompanies normal aging (Cain &

Gent, 1991; Lehrner, Gluck, & Laska, 1999; Marks, 1988). However, this is unlikely to be the case here because the cohort of Experiment 2, although older, cannot be considered elderly, and clearly showed an effect related to intensity. But, previous research has shown that the ameliorating effect of arousal on memory for other types of stimuli persists across the lifespan and can even be found in demented individuals as 148 long as their amygdala is healthy (Comblain, D'Argembeau, Van der Linden, &

Aldenhoff, 2004; Mori et al, 1999).

It has been shown that the amygdala is necessary for emotional arousal to enhance memory. Patients suffering from Urbach-Weithe disease, a rare disease producing damage confined to the amygdala bilaterally, do not remember arousing information (i.e. pictures or stories) better than nonarousing information (Adolphs,

Cahill, Schul, & Babinsky, 1997; Babinsky et al., 1993; Cahill, Babinsky, Markowitsch,

& McGaugh, 1995). A few brain imaging studies also provide evidence that the amygdala has a selective role in the enhancement of memory for emotionally arousing events (Cahill et al., 1996; Canli, Zhao, Brewer, Gabrieli, & Cahill, 2000; Canli, Zhao,

Desmond, Glover, & Gabrieli, 1999; Hamann, Ely, Grafton, & Kilts, 1999). The main finding of those studies is that at encoding, amygdala activation is positively correlated with memory for emotionally arousing stimuli. Bridging nicely the lesion and neuroimaging studies to our finding of enhanced memory for emotionally arousing and intense odors are the results of Anderson et al. (2003). With event-related functional magnetic resonance imaging, Anderson et al. (2003) found that amygdala activation was associated with the intensity of an odor and not its pleasantness. In the frontal lobes, it was the opposite: activation was associated with the pleasantness of an odor and not its intensity. As we found that odor intensity and emotional arousal were associated with better odor memory discrimination (d'), it seems likely that the amygdala plays an important role in enhancing memory for arousing odors. Studies of patients with amygdala lesions will help answer this question. Patients with frontal lesions may provide a better model to study the effect odor pleasantness had on memory in our older participants. 149

Another point of difference, between Experiment 1 and 2 that might prove important to understand why pleasantness and arousal each influenced memory in one experiment but not the other, is the gender ratio. In Experiment 1, 57% of the participants where women; in Experiment 2 this ratio was 41%, and these ratios differed significantly (x2=9.14). Not only are differences observed between the genders in odor cognition (Brand & Millot, 2001), but the neurological basis of emotionally enhanced memory differs between men and women. In men accurate recall of arousing pictures

(such as a decaying animal) has been linked to greatest activity in the right amygdala. In women this relationship is greater with the left amygdala (Cahill et al., 2001; Cahill,

Prins, Weber, & McGaugh, 1994; Uncapher, Kilpatrick, Alkire, & Turner, 2004; Cahill

& van Stegeren, 2003; Canli, Desmond, Zhao, & Gabrieli, 2002; van Stegeren, Evaraed,

Cahill, McGaugh, & Goeren, 1998). However, in both experiments reported here, no gender difference was revealed in emotionally influenced odor memory. This may be because of a relatively small number of men and women in both experiments. Future research should focus on that promising question.

The enhancing effect of arousal on memory has been notably difficult to demonstrate, especially if the memory test is done through recognition and not recall

(Christianson, 1984; Christianson & Loftus, 1987). In a recognition test, all the information to retrieve is available to the subject. In this situation, the advantage given by the richer memory trace of emotionally arousing odors may become less relevant, eliminating or diminishing the enhancing effect of arousal on odor memory. We have used recognition tests in both experiments. With a more powerful recall test, we might have observed better memory for arousing odors more consistently. However, recall memory tests are not appropriate and rarely used in odor memory experiments because 150 they require that subjects recall, and possibly encode, odor names (Schab & Crowder,

1995c), confounding odor memory and memory for odor names.

The differences between Experiments 1 and 2 could also lie in their slightly different encoding procedures. In Experiment 1 participants smelled each odorant twice at encoding (first during autonomic recording and second during SAM*SMELL ratings), compared to only once in Experiment 2. Smelling each odorant twice probably led to a stronger or deeper encoding that may have favored arousing compared to nonarousing odors; while smelling each odorant once could have favored the intensity dimension.

Clearly, more experiments are needed to clarify this issue.

Because better memory for familiar odors is often reported (Oberg, Larsson, &

Backman, 2002; Rabin & Cain, 1984; Savic & Berglund, 2000; Schab & Crowder,

1995c; Sulmont, Issanchou, & Koster, 2002), familiarity could provide an alternative explanation to the enhancing effects of arousal, intensity and pleasantness on odor memory. Arousing and intense odors could have been remembered better because they were more familiar, or familiar odors could have been remembered better because they were more arousing. However plausible, this interpretation is not satisfactory because the correlations between ratings of familiarity and ratings of arousal (mean r=.38 and

.37, Experiment 1 and 2, respectively) and between ratings of familiarity and intensity

(mean r=.37 and .3, Experiment 1 and 2, respectively) were relatively low and significant in only approximately half of the participants (Table 4). An influence of familiarity underlying the effect of pleasantness seems more probable. Indeed, in both experiments, ratings of familiarity and pleasantness were significantly correlated in more than half of the participants (mean rs=.51 and .46, Experiment 1 and 2, respectively).

This positive correlation indicates that the more familiar an odor was, the more pleasant 151 it was also rated. But in Experiment 2 it was unpleasant and hence unfamiliar odors that were remembered better, a finding inconsistent with the favorable role familiarity is reported to play on odor memory.

The effect of semantic relatedness has been used previously to explain the memory enhancement observed for emotional stimuli. Talmi and Moscovitch (2004) postulated that emotional stimuli are naturally more interrelated than neutral information. Because interrelated information is remembered better than nonrelated information (Puff, 1970; Tulving & Pearlstone, 1966), it could be that emotionally arousing information would be remembered better mostly because it is more interrelated, and emotional arousal itself would play only a minor role in enhancing memory.

Language is an important, if not the preferred, tool to establish or identify relationships between items. As opposed to verbal or visual stimuli, odors are notably difficult to name; accuracy in naming odors rarely exceeds 50% (Cain, 1979; Engen, 1987).

Arousing odors might be easier to name than nonarousing odors; however, in our postexperimental questionnaire only two subjects reported naming or trying to name the odors at encoding, and they made no comment about arousal being helpful in naming.

Interestingly, Jonsson, Olsson & Olsson (2005) showed that people are not more accurate in naming arousing compared to nonarousing odors, but they are more confident that they are accurately naming arousing odors. Given the important difficulty associated with odor identification, we think semantic relatedness is an especially inadequate alternative explanation to the observed better memory for arousing odors.

Returning to the notion of remembering the smell of our first love better than that of our first lab mate, it may well be because their odor was intense or unpleasant

(probably not), but possibly (and hopefully) more because it was highly emotionally 152 arousing. Emotional arousal seems to enhance odor memory. As in other sensory modalities, the enhancing effect of emotional arousal on odor memory may not be straightforward. In other modalities, the type of memory test, the length of the retention interval and type of encoding play a determining role (Sharot & Phelps, 2004). How these factors influence emotional odor memory needs to be investigated. A better understanding of the differences and similarities between arousal and intensity in olfaction is also necessary.

* 153

Connection with Study 2

In Study 1,1 found evidence that odors provoking strong emotional reactions

(measured with SAM* SMELL ratings and SCR) were remembered better by healthy volunteers a week later than were odors provoking weaker emotional reactions. It was the first demonstration that emotional arousal can modulate odor memory.

The amygdala has been shown to be crucial for the enhancement of memory (for stimuli that are nonolfactory) by emotional arousal. Patients with amygdala damage do not benefit from the enhancing effect of emotional arousal on memory for pictures or words.

I investigated whether a healthy amygdala would be necessary to observe better memory for emotionally arousing odors. To do so, I tested the odor memory of patients who had undergone amygdala resection as part of a larger removal from the medial temporal lobe and compared their performance to that of matched healthy individuals.

Moreover, to understand better the role of the amygdala in the enhancement of memory for emotionally arousing odors, I analyzed performance as a function of amygdalar volume. 154

CHAPTER 5. STUDY 2

Medial Temporal-Lobe Damage and Memory for Emotionally Arousing Odors

Pouliot, S., and Jones-Gotman, M.

Montreal Neurological Institute, McGill University, Quebec, Canada

Pouliot, S., Jones-Gotman, M., Medial temporal-lobe damage and memory for emotionally arousing odors, Neuropsychologic! (in press, 2007). 155

Abstract

Recently, we found that healthy young adults remember odors leading to large emotional reactions better than odors provoking smaller emotional reactions. Because the amygdala is believed to be critically implicated in memory for emotionally arousing information and because it is part of the primary olfactory area, we hypothesized that patients with a unilateral medial temporal-lobe resection including the amygdala would not show enhanced memory for arousing compared to nonarousing odors. We tested odor memory in 19 patients (10 left, 9 right) who had undergone a unilateral medial temporal-lobe resection including the amygdala (MTLR) for treatment of intractable epilepsy and 19 healthy control subjects. Healthy individuals and patients with left or right MTLR showed comparable subjective emotional reactions to odors. Similarly, healthy individuals and patients with MTLR remembered unpleasant odors better than pleasant ones. However, unlike healthy individuals, patients with MTLR did not show better memory for emotionally arousing odors compared to nonarousing ones. Patients undergoing a MTLR, whether in the left or right hemisphere, lose the specific memory advantage that odors causing strong emotional reactions normally have. 156

Introduction

Everyday experience suggests that we remember highly emotional events better than neutral ones, and numerous studies have demonstrated that memory for emotionally arousing pictures or words is enhanced compared to memory for their neutral counterparts (for a review: Christianson, 1992). A growing body of research now indicates that the amygdala plays a critical role in this effect. Patients with bilateral or unilateral amygdala damage show normal emotional reactions when presented with emotionally arousing information such as graphic pictures or evocative words and stories; however, they do not show the expected enhanced memory for arousing information (Adolphs, Cahill, Schul, & Babinsky, 1997; Adolphs, Tranel, & Denburg,

2000; Brierley, Medford, Shaw, & David, 2004; LaBar & Phelps, 1998; Phelps, LaBar,

& Spencer, 1997). Functional neuroimaging studies reveal that amygdala activation during encoding correlates with how well stimuli are remembered, but this is only true for stimuli that are highly emotionally arousing (Cahill et al., 1996; Cahill et al., 2001;

Canli, Zhao, Brewer, Gabrieli, & Cahill, 2000; Canli, Zhao, Desmond, Glover, &

Gabrieli, 1999; Hamann, Ely, Grafton, & Kilts, 1999).

Being part of the primary olfactory area, the amygdala also plays a central role in odor processing (Jones-Gorman & Zatorre, 1993; Sobel et al., 2000; Zald & Pardo,

2000). For example, patients undergoing intracranial EEG studies show event-related potentials in the amygdala when they smell an odorant (Hudry, Ryvlin, Royet, &

Mauguiere, 2001). Patients with medial temporal-lobe damage show impairments on episodic odor memory tasks (Buchanan, Tranel, & Adolphs, 2003; Dade, Zatorre, &

Jones-Gotman, 2002; Jones-Gotman & Zatorre, 1993) and on odor identification (Jones-

Gotman et al., 1997). Functional neuroimaging studies demonstrate amygdala activation 157 when healthy subjects perceive odors, such as during the nondeclarative memory tasks of olfactory conditioning and extinction (Gottfried & Dolan, 2003, 2004).

Recently, we showed that healthy young adults remember odors leading to large emotional reactions better than odors provoking smaller emotional reactions. This effect was obtained when memory was tested after a week and was independent of how pleasant subjects rated the odors to be (Pouliot, Hudry, & Jones-Gotman, 2004). On a related note, using functional magnetic resonance imaging (fMRI), Anderson et al.

(2003) demonstrated that amygdala activation was associated with odor intensity and not with perceived odor pleasantness. However, in a recent fMRI study, Winston,

Gottfried, Kilner and Dolan (2005) showed that the amygdala was activated in response to intense pleasant and intense unpleasant odors, but not to intense neutral odors. We believe that these results, in conjunction with the previous findings, imply a critical role for the amygdala in the enhancement of memory for emotionally intense, or emotionally arousing, odors.

Considerable knowledge on the biological bases of memory has been gathered with postsurgical studies of patients submitted to unilateral resection from the medial temporal lobe for the relief of intractable epileptic seizures. Patients with unilateral temporal-lobe damage have been found to show subtle material-specific memory deficits

(e.g., Djordjevic & Jones-Gotman, 2004; Milner, 1965, 1970; Rausch, 1991). Few investigations of memory for emotionally arousing information have been conducted in patients with a surgical resection including the amygdala, and, of these few, none concerned odor memory. Those studies report that patients with resection including the left or the right amygdala rate the emotional dimension of stimuli (words or pictures) the same way healthy individuals do, but, unlike healthy individuals, they do not remember 158 arousing stimuli better than nonarousing ones (Adolphs, Tranel, & Denburg, 2000;

Brierley, Medford, Shaw, & David, 2004; Buchanan, Denburg, Tranel, & Adolphs,

2001; Frank & Tomaz, 2003; LaBar & Phelps, 1998).

Whether or not this deficit in emotional memory following unilateral temporal- lobe resection (MTLR) extends to odors is not known. The present study was undertaken to address this question. We hypothesized that patients with a medial resection from the temporal lobe (either a selective resection of amygdala and hippocampus (SAH) or a resection of amygdala and hippocampus including anterior temporal neocortex (CAH)) would show the same influence of odor pleasantness on memory (if there is one) as healthy individuals, but would not show enhanced memory for emotionally arousing compared to nonarousing odors. To test our hypotheses, we compared the performance of patients with either left or right MTLR and healthy individuals on an odor memory task using odors that produced, or did not, significant emotional arousal (measured with skin conductance and self-report ratings). Moreover, to understand better the role of the medial temporal lobe in memory for emotionally arousing odors, we analyzed patients' performance as a function of residual amygdalar and hippocampal volumes.

Method

Subjects

We tested 22 patients who had undergone anterior resection from a temporal lobe

(11 left [5 SAH and 6 CAH] and 11 right [7 SAH and 4 CAH]) for the relief of intractable epileptic seizures. As the extent of amygdalar and hippocampal removal did not differ significantly between SAH and CAH patients (see the results section), we treated them as a single group. We also tested a control group of 19 healthy individuals 159 matched for age, gender and education to the patient group. All healthy subjects were right-handed. One patient who had a left resection and two with right resection were left- handed, but all patients had typical left-hemisphere speech representation as shown by preoperative intracarotid amobarbital tests (Branch, Milner, & Rasmussen, 1964; Wada

& Rasmussen, 1960). All were tested a year or more after surgery and most were seizure-free or had rare seizures (17 were Engel class 1, 4 were Engel class II and one was Engel class IV; (Engel, Van Ness, Rasmussen, & Ojeman, 1993)). Exclusion criteria included infection obstructing the upper nasal airways, respiratory allergies, anosmia

(defined with an odor detection task), or cerebral abnormality extending beyond the temporal lobe. Three patients were excluded from the experiment; one was found to be anosmic (right resection), one had cortical malformations outside the temporal lobe

(right resection) and a third did not show up for the second experimental session (left resection). Thus, we present behavioural data for 19 patients who did not differ significantly on any individual characteristic (Table 5). It was possible to obtain MRI scans and psychophysiological recordings for only 16 patients. MRI scans and psychophysiological recordings were not available for the healthy participants. The study was approved by the Montreal Neurological Institute and Hospital Research Ethics

Board. All subjects gave informed consent. ) 160

Table 5 Characteristics of Retained Participants and Availability of Experimental Data

Group N Resection type Engel class Age Educ FSIQ Psychophys. MRI Left Right W M W M W M available amygdala/ amygdala/ hippocampus hippocampus

Healthy 10 9 39.3 13 Participants (±10) (±1)

Left 4 6 3 SAH 1 SAH 2 SAH: All are 43 14 94 8 (3 W) 8 332.1mm3 1234.4 mm3 Resections 1CAH 5CAH Engel I; Engel I (±7) (±4) (±9.8) (3W) (± 225.2) / (± 129.5) / 1 SAH: 2217.1 mm3 4207.2mm3 Engel IV; (±1596.8) (± 402.3) 1 CAH: Engel II

Right 6 3 6 SAH 1 SAH 5 are All are 40 12.8 88 8(5W) 8 1267.4mm3 214.6 mm3 Resections 2CAH Engel I; 1 Engel I (±10) (±2.6) (±7.8) (5W) (±218.1)/ (± 162.8) / is Engel II 4266 mm3 1161.9 mm3 (± 514.7) (± 852.6)

Note. W, women; M, men; SAH, selective amygdalohippocampectomy; CAH, corticoamygdalohippocampectomy; Educ, education in years; FSIQ, full scale intellectual quotient (£(17)=1.5, p=.\5); Psychophys., availability of psychophysiological data. For age, education, FSIQ and left and right amygdala volume, we report the mean and the standard deviation (in brackets). 161

Material

Odorants. Forty-two odorants were used (Table 6). They were selected from among 130 odorants that had been rated for intensity, pleasantness, familiarity and arousal by 41 healthy subjects in an earlier study (Pouliot, Hudry, & Jones-Gotman,

2003). The 42 odorants were divided into two equivalent sets (A and B) of 21 odorants, ranging widely in ratings of perceived intensity (A: M=5.9 / SD=0.9; B: 5.7 II), pleasantness (A: 4.8 /1.4; B: 4.8 /1.2), familiarity (A: 5.610.9; B: 5.6 /l), and arousal (A:

4.9 /0.8; B: 4.8 /0.7). The set of 21 odorants that was presented at encoding was the memory target set in the recognition test. Odorants from the other set served as foils during the recognition test. The specific odorant set being presented as targets or foils was counterbalanced across subjects.

All odorants were odor chemicals. With a few exceptions, we diluted odorants to

10 % in 4.5 ml of mineral oil. Odorants were presented in 30 ml amber glass bottles, in which a piece of polypropylene was inserted to absorb the odorant, to prevent spilling and to ensure a sufficient exchange with air. Odorants were kept refrigerated when not in use.

Test for general anosmia. The olfactory screening test was a forced-choice test with three alternatives and seven trials. It used three bottles, identical to those used during the odor memory test. One of the three bottles contained an odorant, phenyl ethyl alcohol (a rose-like odor), diluted to 10% in 4.5 ml of mineral oil, and the other two contained only mineral oil. The three bottles were presented in the same randomized order for all participants. On each trial, participants indicated which of the three bottles smelled strongest. Participants with fewer than 5 correct choices (out of 7) were

excluded from the experiment. One subject was excluded on this basis. 162

Table 6 Two Sets ofOdorants Used in the Memory Task B

Ambrarone Angelica root Anise Basil Banana Bois de rose Bergamot Carrot Black Pepper Citronellyl butyrate Butyric acid Coffee Cardamon Eugenol Cineole Galbanum oil Ethy-3-methy-3- phenyglicidate Garlic Freesia Guava Ham Mimosa Lime Musk ambrette Methyl 2-methylbutyrate Octyl acetate Methyl benzoate Orange Methyl ionone gamma Patchouly Mousse de chene Peru balsam Peanut butter Pine needles Pyridine Tarragon Styrax essence Thymol Viridine Trans-cinnamyl butyrate 2-heptanone ___ Verdone

Subjective ratings. A new pen-and-paper rating scale was used to measure subjective responses to perceptual and affective dimensions of the odorants (Figure 13).

Inspired by the Self-Assessment-Manikin (SAM; (Bradley, Greenwald, Petty, & Lang,

1992; Hodes, Cook, & Lang, 1985; Lang, 1980)), a well-known rating scale used in emotion research, the new "SAM* SMELL" scale retains the arousal {very calming- very exciting) and pleasantness {very unpleasant- very pleasant) dimensions of the original scale, but also includes intensity and familiarity dimensions. We implemented an intensity scale {very weak- very intense) because odor intensity is an important component of odor perception (Doty, 1975), and because perceived intensity was found to be highly correlated with both subjective and objective measures of arousal (Bensafi et al., 2002a). We added a familiarity scale {very unfamiliar-very familiar) because 163 familiar odors are often remembered better than unfamiliar ones (Savic & Berglund,

2000; Schab & Crowder, 1995c). For each dimension, five manikins are shown, with expressions conveying increases in the dimension being rated. Subjects rate the dimension by checking on one manikin, or between two of them, producing a nine-point scale. Six SAM* SMELL scales, each comprising the four dimensions, appeared on each page of a rating booklet.

Intensity •\n\u\ ^> JnOnOnOn! Pleasantness ? ? ?# # 5$t Familiarity

'nwnWnwDw Arousal

Figure 13. The SAM*SMELL pen and paper rating scale used to give subjective responses to odors. The pleasantness and arousal dimensions of SAM*SMELL are from Lang, P. J., 1980, Behavioral treatment and bio-behavioral assessment: Computer applications. In J. B. Sidowski, J. H. Johnson, & T A. Williams (Eds.), Technology in mental health care delivery systems (pp. 119-137). Norwood, NJ: Ablex Publishing. Copyright 1980 by Peter J. Lang. Adapted with permission.

Psychophysiology. We amplified and recorded skin conductance and breathing with a Power Lab 4 SP system using Chart 5 for Windows software (AD Instruments).

Skin conductance in microsiemens (uS) was recorded with bipolar nondisposable electrodes attached with velcro™ straps to the palmar surface of the middle segment of the index and middle fingers of the nondominant hand. The GSR amplifier was fully isolated and provided a low constant-voltage AC excitation (22 mV at 75Hz) on one of the two electrodes. Changes in breathing were monitored with a pressure transducer

(PTAFlite, Pro-Tech) fitted to a cannula (Pro-Flow, Pro-Tech) placed at the nostrils. 164

The first important increment in breathing that occurred after presentation of an odor determined when an experimental odor had been sniffed. This increment in sniffing volume corresponded to a positive deflection of the breathing waveform. We examined the different magnitude in phasic skin conductance responses (SCR) during the 10 s after which an odor was sniffed. We subtracted the mean skin conductance magnitude, for each odor, during the 3 s preceding sniff detection (baseline) from the mean skin conductance magnitude in the subsequent 10 s. In a way similar to Bensafi and collaborators (2002a;, 2002b), our prestimulus and poststimulus intervals differ. We chose a 10 s poststimulus window because SCR is relatively slow to rise and we wanted to be certain the maximal phasic value would be included. The subtraction was done to minimize the influence of a general increase in tonic skin conductance. We normalized these differences in mean phasic skin conductance magnitude with log transformations

[logio(SCR+l)] (Dawson, Schell, & Filion, 2000; Venables & Christie, 1980).

Procedure

Odor memory. The experiment comprised two sessions: one for incidental encoding and a later one for a recognition test. Further, the incidental encoding session was divided into two parts; a first part for skin conductance measurements while smelling odors, and a second part for odor rating. We chose to split the incidental encoding session into two successive parts in order to obtain the psychophysiological measures when an odor is first sniffed uncontaminated by interference from hand movements and other cognitive processes that would occur during odor ratings.

In the first part of the incidental encoding session, skin conductance and breathing were recorded while subjects smelled each of the 21odorants. Participants were told that the goal of the experiment was to study their emotional reactions when smelling 165 different odors and that their only task was to sniff when a bottle was placed under their nose. They were also told that they should refrain from talking and moving, sniff each odor the same way, and that they should look straight ahead during this part of the experiment. Before the psychophysiology recording, participants washed and dried their hands (Venables & Christie, 1973). Subjects wore earplugs during the experiment to reduce extraneous stimulation. They were seated comfortably on a chair with an arm rest in a quiet testing room, and the skin conductance electrodes and the cannula to monitor breathing were installed. Participants were trained to sniff when the experimenter placed a bottle under their nose. Once they managed to sniff without moving or looking at the bottle, the experiment began with a three-minute relaxation period. After the relaxation period, the experimenter, who was located beside the participant, began presentation of the 21 odors. Odorants were presented individually in bottles 1cm under the nostrils for three seconds, with an interstimulus interval (IS I) of 45 seconds, in a randomized order.

Half of the subjects received odorant set A and the other half odorant set B. All testing was birhinal.

In the second part of the incidental encoding session, after the skin conductance and breathing recordings, participants were freed from the electrodes and the cannula and were asked to move to a desk. Participants were told that they would smell again the odors and that their task was now to judge each odor with SAM*SMELL for intensity, pleasantness, familiarity and the degree to which they found the odors emotionally arousing. Again, the experimenter presented each odorant for three seconds and the ISI was at least 45 seconds. Also, participants were told that they had to be attentive because they would smell each odorant only once to rate all four dimensions. The future odor recognition test was never mentioned. 166

An unexpected recognition-memory test took place one week later. Forty-two odorants (21 targets and 21 foils, or all odorants from Sets A and B) were presented for approximately three seconds each, in a pseudorandom order such that no more than three targets or three foils were presented consecutively; ISI was again 45 seconds. For each odorant presented, subjects had to state whether or not they remembered smelling that odorant during the first experimental session. Following the odor memory test, we screened subjects for general anosmia. We used this order to prevent interference or confusion from the odor used in the anosmia test with the memory test odors. Finally, in a postexperimental questionnaire, we asked subjects about their experience in the study.

Amygdalar and hippocampal measurements. MRI scans of 16 MTLR patients were acquired with a 1.5 Tesla Siemens Vision scanner. Ti weighted scans were used. They were corrected for magnetic field nonuniformities (Sled, Zijdenbos, & Evans, 1998), underwent a linear stereotaxic transformation into Talairach coordinates (Collins,

Neelin, Peters, & Evans, 1994; Talairach & Tournoux, 1988) and were resampled into a

lmm voxel grid. We assessed amygdalar and hippocampal volumes using DISPLAY

(segmenting software developed at the Brain Imaging Center of the Montreal

Neurological Institute) and with recommended anatomical landmarks (Pruessner et al.,

2000).

To evaluate intrarater reliability, one of the raters (S.P.) measured six brains three times each. The time interval between successive measurements was approximately one

week. The rater was blind to the identity of the brains she was measuring and to the

corresponding odor memory performance. The brains were pseudorandomly chosen to

have an equal number of left and right resections. 167

Results

An alpha level of .05 was used for all statistical tests, and when we report post hoc multiple comparisons, the/?-values are based on Bonferroni adjustments.

Raw Memory Data

First, we wanted to determine whether patients with a left or right resection, compared to healthy control subjects, demonstrated a general odor memory impairment.

We conducted a one way ANOVA with subject group (healthy, left or right resection) as the between-subject variable on the number of hits, misses, false positive errors and correct rejections. We found no significant differences between subject groups (hits:

F(2,34)=1.94,/?=.16; misses: F(2,34)=l.9,p=A7; false positive errors: F(2,34)=1.51, p=.23; correct rejections: F(2,34)=1.51,/?=.23) (Figure 14). Because we found no significant difference between the left and right MTLR groups in this initial analysis, and to increase statistical power, we present most results collapsed for side of resection. 168 21

18

CM 15 II X

12 • healthy participants o B left MTLR O a right MTLR

0) .Q E c

0 hits misses false positive correct errors rejections

Figure 14. Raw odor memory scores as a function of subject group. There was no significant difference between groups. Error bars express standard error of the mean.

Amygdalar and Hippocampal Measurements

Intrarater reliability was calculated with intraclass correlations (Shrout & Fleiss,

1979). Intraclass correlations approach 1 when the within-subject variability is low, or

when the judge is consistent. We calculated intraclass correlations for the left and right

total amygdala volumes. We calculated intrarater reliability for amygdala volume and

not for hippocampus volume because due to its position in the superomedial temporal

lobe, definition of amygdala borders in MRI is especially difficult and may be prone to

more variability (Pruessner et al., 2000). The results revealed that the rater was 169 consistent (left=.98 and right=.96), and therefore our anatomical measures can be meaningfully included in other statistical analyses.

To investigate further the relationship between the medial temporal lobe and odor memory, we conducted a correlational analysis between the left and right amygdala, the left and right hippocampus and d' total, d' for arousing odors and d' for nonarousing odors. No correlation between brain structures and memory measures was significant

(Appendix C).

To verify whether the volumes of remaining amygdala and hippocampus differed between SAH and CAH, we conducted a univariate ANOVA with type of resection

(SAH, CAH) as the between-subject variable on the volumes of remnant amygdala and hippocampus. There was no difference (amygdala: F(l,14)=1.15,_p=.3, hippocampus:

F(l,14)=0.16, p=.l). To verify that patients with left or right resection did not differ significantly in volume of remaining amygdala or hippocampus, we conducted a univariate ANOVA with resection side as the between-subject variable on the volumes of the remnant amygdala and hippocampus and found no significant difference

(amygdala: F(l,14)=0.49,/?=.49; hippocampus: JF(l,14)=1.68,p=.21). We also wanted to verify that patients with a left resection had smaller amygdala and hippocampus on the left side than on the right side, and vice versa. To do so, we performed four paired t- tests. The first two sets of t-tests were conducted in patients with left resection. In one, we compared the volumes of the left and right amygdala and in the other the volumes of the left and right hippocampus. Volumes of left amygdala and hippocampus were smaller than volumes of right amygdala and hippocampus in patients with resection in the left medial temporal lobe (amygdala: t(l)=1.12,p=.0Q0\, hippocampus: t(7)=3.,95, p=.006). We conducted the same sets of paired t-tests in patients with resection in the 170 right medial temporal lobe. Volumes of the right amygdala and right hippocampus were smaller than volumes of the left amygdala and hippocampus in patients with a resection in the right medial temporal lobe (amygdala: ^(7)=12.33,/?=.0001, hippocampus :

£(7)=10.73,/?=.0001). Because these analyses showed that patients had an equivalent total volume removal, irrespective of resection type and side and that both patient groups had significant removals, we think that combining the patients groups is justified. For example, if only the left-sided resections had a significant removal, an odor memory deficit in the combined group would be difficult to explain given the advantage the right hemisphere is believed to have in odor processing. Conversely, if only patients with right resections had a significant removal, it would be ambiguous whether to attribute any observed odor memory deficit to the volume removed or to the side of resection.

Having two groups with equivalent volume removal liberates us from these questions.

SAM*SMELL Ratings

Individual correlations. To investigate whether there was a relationship among the different odor dimensions, we conducted a correlative analysis among the

SAM*SMELL ratings of intensity, familiarity, pleasantness and arousal. We conducted separate analyses for each individual subject, including the healthy participants and

MTLR patients. Because of an a priori hypothesis regarding the direction of each correlation, we performed one-tailed tests. We were expecting positive and linear correlations between ratings of intensity and arousal (Bensafi et al., 2002a) and between ratings of familiarity and pleasantness and ratings of familiarity and intensity (Royet et al., 1999). Because Distel and collaborators (1999) found a positive linear correlation between familiarity and strength of hedonic judgment (a concept close to emotional arousal) we were expecting a positive and linear correlation between familiarity and 171 arousal. Finally, given that a visual inspection of ratings of pleasantness and intensity reported by Royet et al. (1999) strongly suggests a positive quadratic correlation, and given the conceptual similarity between intensity and arousal, we predicted positive quadratic correlations between ratings of pleasantness and intensity and between ratings of pleasantness and arousal. Table 7 depicts the Pearson's correlations averaged across participants, the range of correlations and the proportion of participants whose

correlation was significant (within each of the two [healthy, combined patients] subject

groups).

We conducted binomial tests to determine whether the proportion of participants within each group having a significant correlation to each pair of SAM* SMELL

dimensions was different from chance (or reliable). They were significant in every case

(all/?s<.0001), meaning that ratings obtained with SAM*SMELL are valid and

informative because they accurately replicate the relations shown previously (Bensafi et

al., 2002a; Distel et al, 1999; Royet et al, 1999). 172

Table 7 Pearson Correlations between SAM*SMELL Rating Dimensions for Healthy Participants and Patients with MTLR. Averaged across Participants, Range, Proportion and Percent of Significant Correlation (p<.05, one-tailed, df=19)

Rating dimension Pleasantness Familiarity Arousal

Healthy Participants (N=19)

Intensity r=.23 .3 .46 range =-.56 to .61 -.29 to .76 -.15 to .86 proportion 11/19(58%) 13/19 (68%) significant = 10/19 (53%)

Pleasantness .5 .3 .05 to .88 -.27 to .72 12/19(63%) 10/19 (53%)

Familiarity .33 -.46 to .73 13/19(68%)

MTLR (N=19)

Intensity r= .27 .38 .61 range = -.33 to .79 -.45 to .? .12 to .91 proportion 12/19 (63%) 15/19(79%) significant = 9/19 (47%)

Pleasantness .52 .36 .14 to .88 -.21 to .85 14/19 (70%) 12/19(63%)

Familiarity .37 -.57 to .79 11/19(55%)

Proportions of significant correlations: group differences. We conducted % tests to determine whether the proportions of significant correlations between SAM*SMELL ratings of intensity and pleasantness, of pleasantness and arousal, of intensity and arousal, of familiarity and intensity, of familiarity and pleasantness and of familiarity 173 and arousal differed between healthy individuals and MTLR patients. There was no significant difference; thus the pattern of correlations for odor ratings was equivalent in

MTLR patients and healthy individuals.

Odor Memory

Memory measures. For the specific investigation of how arousal and pleasantness influenced odor memory, we used memory discrimination (d') and response bias indices

(C). We also used d' and C to investigate the effects of intensity on odor memory. The d' is a bias free measure (Snodgrass & Corwin, 1988) that gives a clear estimate of memory accuracy because it takes into account correct recognitions (responding 'it is old' when presented with a target odor) and incorrect recognitions (responding 'it is old' to a foil).

The C is a measure of response tendency or bias. It is important to measure bias because abnormal bias is often a significant component of abnormal memory (Snodgrass

& Corwin, 1988) and may differ among odor dimensions. No response bias is present when C equals 0. A liberal bias, or a tendency to respond "it is old" when uncertain, corresponds to a negative C, while a conservative bias, or a tendency to answer "it is new" when uncertain, corresponds to a positive value.

Experimental groups. To obtain the two dependent variables, d' and C, we computed hit (correct recognition) and false positive error (incorrect recognition) rates.

We did this for odors partitioned into four groups: unpleasant nonarousing, unpleasant arousing, pleasant nonarousing and pleasant arousing. To obtain these four groups, we rank ordered the 21 target odors by pleasantness ratings for each subject. The ranks for odors given identical ratings were decided on the basis of subjects' mean pleasantness ratings for these odors. The 11 odors with the lowest pleasantness ratings were assigned 174 to the unpleasant group, and the other 10 to the pleasant group. Within each pleasantness group, odors were subsequently ranked by their arousal ratings. Again, ties in ranks were broken on the basis of subjects' mean arousal rating for these odors. The 6 odors with the lowest arousal ratings in the unpleasant group and the lowest 5 in the pleasant group were designated nonarousing odors; the remaining 5 odors in both unpleasant and pleasant groups were considered the arousing odors. The 21 alternate odors presented as foils during the recognition test were ranked ordered in a similar way (in order to calculate the corresponding four types of incorrect recognition/false positive rate), however average ratings given by subjects who had rated this alternate set at encoding were used.

Statistical plan. This procedure created odor groups with mean ratings differing significantly from each other (Appendix D). We then conducted two univariate

ANOVAs with pleasantness and arousal as within-subject factors and subject group

(healthy individuals, MTLR patients) as between-subject factor on d' and C.

Because arousal and perceived intensity were strongly correlated in most participants (Table 7) and because of the conceptual similarity existing between these two factors, we also investigated the effect of intensity, separately from arousal, on odor memory. To do so, we repeated on intensity ratings the rank ordering procedure we had performed on arousal ratings. Again, the odors were partitioned into four groups: unpleasant weak, unpleasant intense, pleasant weak and pleasant intense (this partitioning was not arbitrary because the ratings of pleasantness and intensity differed significantly among the four groups, see Appendix D). We conducted separate univariate

ANOVAs on d' and C, each with within-subject factors of pleasantness and intensity 175 and the between-subject factor again being subject group. The results of this analysis will be presented first.

Memory as a function of intensity and pleasantness: d\ We found a main effect of pleasantness on d' (F(l,36)=8.1,_p=.007) indicating that unpleasant odors were remembered better than pleasant odors. There was no effect of intensity (F(l,36)=3.67, p=.01) or of subject group (F(l,36)=1.37,/>=.25) on d'. There was no interaction between intensity and pleasantness (F(l,36)=0.54,/?=.47), intensity and group

(F(l,36)=2.37,p=A3), or between pleasantness and group (F(l,36)=0.57,/?=.46).

However, there was an interaction between intensity, pleasantness and group

(F(l,36)=5.48,£>=.02). Post-hoc comparisons revealed that MTLR patients remembered more unpleasant weak odors than did the healthy individuals (p=.04). More important, post-hoc comparisons also showed that healthy individuals, and not MTLR patients, remembered more unpleasant intense than unpleasant weak odors (p=.005) and than pleasant intense odors (p=.002).

Response bias as a function of intensity and pleasantness: C. This analysis showed no effect of pleasantness on C (F(l,36)=0.33, p=.51). However, there was a main effect of intensity (F(l,36)=4.59, p=.04), indicating that all subjects were more liberal with odors that they judged to be intense. There was no effect of subject group (F(l,36)=1.74, p-2), and no interaction; pleasantness and intensity (F(l,36)=1.3,/?=.26); pleasantness and group (F(l,36)=0.67,p=.42); intensity and group (F(l,36)=0.07,/?=.8), or pleasantness, intensity and group (F(l,36)=0.68,/?=.42).

Memory as a function of arousal and pleasantness: d'. Odor memory accuracy

(d') was again shown to be influenced by pleasantness (F(l,36)=6.43,/?=.02); unpleasant odors were remembered better than pleasant ones (Figure 15). There was no 176 effect of arousal (F(l,36)=0.92,/?=.34) nor of subject group on d'(F(l,36)=0.35,p=.56).

There was no interaction between pleasantness and arousal (F(l ,36)=0.7, ^=.41), between pleasantness and group (F(l,36)=0.51,^=.48), or between pleasantness, arousal and group (F(l,36)=0.008,/?=.93) on d'. However, the interaction between arousal and group approached significance (F(l,36)=2.65,p=.06; one-tailed). Because we had predicted a significant interaction between arousal and group, we carried out planned comparisons. They revealed that only healthy control subjects, and not MTLR patients, remembered arousing odors better than nonarousing ones (t(\8)=2.27,p=.04 and t(lS)=0A\,p=.69, respectively) (Figure 16).

Figure 15. Odor memory discrimination (d') as a function of pleasantness. Error bars express standard error of the mean.

• nonarousing • arousing

Figure 16. Mean odor memory discrimination (d') as a function of subject group and emotional arousal. Error bars healthy MTLR express standard error of the mean. participants 177

Response bias as a function of arousal and pleasantness: C. When we analysed response bias, no effect was significant (pleasantness: F(l,36)=0.05,/?=.83; arousal:

F(l,36)=3A6,p=.07; subject group: F(l,36)=1.32,p=.26; interaction between arousal and pleasantness: F(l,36)=0.23,/?=.64; interaction between pleasantness and subject group: F(l,36)=2.52,/?=.12; interaction between arousal and subject group:

F(l,36)=0.08, p=.78; and interaction between pleasantness, arousal and subject group:

F(l,36)=2.44,jp=.13).

Psychophysiology

We calculated the mean phasic SCR magnitude within each of the four pleasantness and intensity levels and within the four pleasantness and arousal levels for each patient (16 available). We carried out two univariate ANOVAs on the mean phasic

SCR magnitude. One ANOVA had pleasantness and intensity as within-subject factors and the other had pleasantness and arousal as within-subject factors. We found no effect of pleasantness on phasic SCR (F(l, 15)=1.8, /?=. 19). We found that individuals with

MTLR showed a larger phasic SCR when smelling odors that they had rated as intense

(M=0.12) compared to weak (M=0.1) (F(l,l5)=5.6,p=.03). However, they did not show a larger phasic SCR when smelling odors they had reported to be arousing

(M=0.11) compared to those reported as nonarousing (M=0.11) (i7(l,15)=0.04,p=.84).

7 There was no interaction between pleasantness and intensity (i (l,15)=0.12,jp=.74), or between pleasantness and arousal (F(l,15)=2.02,/?=.18). These SCR values may seem alike, but they differ significantly on the intensity dimension (Partial Eta =.29, indicating that intensity accounted for 29% of the variability in magnitude of phasic

SCR). Moreover, it must be kept in mind that they were log transformed and that they 178 represent the mean magnitude difference in SCR between before and after an odor is smelled (hence phasic SGR).

Discussion

We found that unilateral medial temporal lobe resection including the amygdala is associated with a specific impairment in odor memory. This impairment was specific because no difference in memory between healthy individuals and MTLR patients could be observed when the total number of odors remembered, or global odor memory, was considered. This odor-memory impairment was limited to the predicted memory enhancement for arousing compared to nonarousing odors. We demonstrated that healthy individuals remember odors better when they are emotionally arousing than when nonarousing, and when they are unpleasant compared to pleasant. Whereas MTLR patients also remember unpleasant odors better than pleasant ones, they do not show enhanced memory for arousing compared to nonarousing odors.

The lack of memory superiority for emotionally arousing odors in our MTLR patients is consistent with other studies demonstrating that patients with unilateral or bilateral amygdala damage have impaired memory for emotional stimuli (Adolphs,

Cahill, Schul, & Babinsky, 1997; Adolphs, Tranel, & Buchanan, 2005; Adolphs, Tranel,

& Denburg, 2000; Phelps, LaBar, & Spencer, 1997; Richardson, Strange, & Dolan,

2004). However, the present study is the first to indicate that the reduction in memory enhancement for emotional information after MTLR extends to odorants.

Several studies have shown that medial temporal-lobe damage disturbs odor discrimination, odor identification and odor memory (Eskenazi, Cain, Novelly, &

Friend, 1983; Jones-Gotman & Zatorre, 1988, 1993; Jones-Gotman et al, 1997;

Martinez et al., 1993; Zatorre & Jones-Gotman, 1991). These deficits were generally 179 observed when odors were sniffed monorhinally, using the nostril ipsilateral to the resection (but see Jones-Gotman & Zatorre, 1988, 1993). In the present experiment, we did not observe any global odor memory deficit, and one reason may be because our subject sniffed odors with both nostrils.

Another possible reason why we did not observe any global odor-memory deficit may be a floor effect that obscured group differences. We think the floor effect explanation is an unlikely one given that, although relatively low, odor memory performance in our task was not at chance (Appendix E). A more likely possibility would be that in studies where a global odor memory deficit was found, what was really observed was a memory deficit for odors that led to a greater emotional arousal.

However, because this variable was not controlled for, it could not be used as an argument for or against any effect of emotional arousal or pleasantness on odor memory.

Although we made certain that our odors differed maximally on the dimension of emotional arousal, an alternative explanation to our finding of better memory for arousing odors in healthy individuals could be that arousing odors were remembered better because of some other property. For example, arousing odors could have been easier to name, and consequently easier to remember. This alternative explanation appears unlikely, considering the findings of Jonsson, Olsson & Olsson (2005) who showed that although subjects believed they were naming more accurately odors they found arousing, they also were, in fact, overconfident; their naming was not more accurate for arousing than for nonarousing odors. In addition, in our postexperimental questionnaire, no subject reported naming the odors as a way to remember them. Had participants named arousing odors to remember them, we might have observed a special impairment in subjects with left resection given their known deficit in learning and 180 retention of verbal material (e.g., Djordjevic & Jones-Gotman, 2004; Hermann, Wyler,

Bush, & Tabatabai, 1992; Milner, 1968). But this was not the case.

Another dimension that comes to mind as an alternative hypothesis to the effect of arousal is perceived intensity, especially as ratings of arousal were correlated with intensity ratings in most participants. However, examination of the discrimination index

(d') and response bias (C) data reveals that participants did not remember intense odors better than weak ones and that they were more liberal with intense compared to weak odors; that is, they made more incorrect recognitions to intense than to weak odors. In contrast, we do not find this difference in response bias as a function of arousal. Odor intensity seems to enhance the tendency to respond positively when presented with an intense odor rather than enhancing memory recognition per se. The intensity explanation for the memory enhancement is even less likely given the extensive evidence indicating a clear effect of emotional arousal on memory for other types of stimuli (Adolphs,

Cahill, Schul, & Babinsky, 1997; Adolphs, Tranel, & Buchanan, 2005; Adolphs, Tranel,

& Denburg, 2000; LaBar & Phelps, 1998). Although correlated, intensity and arousal represent a distinct, perceptual or affective, dimension in human olfaction.

The interaction between intensity, pleasantness and subject group, in which MTLR patients were found to have better memory than did healthy participants for unpleasant weak odors, is worth mentioning. Superior performance of MTLR patients compared to healthy individuals on any odor memory measure is highly surprising. However, a closer examination of their memory performance reveals that if MTLR patients were better than the healthy subjects on memory for unpleasant weak odors, it was probably largely due to the fact that they remembered odors they had judged to be weak as well as they 181 remembered odors they had judged to be more intense. In contrast, the healthy subjects had better memory for intense than weak unpleasant odors.

A final possible explanation for the differential effect of arousal on odor memory for healthy participants and individuals with MTLR could be perceptual differences, or a primary sensory loss. For example, patients might have had a global odor detection deficit. We controlled for this eventuality by screening all participants for general anosmia. Based on this screening we had to exclude only one patient from the experiment. Further, like healthy participants, patients were able to respond differentially according to odor intensity (intensity ratings and C index). Additionally, patients could also have not experienced different arousal to different odors, and consequently not reported differential ratings to arousing and nonarousing odors.

However, the odor arousal ratings of patients were comparable to those of the control group, a finding consistent with reports of a dissociation between experience of emotion and memory for emotional information (Adolphs, Cahill, Schul, & Babinsky, 1997;

Brierley, Medford, Shaw, & David, 2004).

We had predicted the arousal difference in odor-memory discrimination between healthy individuals and patients with amygdala resection. However, we did not expect better memory for unpleasant odors in healthy or MTLR subjects because usually pleasantness is not found to influence odor recognition memory (Lawless & Cain, 1975;

Sulmont, Issanchou, & Koster, 2002). But many teams have reported a strong positive association between familiarity and pleasantness (Ayabe-Kanamura et al., 1998; Jellinek

& Koster, 1979,1983; Royet et al., 1999), and familiar odors tend to be remembered better than unfamiliar odors (Rabin & Cain, 1984; but see Engen & Ross, 1973; Lawless

& Cain, 1975). If familiar odors are more pleasant and familiar odors are remembered 182 better, we should have observed better memory for pleasant odors. In fact, subjects found familiar odors more pleasant because the correlation between ratings of familiarity and pleasantness was positive in all subjects (M=.51, range=.05-.88, significant in 68% of MTLR and healthy participants). However, in the present study it was unpleasant odors that had the memory advantage.

Also, it could be argued that healthy participants remembered arousing odors better because they were more familiar. However plausible, this interpretation is not satisfactory because the correlations between ratings of familiarity and ratings of arousal

(mean r=.33, range=-.46 to .73, significant in 68% of healthy participants) were relatively low and not in the same direction for all participants. This means that for some participants, the more familiar an odor was the more arousing it was; for others, the opposite was true. Thus, the effect of arousal on odor memory cannot easily be reduced to a familiarity effect.

The finding that patients with MTLR remember unpleasant odors better than pleasant odors, as do healthy participants, is consistent with reports indicating that the amygdala processes mostly intensity and arousal and not the pleasantness of olfactory information (Anderson et al., 2003; Winston, Gottfried, Kilner, & Dolan, 2005). The few functional neuroimaging studies that investigated the neural basis of odor hedonic judgments revealed different patterns of activation. Zald and Pardo (1997) found activity in the left orbitofrontal cortex and the amygdala bilaterally when participants were smelling very unpleasant odors. Royet et al. (2000) reported activation in the left orbitofrontal cortex, the left temporal pole, the left superior frontal gyrus, the hypothalamus, the subcallosal gyrus and the amygdala bilaterally when participants judged hedonic qualities of odors. Zatorre, Jones-Gotman and Rouby (2000) reported 183 activation in the right orbitofrontal cortex and the hypothalamus when participants made pleasantness judgments to pleasant and unpleasant odors. Bensafi and colleagues (2002;

2003) investigated hemispheric specialization in the processing of odor pleasantness using a different approach. In their studies, subjects were faster to judge the pleasantness of an unpleasant odor than of neutral or pleasant odors when this odor was presented to the right nostril. This was not true for the left nostril. Because the olfactory nerve projections are mostly ipsilateral (Price, 1990), Bensafi's results support a right- hemisphere advantage in the processing of unpleasant odors. To date, there is no consensus as to whether there is hemispheric specialization or not in judgment of odor pleasantness, but it seems clear that a neural network that goes beyond the medial temporal lobe structures is involved.

We measured autonomic responses of patients with MTLR during odor encoding.

We found that they did not show a larger phasic SCR to odors they had rated as being more arousing. This was surprising, given that we were expecting no difference in patients reactions of arousal and that a strong association between arousal ratings and

SCR has been reported (Bensafi et al., 2002a). In contrast, MTLR patients did show a larger phasic SCR to odors they had rated as intense compared to weak ones, but this was not accompanied by an enhancement in memory for intense odors. In healthy subjects, increased SCR has been associated with better memory (e.g., Corteen, 1969;

Craik & Blankstein, 1975). Therefore, autonomic arousal does not seem to modulate odor memory in the absence of healthy medial temporal-lobe structures (i.e., hippocampus and amygdala) in one cerebral hemisphere.

We found no correlation between odor memory (global, nonarousing or arousing) and amygdalar or hippocampal volumes. These negative results probably reflect a lack 184 of statistical power due to the relatively small number of MRI scans (16) available for analysis. It seems unlikely that this lack of correlation was due to inaccuracies in measurements because the anatomical volumes were made by closely following a standard protocol (Pruessner et al., 2000) and the reliability coefficient was high. As it is generally acknowledged that the amygdala is important for odor memory (Babinsky et al., 1993; Buchanan, Tranel, & Adolphs, 2003; Markowitsch et al., 1994) and that the right hemisphere has a relative advantage in olfactory processing (Eskenazi, Cain,

Novelly, & Friend, 1983; Jones-Gotman & Zatorre, 1988, 1993; Jones-Gotman et al.,

1997; Martinez et al, 1993; Zatorre & Jones-Gotman, 1990, 1991; Zatorre, Jones-

Gotman, Evans, & Meyer, 1992), future researchers might find distinct correlations between type of odor memory and brain structure using a larger sample. A possible pattern of findings could be correlation between the right amygdala and memory for arousing odors in the absence of such a relationship with the right hippocampus.

However, because a different role for the left and right amygdala in men and women in the enhancement of memory for arousing information has been reported (Cahill et al.,

2001; Canli, Desmond, Zhao, & Gabrieli, 2002), it would be instructive to analyse these data separately for each gender.

Our findings cannot unambiguously implicate the amygdala as the unique structure responsible for the enhancement of memory for emotionally arousing odors. In no patient was the surgery limited to a unilateral removal of the amygdala. In all cases there was additional surgical removal of the surrounding medial temporal lobe. Our may reflect the effects of an underlying pathology in temporal lobe epilepsy, cerebral reorganization after life long epilepsy or a disconnection, consecutive to resective surgery, in some odor/hedonic circuit. Nevertheless, because MTLR patients 185 did not show a general odor memory deficit, because their impairment was restricted to the enhancement in memory for arousing and not for unpleasant odors and because of converging evidence from neuroimaging and brain lesion studies, our findings suggest that the amygdala might play a pivotal role in the enhancement of memory for emotionally arousing odors, like it does for other types of sensory information. The investigation of the influence of emotional arousal on odor memory is just beginning and unanswered questions abound. Future neuroimaging studies of this phenomenon should enrich our understanding. 186

Connection with Study 3

In Study 2,1 found evidence that the amygdala was necessary to enhance memory for emotionally arousing odors. I obtained these results with an experimental paradigm in which learning was incidental and odor memory was tested approximately a week later. In Study 1 too, learning was incidental and memory was tested after a long retention interval. These two conditions are implemented in most studies of the enhancing effect of emotional arousal (for nonolfactory stimuli), because they generally lead to less ambiguous results.

In Study 3,1 investigated whether these manipulations were necessary to obtain enhancement of odor memory by emotional arousal. In the first experiment, subjects had to recognize odors immediately after encoding and after a week long retention interval.

In the second experiment, subjects' odor memory was tested after incidental and after intentional encoding. 187

CHAPTER 6. STUDY 3

Odor Memory and Emotional Arousal: A Role for Retention Interval and Learning Intention?

Pouliot, S. and Jones-Gotman, M.

Montreal Neurological Institute, McGill University, Quebec, Canada

This work has been submitted for publication to The Quarterly Journal of . 188

Abstract

In nonolfactory sensory modalities, enhancement of memory by emotional arousal is typically observed after incidental encoding and delayed memory tests. In two separate experiments, we assessed whether these conditions are necessary for emotional arousal to enhance odor memory. In the first experiment, we found that a long retention interval is not necessary to enhance memory for emotionally arousing odors. In the second experiment, we found that memory for arousing odors is better than memory for nonarousing odors after intentional learning instructions. Our findings suggest that incidental learning and a long retention interval may not be necessary for emotional arousal to enhance odor memory. Moreover, depending on the pleasantness of the odor, emotional arousal would seem to enhance memory through different processes. For arousing unpleasant odors, consolidation processes may be more involved, whereas for arousing pleasant odors, attentional influences may be more important. 189

Introduction

The powerful experience of unexpectedly smelling the perfume of a person we loved makes it clear that a strong relationship exists between emotions, odors and memory. Literary and experimental evidence in support of this association abound. In "A la recherche du temps perdu"', Marcel Proust (1913), an author popular in the community of scientists investigating odor cognition and emotions, describes a particularly vivid and emotional childhood memory triggered by a bite of a tea-soaked piece of cake. This rich multi-sensory experience has motivated many scientific investigations. Some report that we remember odors relatively well over a long time interval (Engen & Ross, 1973), others that what odors remind us of is more emotional than reminders from other modalities (Herz & Cupchik, 1995; Herz, Eliassen, Beland, &

Souza, 2004; Herz & Schooler, 2002; Rubin, Groth, & Goldsmith, 1984), or that odors

are especially efficient cues to memories that are both older and more emotional (Chu &

Downes, 2000a, 2000b, 2002).

In the nonolfactory literature, the influence of emotions on episodic memory has

been studied extensively. Emotions have multiple effects on memory (Reisberg &

Heuer, 1995). The enhancement of memory by emotional arousal has been the focus of

numerous experiments (Bradley, Greenwald, Petry, & Lang, 1992; Brewer, 1988;

Christianson, 1992; Sharot & Phelps, 2004). However, our laboratory was the first to

investigate whether emotional arousal influences odor memory (Pouliot, Hudry, &

Jones-Gotman, 2004). In most studies that successfully obtained an enhancing effect of

emotional arousal on memory, the encoding was incidental and the effect of arousal was

stronger after a long retention interval; therefore we designed a similar experimental 190 paradigm. During an encoding phase, subjects simply smelled different odors and assessed their emotional reaction to each one. All participants returned a week later for an unexpected recognition memory test. With this method, we found that odors rated as' more emotionally arousing and leading to a larger skin conductance response (SCR, a measure of autonomic arousal) were remembered better than odors that were less

arousing. The question we now ask is: are those conditions-incidental learning and a long retention interval-necessary for emotional arousal to enhance odor memory?

Emotional Arousal and Retention Interval

A well-known finding in the emotion and memory field is that of an interaction between emotional arousal and retention interval. Emotionally arousing stimuli (words,

stories or pictures) are usually remembered better than nonarousing ones after a

relatively long retention interval; in contrast, it is the nonarousing stimuli that are

remembered better immediately after incidental encoding (Kaplan & Kaplan, 1969;

Kleinsmith & Kaplan, 1963, 1964; Maltzman, Kantor, & Langdon, 1966; Osborne,

1972; Quevedo et al, 2003; Sharot & Phelps, 2004; Walker & Tarte, 1963). Because the

memory enhancement was observed after a long retention interval, it was suggested that

emotional arousal was influencing consolidation processes.

Numerous studies of the neural mechanisms underlying this effect of retention

interval strongly support a key role for consolidation processes. Adrenal hormones

released in consequence of emotionally arousing situations activate the amygdala, and

this amygdala activation is considered crucial to enhance memory consolidation of the

arousing situation (McGaugh, 2000). Cahill, Prins, Weber and McGaugh (1994) have

demonstrated that adrenergic activation was necessary for emotional arousal to enhance

memory. Also, unilateral or bilateral lesions to the amygdala impair the enhancement of 191 memory for emotionally arousing information (Adolphs, Cahill, Schul, & Babinsky,

1997; Adolphs, Tranel, & Denburg, 2000; LaBar & Phelps, 1998). Our initial finding of better memory for emotionally arousing odors could be accounted for by a modulation of consolidation processes. Indeed this enhancement was obtained after a long retention interval (a week), and consolidation of memories occurs gradually over time (McGaugh,

2000).

However, emotional arousal could also enhance odor memory by influencing attention during encoding. A few experiments support this alternate hypothesis.

Enhanced memory for emotional stimuli in several nonolfactory modalities has been observed immediately after incidental encoding (Christianson & Loftus, 1987;

Kensinger & Corkin, 2003; Maltzman, Kantor, & Langdon, 1966). Three phenomena could explain how emotional arousal influences attention. Easterbrook (1959) has proposed that arousal narrows attention. Narrowed attention focuses on the arousing details; these will be better encoded at the expense of the nonarousing details. Fox,

Russo, Bowles and Dutton (2001) showed that after seeing an arousing stimulus

(threatening face or word) it took subjects longer to detect another stimulus. Hence, arousing stimuli can hold attention and slow attentional engagement to subsequent stimuli. Finally, there are many indications that arousing stimuli are processed more efficiently, perhaps automatically (Christianson, 1992). For example, healthy individuals have enhanced perception of arousing compared to nonarousing words in attentional blink experiments (attention is limited due to rapid presentation of stimuli)

(Anderson & Phelps, 2001).

Because in our initial study of odor memory and arousal (Pouliot, Hudry, &

Jones-Gotman, 2004) we did not test odor memory immediately after incidental 192 encoding, a modulation of attention at encoding by emotional arousal cannot be ruled out. If arousal influences odor memory by altering attention during encoding, memory for emotionally arousing odors should be already superior at the immediate memory test.

Emotional Arousal and Encoding Instructions

In most studies of emotional arousal and memory, the learning instructions are incidental. At encoding, participants are not aware that their memory will be tested subsequently because researchers want to minimize, or control, the influence of rehearsal and other mnemonic strategies on emotional memory. Researchers also want to mimic the conditions of real life as much as possible, as we are seldom told what to remember. These preoccupations are so prevalent that the majority, if not all, of neuroimaging studies of this effect implemented incidental learning instructions (Cahill et al., 1996; Cahill et al., 2001; Cahill, Uncapher, Kilpatrick, Alkire, & Turner, 2004;

Canli, Desmond, Zhao, Glover, & Gabrieli, 1998; Canli, Zhao, Brewer, Gabrieli, &

Cahill, 2000; Canli, Zhao, Desmond, Glover, & Gabrieli, 1999; Hamann, Ely, Grafton,

& Kilts, 1999; Kilpatrick & Cahill, 2003).

Very few studies have looked at the impact intentional instructions would have on the enhancement of memory by emotional arousal. We are aware of three studies that have manipulated encoding instructions. In the first one, McLean (1969) conducted two experiments of paired-associate learning that differed in learning instructions; in one they were incidental and in the other intentional. McLean (1969) found that under incidental learning conditions, participants remembered more of the arousing pairs immediately and after one day. Compared with immediate recall, there was also more forgetting for the nonarousing than for the arousing pairs at the one-day recall. The 193 results were different with the intentional learning instructions. The arousing pairs were no longer remembered better than the nonarousing ones.

A second study of arousal and memory in which encoding instructions were manipulated was conducted by Heuer and Reisberg (1990). They compared memory for

12 pictures depicting either an arousing or a neutral story after a retention interval of 2 weeks. The stories were identical except for their middle part. Both depicted a little boy and his mother going to visit his father at work. In the neutral version, the father is a mechanic at the local garage and repairs a car that was towed in. In the arousal version, the father is a surgeon and operates on the severed limbs of an individual who had had a terrible car accident. In the incidental encoding condition, the group shown the arousing story was told only to attend to it, and that the researchers were interested in their physiological reactions to visual stimulation. In the intentional encoding condition another group was shown the neutral pictures and told that their memory for the pictures would be tested. The arousal-incidental group had better memory scores than the neutral-intentional encoding group. However, this effect was more evident for the middle part of the story, which used different pictures. The arousal-incidental group also remembered better the final pictures, which were the same for both groups. If the effect of arousal were attributable to rehearsal, the arousal-incidental group and the neutral- intentional group should have had equivalent memory for these final pictures. However

interesting, this study is not informative regarding the memory advantage that incidental

encoding might have over intentional encoding. Further, that experiment contained a

serious confound because the design was not orthogonal. Namely, memory for the

arousing story was tested only after incidental encoding and memory for the neutral

story was tested only after intentional encoding. Limiting interpretation of the results in 194

an additional way is the fact that there was no information to suggest that the different

pictures used in the intentional and incidental tests had been equated for memorability.

Finally, the third study of memory and emotional arousal that manipulated

learning intention consisted of two experiments in which participants were younger and

older adults (Kensinger, Piguet, Krendl, & Corkin, 2005). In both experiments, 40

composite pictures were presented. Each picture was made of a central and a peripheral

• part. Peripheral parts were either a small geometric shape or a background detail. Half of

the pictures had a neutral central part and the other half a negative central part. The

peripheral part was always neutral (e.g., central neutral: a man holding an ice cream

cone; periphery neutral: a lozenge in the top right corner; central negative: a man

holding a gun; periphery neutral: a dirt road in the background). One experiment used

incidental instructions-participants had to state whether they wanted to approach or

move away from each picture-and the other had intentional learning instructions-

participants were told to remember the pictures as well as they could. Fifteen minutes

later, participants were submitted to a recognition test consisting of central or peripheral

fragments of encoded or foil pictures. With incidental instructions, both subject groups

(young and old) were more accurate in their recognition of the central parts of the

negative compared to neutral pictures, but they also showed poorer memory for the

peripheral parts of the negative compared to neutral ones. With intentional learning

instructions, both groups again remembered more negative than neutral central elements.

However, only the younger group overcame the emotional attentional bias and

remembered peripheral elements of negative and neutral pictures equally well.

From these studies, it seems that a paradigm using incidental instructions is best

for eliciting the effects of emotion on memory. As Kensinger et al. (2005) suggested, 195 with incidental instructions emotionally arousing stimuli automatically grab more attentional resources, explaining why they are remembered more accurately than nonarousing stimuli. With intentional instructions, subjects can overcome the emotional attentional bias and devote equal attention (or cognitive resources) to arousing and nonarousing information. However, none of these experiments used odors as memory targets. We are aware of only one study in which odors were the memory targets and in which encoding instructions were manipulated, but that study did not focus on emotional arousal. Larsson, Oberg and Backman (2006) asked younger and older adults to smell a set of familiar and unfamiliar odors after incidental or intentional encoding instructions.

They report an interaction between odor familiarity and encoding instructions.

Unfamiliar odors were recognized better after intentional than incidental encoding whereas encoding instructions did not influence memory for the familiar odors.

According to Larsson, Oberg and Backman (2006) it is because unfamiliar odors are poor in semantic features that they could be remembered better with intentional

encoding.

The Present Study

The enhancing effect of emotional arousal on memory, for stimuli that are not

olfactory, appears to flourish in specific conditions. A relatively long retention interval

and incidental encoding seem to be its fertile ground. If odor memory represents a memory system different from the one implicated with other sensory modalities (Herz,

1998; Herz & Engen, 1996; White, 1998), is it reasonable to predict that with odors, the

enhancing effect of emotional arousal on memory will also be observed preferentially

after a longer retention interval and after incidental learning instructions? In two

experiments we tested whether these conditions are necessary to obtain the expected 196 enhancement. In Experiment 1, we measured the influence of retention interval by testing memory for arousing and nonarousing odors immediately and a week after incidental encoding. In Experiment 2, we assessed the influence of learning intention by testing odor memory after incidental and intentional learning instructions. As an additional way to assess the degree of emotional arousal, we also measured SCR during encoding and recognition in Experiment 2.

Experiment 1

Arousal and Retention Interval: Immediate versus Delayed

Method

Participants

Forty right-handed undergraduate students (20 women, mean age=21, range=18-

30) participated in this experiment. Exclusion criteria were infection obstructing the upper nasal airways, respiratory allergies, or neurological or psychiatric antecedents. A general anosmia test revealed that all participants had an adequate sense of smell (see below). All subjects gave informed consent.

Material

Odorants. Forty odorants were used (Appendix F). They were selected from among 130 that had been rated for intensity, pleasantness, familiarity and arousal by 41

subjects in an earlier study (Pouliot, Hudry, & Jones-Gotman, 2003). The 40 odorants were divided into two equivalent sets (A and B) of 20, ranging in ratings of intensity, pleasantness, familiarity and arousal, as shown in Table 8. The 20 odorants that were presented at encoding comprised the memory target set in the recognition tests. Odorants 197

from the other set served as foils during recognition. The specific odorant set being

presented as targets or foils was counterbalanced across subjects.

Table 8

Mean Ratings of Intensity, Pleasantness, Familiarity and Arousal for Odorant Sets

Odorant Set Intensity Pleasantness Familiarity Arousal

A Mean 6.0 4.9 5.8 5.1 Range 1-9 1-9 1-9 1-9

B Mean 5.5 4.8 5.3 4.9

Range 1-9 1-9 1-9 1-9

Equivalence t(3S)=0.5, f(38)=0.006, f(38)=0.12, *(38)=0.7,

of Sets p=.62 p=.99 p=.91 p=A9

Note. Ratings are from a previous study; Pouliot, Hudry & Jones-Gotman (2003).

All odorants were chemical compounds or artificial aromas. With a few

exceptions, we diluted odorants to 10 % in 4.5 ml of mineral oil (Appendix F). They

were presented in 30 ml amber glass bottles in which a piece of polypropylene was

inserted to absorb the odorant, prevent spilling and ensure a better exchange with air.

Odorants were kept refrigerated when not in use.

Subjective ratings. A pen and paper rating scale was used to measure subjective

responses to perceptual and affective dimensions of the odorants (Figure 17). Inspired by

the Self-Assessment-Manikin (SAM), a well-known rating scale used in emotion

research (Hodes, Cook, & Lang, 1985; Lang, 1980), the SAM*SMELL scale keeps the

arousal and pleasantness dimensions of the original scale, but also includes intensity and 198 familiarity dimensions. We implemented an intensity scale because odor intensity is an important component of odor perception (Doty, 1975) and because intensity was found to be highly correlated with subjective and objective measures of arousal (Bensafi et al.,

2002a). We added a familiarity scale because familiar odors are often remembered better than unfamiliar ones (Larsson, Oberg, & Backman, 2006; Savic & Berglund, 2000;

Schab & Crowder, 1995c). For each dimension, ratings were made by checking on or between one of the five figures, producing a nine-point scale. Six SAM* SMELL scales, each comprised of the four dimensions, appeared on each page of a rating booklet. The ratings of familiarity and intensity are part of another study and will not be discussed further in the present paper.

J •\D\DvU^ Intensity

Pleasantness

? ? # $ 30t Familiarity

dWnWnW™' Arousal

Figure 17. The SAM*SMELL pen and paper rating scale used to give subjective responses to odors. The pleasantness and arousal dimensions of SAM*SMELL are from' Lang, P. J., 1980, Behavioral treatment and bio-behavioral assessment: Computer applications. In J. B. Sidowski, J. H. Johnson, & T A. Williams (Eds.), Technology in mental health care delivery systems (pp. 119-137). Norwood, NJ: Ablex Publishing. Copyright 1980 by Peter J. Lang. Adapted with permission.

Test for general anosmia. The olfactory screening test was a forced choice test with three alternatives and seven trials. It used three bottles, identical to those used 199 during the odor memory test. One of the three bottles contained an odorant, phenyl ethyl alcohol (a rose-like odor), diluted to 10% in 4.5 ml of mineral oil, and the other two contained only mineral oil. The three bottles were presented in a randomized order that was identical for all participants. On each trial, participants indicated which of the three bottles smelled strongest. No participant had fewer than 5 correct choices (out of 7) and none was excluded from the experiment (average=6.9/7, range 5-7).

Procedure

Participants were led to believe that the experiment was about their emotional reactions to different odors. Subsequent memory tests were never mentioned. The experiment comprised two sessions: one for incidental encoding and the immediate memory test and a later one for the delayed recognition test. The delayed recognition test was carried out one week after the first experimental session (average= 7.3 days later, range=7-14).

During the incidental encoding session, subjects smelled and rated 20 odorants using SAM*SMELL. Odorants were presented in bottles 1cm under the nostrils for approximately three seconds, with an interstimulus interval (ISI) of 45 seconds, in a randomized order. Half of the subjects received odorant Set A and the other half odorant

SetB.

After a 20-minute break, participants were surprised with the first recognition memory test. Twenty odorants (10 targets and 10 foils, or half of the odorants from Sets

A and B) were presented for approximately three seconds each, in a pseudorandom order

such that no more than three targets or three foils were presented consecutively; ISI was

again 45 seconds. For each odorant presented, subjects stated whether or not they remembered smelling that odorant during the encoding session. 200

A week later, participants came back to the laboratory expecting to smell and rate more odorants, but they were welcomed with the delayed recognition test. During that test they smelled 20 odorants (the remaining 10 targets and 10 new foils) and, for each, they had to indicate whether they remembered smelling them during the encoding session. The time of presentation (3s) and the ISI (45s) were the same as during the immediate recognition test and the order of presentation was similarly pseudorandom.

Following this test, we screened participants for general anosmia. We used this order to prevent interference or confusion from the odors used in the test for general anosmia with the memory test odors.

Design

A 2 (arousal: nonarousing and arousing) X 2 (pleasantness: unpleasant and pleasant) X 2 (retention interval: immediate and a week later) repeated measures analysis of variance (ANOVA) was used. The dependent variable was memory accuracy

(d') index (Snodgrass & Corwin, 1988). We included pleasantness in the ANOVA because unpleasant odors could be especially arousing and could have an influence on odor memory. For each subject, the levels of arousal and pleasantness were determined on the basis of their SAM*SMELL ratings for each odor. We calculated d' for odors partitioned into eight groups: unpleasant nonarousing immediate and a week later, unpleasant arousing immediate and a week later, pleasant nonarousing immediate and a week later and pleasant arousing immediate and a week later (see Appendix G and Table

Gl for a description of this partitioning).

Results

An alpha level of .05 was used for all statistical tests in this paper, and when we

report post hoc multiple comparisons, the ^-values are based on Bonferonni adjustments. 201

Participants remembered pleasant and unpleasant odors equally well,

F(1,39)=0A3, p=J2. Their memory was more accurate for arousing compared to nonarousing odors, F(l,39)=9.76, p=.003, and at the immediate compared to the week- long retention interval, F(l,39)=8.9, p=.005. There was no interaction between pleasantness and arousal, F(l,39)=0.003,/?=.95, between pleasantness and retention interval, F(\ ,39)=0.3, p=.5&, or between arousal and retention interval, F(\ ,39)=1.45, p=.24. There was a significant three-way interaction between pleasantness, arousal and retention interval, F(l,39)=5.21, p=.03. Post hoc comparisons revealed that pleasant arousing odors were remembered better immediately after encoding than after a week, p=.003. It was also uncovered that at the immediate test, memory for pleasant arousing odors was enhanced relative to memory for pleasant nonarousing odors, p=.001; this difference was no longer observable at the delayed test, p=.l. With unpleasant odors, an opposite pattern was observed: at the immediate memory test there was no difference between nonarousing and arousing odors, p=A. It was only at the long retention interval that memory for unpleasant arousing odors was enhanced compared to memory for unpleasant nonarousing odors, p=.05. No other comparisons were significant (Figure

18). 202

1,4 1,2 1 0,8 H d' 0,6 T 0,4 0,2 0 D) D) c C tc c U) (0 V) 3 3 3 o o1_ oi_ o TO (0 c 03 c

o on a c o c c o c unpleasant plea sant unpleasant pleasant

immediate test delayed test

Figure 18. Odor memory discrimination (d') as a function of pleasantness, arousal and retention interval. Error bars express standard error of the mean.

Experiment 2

Arousal and Learning intention: Incidental versus Intentional Learning

Method

Participants

Twenty-one undergraduate students participated in this experiment (12 women,

mean age=22, range=18-29, all participants except one were right-handed). Exclusion

criteria were the same as in Experiment 1. All participants obtained a perfect score on

the general anosmia test and all gave informed consent.

Material 203

Odorants, subjective ratings and test for general anosmia. We used the odorants

(see Appendix F), rating scale (Figure 17) and test for general anosmia described in

Experiment 1.

Psychophysiology. We amplified and recorded skin conductance and breathing with a Power Lab 4 SP system using Chart 5 for Windows software (AD Instruments).

Skin conductance in microsiemens (uS) was recorded with bipolar nondisposable electrodes attached with velcro™ straps to the palmar surface of the middle segment of the fore and middle fingers of the nondominant hand. The GSR amplifier was fully isolated and provided a low constant-voltage AC excitation (22 mV at 75Hz) on one of the two electrodes. Changes in breathing were monitored with a pressure transducer

(PTAFlite, Pro-Tech) fitted to a cannula (Pro-Flow, Pro-Tech) placed at the nostrils.

The first important increment in breathing that occurred after presentation of an odor determined when an experimental odor had been sniffed. This increment in sniffing volume corresponded to a positive deflection of the breathing waveform. We examined the different magnitude in phasic skin conductance responses (SCR) during the 10

seconds after which an odor was sniffed. We subtracted the mean skin conductance magnitude, for each odor, during the 3 seconds preceding sniff detection (baseline) from the mean skin conductance magnitude in the subsequent 10 seconds. In a way similar to

Bensafi and collaborators (2002a; 2002b) our prestimulus and poststimulus interval

differ. We chose a 10 second poststimulus window because SCR is relatively slow to rise and we wanted to be certain the maximal phasic value would be included. The

subtraction was done to minimize the influence of the general increase in tonic skin

conductance. We normalized these differences in mean phasic skin conductance 204 magnitude with log transformations [logio(SCR+l)] (Dawson, Schell, & Filion, 2000;

Venables & Christie, 1980).

Procedure

The experiment included three sessions held at a week's interval. The first session was for incidental odor encoding. The second session was for an unsuspected odor recognition test and intentional encoding of a new set of target odors. The third and final session was for the expected odor recognition test. SCR and breathing were recorded during the three experimental sessions.

During the first session participants were led to believe that the experiment was about their subjective and objective emotional reactions to different odors. They smelled

10 odorants twice, first while skin conductance and breathing were recorded and second while they rated the odors with SAM*SMELL. For the autonomic recordings, subjects were trained to breathe regularly, to sniff when a bottle was placed under their nose, and to remain silent and calm. They wore earplugs to reduce extraneous stimulation, and the experiment began with a three-minute relaxation period. Odorants were presented in bottles 1cm under the nostrils in a randomized order for approximately three seconds, with an ISI of 45 seconds. They were not told to remember the odors. Half of the participants smelled odorants from Set A and the other half, odorants from Set B.

During the second session a week later, participants were surprised with the unexpected recognition test. Twenty odorants (10 targets and 10 foils, or half of the

odorants from Sets A and B) were presented for approximately three seconds each, in a pseudorandom order such that no more than three targets or three foils were presented

consecutively; ISI was again 45 seconds. For each odorant presented, participants stated

whether or not they remembered smelling that odorant during the encoding session. 205

After a 15-minute break, we proceeded to the intentional encoding phase. Again, participants smelled 10 odors twice, first for autonomic recordings and second for

SAM* SMELL ratings, and this time they were aware that their memory for these odors would be tested later.

During the third and final session, a week after the second one, participants encountered the expected odor recognition test. Again, twenty odorants were presented

(the remaining 10 targets and 10 new foils) and for each, participants indicated whether they remembered smelling it before or not. The time of presentation and the ISI were the

same as during the unexpected recognition test and the order of presentation was again pseudorandom. As in Experiment 1, the general anosmia test was administered after this last odor recognition test.

Design

A 2 (arousal: nonarousing and arousing) X 2 (pleasantness: unpleasant and pleasant) X 2 (learning instructions: incidental and intentional learning) repeated measures ANOVA was used. The dependent variables were memory accuracy (d') index

(Snodgrass & Corwin, 1988) and SCR. As in Experiment 1, for each subject the levels

of arousal and pleasantness were determined on the basis of their SAM*SMELL ratings

to each odor. We calculated d' for odors partitioned into eight groups: unpleasant nonarousing incidental and intentional learning, unpleasant arousing incidental and

intentional learning, pleasant nonarousing incidental and intentional learning and

pleasant arousing incidental and intentional learning (see Appendix G and Table Gl for

details of this partitioning). 206

Results

Memory Discrimination (d')

Odor pleasantness did not influence memory scores, F(l,20)=0.49,/?=.49, nor did arousal, F{\ ,20)=2.78, p=. 11. Participants earned higher odor memory scores after incidental compared to intentional learning instructions, F(l,20)=4.22,/>=.05. There was no interaction between pleasantness and arousal, F(l,20)-l.77,p-.2, or between pleasantness and learning intention, F(l,20)=1.48,/?=.24. There was no interaction between arousal and learning intention either, F(l,20)=2.06,/>=.17, but because we had predicted enhanced memory for arousing odors after incidental learning instructions, we carried out planned comparisons. These revealed that memory was better for arousing compared to nonarousing odors after intentional encoding instructions, £(20)=2.16, j9=.04, but did not differ as a function of incidental encoding instructions, £(20)=0.04,

/?=.97. However, analyzing arousing odors alone, no influence of encoding instructions was found, £(20)=0.18,/?=.86 (Figure 19). There was no three-way interaction between pleasantness, arousal and learning intention, F(l,20)=0.06,/?=.81.

2,5 i * *

1,5 • nonarousing • arousing

0,5 j

o-i incidental intentional

Figure 19. Odor memory discrimination (d') as a function of arousal and learning instructions. Error bars express standard error of the mean. 207

Psychophysiology

Skin conductance response during encoding. There was no effect of pleasantness,

F(l,20)=0.7,p=.41, or of arousal, F(l,20)=2, p=.\l, on magnitude of phasic SCR at

encoding. However, encoding instructions had a significant influence, F(l,20)=27.21,/?=.001.

SCR at encoding was larger after incidental than intentional instructions. Pleasantness and

arousal interacted, F(l,20)=6.21,/?=.02. The post hoc comparisons revealed that during

encoding the magnitude of phasic SCR was larger to unpleasant arousing than unpleasant

nonarousing odors, p=.04 and larger to unpleasant arousing than pleasant arousing odors, p=.04 (Figure 20). No other interaction was significant: pleasantness and learning intention,

F( 1,20)= 1.21,p=.28, arousal and learning intention, F(l,20)=1.78,p=.2, pleasantness, arousal

and learning intention, F(l,20)=0.01,/?=.91.

arousing nonarousing arousing unpleasant pleasant

Figure 20. Phasic SCR during encoding as a function of arousal and pleasantness. Error bars express standard error of the mean.

Skin conductance response during recognition. To analyze autonomic arousal

during odor recognition we carried out a 2 (arousal: nonarousing and arousing) X 2

(pleasantness: unpleasant and pleasant) X 2 (learning instructions: incidental and 208 intentional learning) X 2 (odor type: target or foil) repeated measures ANOVA. The only significant effect during recognition was an interaction between odor type and learning instructions, F(l,20)=10.39,/?=.004. The post hoc comparisons revealed that the magnitude of phasic SCR was higher to foils presented at the unexpected recognition test (incidental condition) than to foils in the expected test (intentional condition), p=.05; during the unexpected test foils were also accompanied by a larger phasic SCR than were targets, p=.007 (Table 9 for complete statistics). 209

Table 9 Magnitude of Phasic Skin Conductance during Recognition

Pleasantness Arousal Learning Odor Type F(l,20)= P= Instructions (Targets or Foils)

X 1.03 .32

X 0.22 .64

X 1.89 .18

X 1.77 .2

X X 2.72 .11

X X 0.45 .51

X X 1.91 .18

X X X 1.31 .27

X X X 0.17 .68

X X X 2.68 .12

X X X X 0.1 .75

X X 1.6 .22

X X 0.01 .92

X X X 2.96 .1

X X 10.39 .004* 210

General Discussion

Whether a longer retention interval was necessary to obtain the enhancement of memory for emotionally arousing odors was tested in Experiment 1. Because in the nonolfactory literature an interaction between emotional arousal and retention interval is reported (Kaplan & Kaplan, 1969; Kleinsmith & Kaplan, 1963, 1964; Sharot & Phelps,

2004), we predicted better memory for arousing compared to nonarousing odors at the week-long retention interval, and the inverse-better memory for nonarousing compared to arousing odors-at the immediate memory test. We found a main effect of arousal- arousing odors were remembered better-and a main effect of retention interval-odor memory was better at the immediate test-but there was no interaction between arousal and retention interval. However, the inclusion of pleasantness in the analysis was revealing. There was a significant interaction between arousal, retention interval and pleasantness. At the immediate test, arousing pleasant compared to nonarousing pleasant odors were remembered better and at the delayed test it was the arousing unpleasant

compared to the nonarousing unpleasant odors that were remembered better.

In Experiment 2, we tested whether manipulating encoding instructions would influence the effect of emotional arousal on odor memory. Incidental encoding is routinely used in investigations of arousal and memory. We are aware of only three

studies investigating emotional arousal and memory that compared intentional and

incidental encoding (Heuer & Reisberg, 1990; Kensinger, Piguet, Krendl, & Corkin,

2005; McLean? 1969). None of these studies used odors as memory targets, but all of

them implied that incidental encoding led to better memory for emotionally arousing

stimuli. Here we obtained a main effect of encoding instructions: participants had

superior memory after incidental encoding. There was no main effect of arousal and no 211 significant interaction between arousal and encoding instructions. These null findings are possibly related to a power issue due to the small number of participants. However, we carried out planned comparisons that revealed unanticipated results. Memory for arousing odors was better than for nonarousing odors after intentional encoding instructions but not after incidental encoding; memory for arousing odors was the same in both encoding conditions. This result seems consistent with the finding of better memory for unfamiliar odors after intentional compared to incidental encoding described by Larsson, Oberg, and Backman (2006). However, it is surprising given previous reports of better memory for emotionally arousing stimuli after incidental encoding (Cahill et al., 1996; Canli, Zhao, Brewer, Gabrieli, & Cahill, 2000; Hamann,

Ely, Grafton, & Kilts, 1999; Heuer & Reisberg, 1990; McLean, 1969), and our own finding of enhanced memory for arousing odors in incidental conditions (Pouliot, Hudry,

& Jones-Gotman, 2004).

Retention Interval

Whether emotional arousal influences memory through modulation of attentional or consolidation processes is currently debated (Hamann, 2001; Sharot & Phelps, 2004).

We found evidence for both processes. At the immediate test and not at delay, pleasant arousing odors were remembered better than pleasant nonarousing odors. This early effect of arousal must be attributed to differential attention during encoding and not to differential consolidation. Indeed, consolidation requires time to occur, and at the immediate test it was too early to have taken place. However, we also found evidence of

consolidation modulation by arousal. After a week, and not at the immediate test, unpleasant arousing odors were recognized better than unpleasant nonarousing odors.

Our findings suggest that depending on how pleasant an odor is judged to be, its arousal 212 will enhance memory through different processes. If the odor is pleasant, arousal may influence memory by modulating attention at encoding. If the odor is unpleasant, arousal may influence memory by modulating consolidation processes. This interaction suggests that with odors, the enhancement of memory by emotional arousal is related not only to time for consolidation, but that emotionally arousing odors can also modulate attention.

Given the advantage of pleasant arousing odors in the immediate recognition test, they must have a specific attention-grabbing capacity that they do not share with unpleasant arousing odors. Recent evidence does suggest a special ability of pleasant odors to modulate attention. Bensafi et al. (2003) demonstrated that when smelling pleasant compared to unpleasant odors, the sniff volume was greater. If the sniff is an indication of olfactory attention, this suggests that pleasant stimuli must facilitate olfactory attention and encoding. If the sniff volume (and olfactory attention) increases with odor pleasantness, it could help explain the difference in memorability of arousing pleasant versus nonarousing pleasant odors at the immediate test. Arousal more or less

corresponds to emotional intensity (Anderson et al., 2003), and consequently arousing pleasant odors were likely "more pleasant" than nonarousing pleasant odors. We

analyzed pleasantness ratings as a function of the odor groups and found an interaction between pleasantness and arousal, F(l,39)=49.3,p=.00001. Posthoc comparisons revealed that arousing pleasant odors (m=5.91) did receive higher pleasantness ratings

than did the nonarousing pleasant odors (m=5.52) (p=.0001), and that arousing

unpleasant odors (m=4.13) received inferior pleasantness ratings compared to

nonarousing unpleasant odors (m=4.32) (p=.002). Thus, being "more pleasant", the

arousing pleasant odors could have led to larger sniff volume, allowing them to be better 213 attended to and better encoded. Unfortunately, because we did not measure sniff volume this interpretation awaits confirmation.

For arousing unpleasant compared to nonarousing unpleasant odors, memory was enhanced, or the forgetting was reduced, only during delayed recognition. This finding fits more easily in the model in which emotional arousal modulates memory

consolidation (McGaugh, 2004a). We did not monitor autonomic arousal in Experiment

1, but we did in Experiment 2. Given the resemblance between the participants and designs of the two experiments, we think the following interpretation is founded. Only

arousing unpleasant odors (and not arousing pleasant odors) were accompanied by a larger phasic SCR at encoding. Larger SCR at encoding also means more autonomic

arousal when smelling these specific odors. It has been suggested that autonomic arousal

activates the release of stress hormones that will interact with the amygdala to modulate memory consolidation in other brain regions (Cahill & McGaugh, 1998; McGaugh,

2004). Consequently, the increased autonomic arousal we measured during encoding of

arousing unpleasant odors might very well have modulated their consolidation in

memory, explaining why they were remember better after the longer retention interval.

Encoding Instructions

The only study of odor memory that manipulated encoding instructions did not

control for emotional arousal (Larsson, Oberg, & Backman, 2006). At first glance, our

finding of enhanced memory for arousing compared to nonarousing odors after

intentional and not after incidental encoding seems consistent with the results of

Larsson, Oberg and Backman (2006), who reported that recognition of unfamiliar odors

was better after intentional than after incidental encoding and that memory for familiar

odors did not vary as a function of encoding instructions. Because Larsson, Oberg and 214

Backman (2006) found that odor familiarity interacted with encoding instructions, we analyzed the association of odor familiarity and arousal. We found a positive correlation between ratings of arousal and ratings of familiarity (mean r =.29, range=-.04 to .67,

r

significant in 6 out of 21 subjects; a binomial test indicates that this proportion of

significant correlations could not be due to chance). Therefore, we could have expected that the less arousing odors would also be the less familiar ones. Like Larsson, Oberg

and Backman (2006), our more familiar odors (arousing ones) were remembered equally

well across encoding conditions. However their unfamiliar odors were remembered

better after intentional encoding, whereas our "less familiar" odors, the nonarousing

ones, were remembered better after incidental encoding. An important difference

between their study and ours is that their familiar odors were the same for all subjects

whereas in our study, the familiar odors were determined individually for each subject

and consisted of the ones rated as the most familiar. Another point that may explain the

divergence was that the familiar odors in the Larsson et al. study were real-world

substances (e.g., lemon, cinnamon, coffee...) as opposed to chemicals (e.g., thymol,

eugenol, rose oil...), whereas our familiar odors were the ones our subjects rated as

having the impression of knowing the best. Given that odor perception is a highly

subjective process (Hudson & Distel, 2002), it might be more accurate to use

individual's indication to decide whether an odor belongs to one group or another (e.g.,

familiar vs unfamiliar).

Autonomic Arousal

In Experiment 2 we measured phasic SCR during encoding. We found that

incidental encoding led to a larger phasic SCR than did intentional encoding. It also led

to better odor memory a week later. This association of higher phasic SCR during 215 stimulus presentation and superior delayed memory has been reported many times

(Corteen, 1969; Kleinsmith & Kaplan, 1963; Maltzman, Kantor, & Langdon, 1966).

Autonomic arousal may have modulated memory consolidation and might explain why odors learned incidentally were remembered better. However, we also expected to find larger phasic SCR to odors rated as more arousing, but this was not the case. We had

found this association in a previous experiment (Pouliot, Hudry, & Jones-Gotman,

2004), and other researchers have reported a strong correlation between SCR and

subjective ratings of arousal (Bensafi et al., 2002a, 2002b). The absence of higher SCR to odors judged as being more arousing may be an artifact of the experimental paradigm.

Anxiety has been associated with a reduction of SCR (Naveteur, Buisine, & Gruzelier,

2005; Wilken, Smith, Tola, & Mann, 2000), and because asking subjects to memorize

the presented odors may make them more anxious, a diminished SCR should not be

surprising. Thus the higher task demands of having to remember the odors may have

overridden the more subtle effect of arousal on SCR.

Autonomic arousal was measured also during recognition. Not much is known

about the meaning of SCR during recognition. Some report higher SCR to targets than to

foils, irrespective of their explicit recognition (Tranel & Damasio, 1985; Tranel,

Damasio, & Damasio, 1995; Verfaellie, Bauer, & Bowers, 1991), and others that SCR is

higher to stimuli that are not recognized (Stelmack, Plouffe, & Winogron, 1983). Here,

the only significant finding was an interaction between learning instructions and odor

type (target or foil). SCR was larger to foils that were presented during the unexpected

test (incidental learning) than during the expected test (intentional learning) and also

larger to foils presented during the unexpected test than to targets presented during the

unexpected test. According to Sokolov (1975) and also to Stelmack, Plouffe & 216

Winogron (1983), the orienting response magnitude (or SCR when perceiving a stimulus) is determined by stimulus novelty or by the availability of its memory trace, where a less accessible trace would lead to a larger response. We think higher SCR during the presentation of new odors (foils) compared to old odors (targets) in the unexpected test (incidental learning) shows evidence of learning, even if the explicit performance was relatively low.

Interference

Could an order or interfering effect explain the results of Experiments 1 and 2 parsimoniously? In Experiment 1, odor memory was more accurate at the immediate compared to the delayed retention interval. In Experiment 2, odor memory was more accurate after incidental than after intentional encoding. These two superior conditions were also the first tested. This order was inevitable. Because we wanted to avoid differences related to subject groups, we carried out within-subject design experiments.

In both experiments, every subject was tested in both conditions-immediate versus delayed and incidental versus intentional. Because there was only one encoding session in Experiment 1, it was not possible to assess immediate memory after having assessed delayed memory. Moreover, in Experiment 2 it would have been impossible to assess incidental memory after having tested it with intentional instructions and to keep the experimental situations as similar as possible without subjects guessing the upcoming memory test. Thus, proactive interference of the first odor memory tests (immediate or incidental) on the second ones (delayed or intentional) could have resulted from the within-subject design used here. However, even if some authors report that odors are not

subject to important forgetting over time (Engen & Ross, 1973; Lawless, 1978; Lawless

& Cain, 1975), odor memory is not immune to the effect of time, and some forgetting is 217

expected. Proactive interference or not, it should not be a surprise that odor memory is weaker a week after encoding than 15 minutes after. We have no reason to believe that

interference would lead to differential forgetting for odors varying in levels of arousal

and pleasantness. Nevertheless, in the delayed test of Experiment 1 only unpleasant

nonarousing odors were forgotten more than unpleasant arousing ones. In the intentional

test of Experiment, 2 only nonarousing odors were remembered less well. To eradicate

the influence of proactive interference, one would need to carry out a between subject

experiment; however problems such as diminished power and group differences would

emerge.

Conclusion

The question guiding the present investigation was whether incidental learning

and a relatively long retention interval were necessary conditions for emotional arousal

to enhance odor memory. Our findings indicate that they may not be necessary, and that

in olfaction the influence of pleasantness is important. Lately researchers have favored

the role of memory consolidation over attention to explain how emotional arousal

enhances memory. With odors, our findings suggest that they both play a role. In

olfaction, modulations of attentional and of consolidation processes by emotional

arousal to influence memory are not alternative hypotheses. They are complementary.

The investigation of odor memory and emotional arousal is still in its infancy and many

questions remain regarding the cognitive, neuropsychological and even olfactomotor

mechanisms involved. 218

CHAPTER 7. CONCLUSION 219

Conclusion

On the one hand, the influence of emotional arousal on memory has been, and still is, giving rise to a large number of cognitive and neuroscientific investigations (e.g.,

Christianson, 1992; LaBar & Cabeza, 2006; McGaugh, 2004a). On the other, the special ability of odors to cue older and more emotionally laden memories has motivated writers and chemosensory scientists to search for the roots of this phenomenon (e.g., Chu &

Downes, 2000b; Herz & Cupchik, 1995; Rubin, Groth, & Goldsmith, 1984). It may be because the most salient or noticeable affective reaction one has when smelling an odor is of liking or disliking it, that the other defining characteristic of emotional reactions, arousal, has been relatively neglected in olfaction.

This relative neglect of emotional arousal may also explain why the path of emotional arousal and memory has never crossed the path of the emotional specificity of odor memory. Indeed, the closest these two questions have been to each other was in a suggestion that odors were especially good at cueing emotional memories because they were particularly arousing (Aggleton & Waskett, 1999; Herz, 1997). However, this suggestion has never been investigated. Moreover, as reviewed in Chapter 2, no study had been conducted to determine if emotional arousal had some influence on odor memory. Therefore, the goal I pursued in this dissertation was to investigate if and how emotional arousal influences odor episodic memory.

I conducted three studies in which participants had to rate a set of odors with a smell-adapted version of SAM (Lang, 1980), the SAM*SMELL scale, and in which their memory was tested later in an odor recognition test. Whether an odor was arousing or not was determined separately for each subject on the basis of his own SAM*SMELL ratings. Because odor perception is highly idiosyncratic (Hudson & Distel, 2002) and to 220 have odor groups that accurately represented the dimension they were supposed to, I chose to use the ratings of each individual subject to assign odors to one group dimension or another.

In the first study (Chapter 4), I ran two experiments in which healthy participants were submitted to an unexpected odor recognition test one week after an encoding session. In one experiment, memory was more accurate for odors rated as more arousing, but in the other, the effect of arousal failed to reach significance.

In the second study (Chapter 5), I tested patients who had undergone a unilateral resection from the temporal lobe including the amygdala (MTLR). I thought this experiment was of high interest because the amygdala is believed to be critically implicated in memory for emotionally arousing nonolfactory information (e.g., LaBar &

Phelps, 1998; Markowitsch et al., 1994) and because the amygdala is part of the primary

olfactory area (e.g., Carmichael, Clugnet, & Price, 1994). I found that, unlike healthy

individuals, patients with MTLR did not show better memory for emotionally arousing

odors compared to nonarousing ones.

In the third study (Chapter 6), I carried out two separate experiments in which I

tested whether incidental encoding and testing odor recognition after a long delay were

essential conditions for emotional arousal to enhance odor memory. My findings suggest

they are not. But, interestingly they also imply that depending on the pleasantness of the

odor, emotional arousal would enhance memory through different processes.

Alternative Explanations: General

As discussed in the literature review, numerous explanations for the effect of

arousal on episodic memory for nonolfactory stimuli have been proposed. I will now

evaluate whether the propositions of event distinctiveness, of differential distribution of 221 attention, of semantic relatedness and of greater rehearsal and elaboration could explain the finding of enhanced memory for emotionally arousing odors.

Event Distinctiveness

For the reason that emotional events can be considered more distinctive than neutral events and that distinctiveness has been shown to enhance memory (Hunt &

Elliott, 1980; McDaniel & Einstein, 1986), the distinctiveness of emotional events was suggested to be the underlying factor of the enhancing effect of emotional arousal on memory. With visual information, Christianson and Loftus (1991) showed that distinctiveness of information was not sufficient to explain the effect of emotional arousal on memory. For distinctive and emotional pictures (e.g., distinctive: a woman carrying a bicycle on her shoulders; emotional: a woman lying wounded beside her bicycle), peripheral details were well recalled; but it was only with emotional pictures that memory for central details were improved.

Although I did not test specifically the hypothesis of arousing odors being more distinctive, and thus remembered better, I think this explanation is particularly inappropriate in the case of olfaction. First, humans have evolved without emphasizing the cognitive information found with odorants, in such a way that they rely mostly on their other senses to gather accurate facts about their environment (Holley, 2002).

Second, humans are notably poor at distinguishing between more and less complex

(distinctive?) olfactory information. For example, it was shown that humans have a limited capacity to perceive the odors contained in a mixture, that odors in mixtures tend to blend to form a single new odor (Laing & Francis, 1989), and that even with training, discrimination of the different odor components in a mixture remains very difficult

(Livermore & Laing, 1996). Finally, an additional point that makes me doubt that odor 222 distinctiveness could underlie the effect of arousal on odor memory in my experiments is that I kept constant one of the most important features of odorants that could have provided a distinctive cue—intensity. Indeed, odorants in the two sets of my experiments were chosen to have an approximately equal perceptual intensity.

Differential Distribution of Attention

Another alternative explanation for the effect of arousal on memory for nonolfactory information is the proposition of a "differential distribution of attention".

Emotionally arousing events could be remembered better because subjects pay more attention to them. Christianson, Loftus, Hoffman and Loftus (1991) found that even when the amount of attention subjects were devoting to neutral and emotional pictures was controlled—(tachistoscopic presentation), memory for the central details of emotional pictures was still superior to that of neutral ones. These results indicate that attentional focus cannot explain all effects of emotion on memory.

I found evidence that a differential distribution of attention may account for some effects of emotional arousal on odor memory. In Study 3, pleasant arousing odors were remembered better than pleasant nonarousing odors only at the immediate and not at the delayed test. This early effect of arousal must be attributed to differential attention during encoding and not to differential memory consolidation. Indeed, consolidation requires time to occur (McGaugh, 2004b), and at the immediate test it was too early to have taken place. Given the advantage of pleasant arousing odors in the immediate recognition test, they must have a specific attention-grabbing capacity that they do not

share with unpleasant arousing odors. In fact, recent evidence does suggest a special

ability of pleasant odors to modulate attention. Bensafi et al. (2003) demonstrated that

when smelling pleasant compared to unpleasant odors, the sniff volume was greater. If 223 the sniff is an indication of olfactory attention, this suggests that pleasant stimuli must facilitate olfactory attention and encoding.

However, all effects of arousal on odor memory cannot be reduced to attentional

factors. In Study 3,1 also found that after a week, and not at the immediate test, unpleasant arousing odors, which presumably lead to smaller sniff volume and less

olfactory attention, were recognized better than unpleasant nonarousing odors. These

findings suggest that, depending on how pleasant an odor is judged to be, its arousal will

enhance memory through different processes. If the odor is pleasant, arousal may

influence memory by modulating attention at encoding. If the odor is unpleasant, arousal may influence memory by modulating consolidation processes.

Semantic Relatedness

The effect of semantic relatedness has been proposed to explain the memory

enhancement observed for emotional stimuli. Talmi and Moscovitch (2004) postulated

that emotional stimuli are naturally more interrelated than neutral information. Because

interrelated information is remembered better than nonrelated information (Puff, 1970;

Tulving & Pearlstone, 1966), it could be that emotionally arousing information is

remembered better mostly because it is more interrelated.

Language is an important, if not the preferred, tool to establish or identify

relationships between items. As opposed to verbal or visual stimuli, odors are notably

difficult to name; accuracy in naming odors rarely exceeds 50% (Cain, 1979; Engen,

1987). Arousing odors might be easier to name than nonarousing odors. However in all

my experiments, subjects rarely reported naming or trying to name the odors at

encoding. Interestingly, Jonsson, Olsson & Olsson (2005) showed that people are not

more accurate in naming arousing compared to nonarousing odors, but that they are 224 more confident that they are accurately naming arousing odors. Given the important difficulty associated with odor identification, I think semantic relatedness is an

especially inadequate alternative explanation to the observed better memory for arousing

odors.

Greater Rehearsal and Elaboration

It was also suggested that arousal influenced memory because emotional stimuli

receive greater rehearsal and elaboration than neutral stimuli (Schacter, 1996). For

example, some studies report a positive correlation among emotion, rehearsal and

memory (Cohen, Conway, & Maylor, 1994; Conway & Bekerian, 1988; Rubin & Kozin,

1984). But Heuer and Reisberg (1990) and Guy and Cahill (1999) showed that

manipulating rehearsal when memorizing a film or story did not reproduce the effects of

emotion on memory.

In my odor memory experiments, had greater rehearsal and elaboration underlay

the effect of emotional arousal on odor memory, its effect would have been minimal. In

fact, in studies in which the encoding was incidental, no subject guessed that their

memory would be tested, and much less tried to remember and rehearse the odors

smelled in the first experimental session. In the condition in which subjects had to

intentionally encode the odors, no subjects reported a specific memorization strategy

apart from trying to think about the odors. This may not be a big surprise when

considering that odors are difficult to identify when they are presented out of context—

such as in the brown glass bottles that I used—(Cain, 1979; Chobor, 1992), and

considering that rehearsal may be less efficient with odors (White, 1998). 225

Alternative Explanations: Specific to Olfaction

In nonolfactory sensory modalities, the enhancing effect of emotional arousal on memory can be difficult to demonstrate but is, nonetheless, acknowledged as a real phenomenon (Christianson, 1984; Christianson & Loftus, 1987). Because in my

experiments also, the effect of arousal on memory did not always reach significance, it is

necessary to consider other alternative explanations, specific to olfaction, for when it

did. I will now discuss the potential of perceptual intensity, of pleasantness and of

familiarity to account for the effect of emotional arousal on odor memory.

Intensity vs Arousal

Because ratings of intensity and arousal were highly correlated in most

participants, one may suggest that the effect arousal has on odor memory discrimination

may simply be an effect of intensity or vice versa; basically, that intensity and arousal

are the same thing. Bensafi et al. (2002a) have also found a strong positive correlation

between ratings of arousal and ratings of intensity. Like them, I am tempted to suggest

that in olfaction, intensity and arousal are connected to a similar phenomenon. Judgment

of intensity may refer to the intrinsic property of the odorant while judgment of arousal

could refer to the effect the odor has on the subjective and autonomic state.

The results of Study 1 support the notion of a functional dissociation between

intensity and arousal because my objective measure of autonomic arousal (phasic SCR

magnitude) differed significantly only between smelling arousing versus nonarousing

odors. There was no difference in phasic SCR when smelling odors rated as intense

versus weak. This also suggests that the memory superiority that odors rated as arousing

had over less arousing ones was driven by an autonomic arousal difference, whereas the

memory superiority for odors rated as more intense was most likely driven by a 226 perceptual one. Thus emotional arousal and intensity may enhance odor memory to a similar degree, but not through the same processes. On one hand, intense odorants could be remembered better because they are easier to attend to and to be encoded. On the other hand, emotionally arousing odorants may be remembered better because consolidation is enhanced for arousing stimuli (Cahill & McGaugh, 1998).

The results of Study 2 are also interesting in that they suggest that the effect intensity sometimes has on memory is because participants tend to be more liberal in their response (old vs new) to intense than to weak odors (C). I never found a response bias difference as a function of arousal in any of my studies. Odor intensity seems to enhance the tendency to decide an odor had been smelled before rather than enhancing memory recognition per se. The intensity explanation for memory enhancement is even less likely given the extensive evidence indicating an effect of emotional arousal on memory for other types of stimuli (e.g., Cahill & McGaugh, 1998; LaBar & Cabeza,

2006). Although correlated, intensity and arousal may represent a distinct, perceptual or affective, dimension in human olfaction

Pleasantness vs Arousal

I had not predicted an effect of pleasantness on odor memory, because usually pleasantness is not found to influence odor recognition memory (Lawless & Cain, 1975;

Sulmont, Issanchou, & Koster, 2002). Yet, I found one in Experiment 2 of Study 1 and in Study 2. In both cases, unpleasant odors were remembered better than pleasant odors.

In Study 1, in which healthy participants were tested, the effect of pleasantness may be attributed partially to arousal because of the quadratic relationship observed between ratings of arousal and pleasantness; odors rated as more pleasant or more unpleasant were also rated as more arousing. 227

However, in Study 2 MTLR patients also remembered unpleasant odors better, and the argument of an effect of emotional arousal accounting for the effect of pleasantness cannot be used convincingly any more. In fact, I found a specific impairment of emotional arousal to enhance odor memory in MTLR patients. Moreover, the nonolfactory literature contains many reports of an abolished effect of emotional arousal on memory in people who underwent amygdalar resection (Adolphs, Tranel, &

Denburg, 2000; Brierley, Medford, Shaw, & David, 2004; Buchanan, Denburg, Tranel,

& Adolphs, 2001; Frank & Tomaz, 2003).

Because a strong positive association between familiarity and pleasantness has been reported (Ayabe-Kanamura et al., 1998; Jellinek & Koster, 1979, 1983; Royet et al., 1999), and familiar odors tend to be remembered better than unfamiliar odors (Rabin

& Cain, 1984; but see Engen & Ross, 1973; Lawless & Cain, 1975), it may be that the effect of pleasantness on memory was caused by familiarity. Still, subjects found familiar odors more pleasant because the correlation between ratings of familiarity and pleasantness was positive in all subjects. It was unpleasant odors (the less familiar ones) that had the memory advantage, a finding inconsistent with the favorable role familiarity is reported to play on odor memory.

Familiarity vs Arousal

The effect of odor familiarity could also provide an alternative explanation to the enhancing effect of arousal on odor memory. For example, arousing odors could have been remembered better because they were more familiar, and vice versa. This interpretation may seem plausible, but it is not satisfactory. Indeed, the correlations between ratings of familiarity and of arousal were relatively low, not in the same direction for all participants and significant in only approximately half of the 228 participants. This means that for some participants, the more familiar an odor was the more arousing it was; for others, the opposite was true. Thus, the effect of arousal on odor memory cannot easily be reduced to a familiarity effect.

Odor Memory and MTLR Patients

In Study 2,1 tested odor memory in MTLR patients. There are some marked advantages and disadvantages in testing patients with surgical resection from a brain area. On the positive side, MTLR patients are a unique and exceptional group who can teach us which brain areas are critically involved in different cognitive processes, such as learning and memory. Brenda Milner was the pioneer in this domain, and her findings

(e.g., with HM) shaped today's cognitive neuroscience. On the negative side, these patients are relatively rare, and with the many exclusion criteria of controlled experimental studies, it can take many years before enough subjects in one experiment can be grouped to yield meaningful results.

I did not find the odor memory deficit that patients with temporal-lobe resection,

especially on the right side, usually show (Eskenazi, Cain, Novelly, & Friend, 1983;

Jones-Gorman & Zatorre, 1988, 1993; Jones-Gorman et al., 1997; Martinez et al., 1993;

Zatorre & Jones-Gotman, 1991). One reason for this may be that I did not have enough patients (19) in my experiment, thus a statistical power issue. Another reason may be

that our subjects sniffed odors with both nostrils (thus allowing both hemispheres to

process the olfactory information), because in many studies in which a deficit was

found, odors were sniffed monorhinally (and deficits were generally found ipsilateral to

resection). A final possibility would be that in studies where a global odor memory

deficit was found, what was really observed was a memory deficit for odors that led to a

greater emotional arousal. However, because this variable was not controlled for, it 229 could not be used as an argument for or against any effect of emotional arousal or pleasantness on odor memory.

My findings cannot unambiguously implicate the amygdala as the unique structure responsible for the enhancement of memory for emotionally arousing odors. In no patient was the surgery limited to a unilateral removal of the amygdala. In all cases there was additional surgical removal of the surrounding medial temporal lobe. The observation of impaired enhancement of memory for emotionally arousing odors may reflect the effects of an underlying pathology in temporal lobe epilepsy, cerebral reorganization after life long epilepsy or a disconnection, consecutive to resective surgery, in some odor/hedonic circuit. Nevertheless, because MTLR patients did not show a general odor memory deficit, because their impairment was restricted to the enhancement in memory for arousing and not for unpleasant odors and because of converging evidence from neuroimaging and brain lesion studies, my findings suggest that the amygdala might play a pivotal role in the enhancement of memory for emotionally arousing odors, like it does for other types of sensory information. 230

Future Directions

In this dissertation I investigated whether emotional arousal enhanced odor memory. Because in many cases I found an effect of arousal on odor memory, and because none of many alternative explanations can account satisfactorily for it, I think that emotional arousal can enhance odor memory.

The relationship of emotional arousal and odor memory is a promising and fascinating research topic. The findings in healthy participants need to be reproduced

and the use of objective measures of arousal, such as SCR and EEG, instead of rating

scales, may give more consistent results. Because a different role for the left and right

amygdala in men and women in the enhancement of memory for arousing information has been reported (Cahill et al., 2001; Canli, Desmond, Zhao, & Gabrieli, 2002), it would be instructive to analyse olfactory data separately for each gender (however, I was not able to find any gender differences in any of my experiments). This is especially

true for MTLR patients, if one can test a sufficient number of men and women to make meaningful comparisons.

Coming back to the « Proust effect », as discussed in the Introduction of this

thesis, could the arousal characteristic of odorants be one of its fundamental dimensions?

My results from experimental manipulations suggest it could very well be, and that

explicitly testing the hypothesis that arousing odors are the best to cue autobiographical

memories may be revealing.

A conclusion has never smelled so good. Chances are I will remember it well! 231

REFERENCES 232

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APPENDICES 282 )

Appendix A

List of Odorant Names (and distributing society) and Concentration at which they Were Tested in the Preliminary Study

Providers Odorant Name Concentration Providers Odorant Name Concentration

Adrich Bell 1. Acetic acid l%v\v 1. Angelica root oil 10%v\v 2. Acetone 1% v\v 2. Banana 10%v\v 3. Allyl sulphide l%v\v 3. Caramel 10%v\v 4. Basil oil 10%v\v 4. Coffee natural 10%v\v 5. Benzyl butyrate 10%v\v 5. Damascenone 10%v\v 6. Benzyl butyrate 10%v\v 6. Field strawberry 10%v\v 7. Bois de rose 10%v\v 7. Green grass fragrance 10%v\v 8. Butyric acid l%v\v 8. Ham type 10%v\v 9. Cardamom 10%v\v 9. Lemon 10%v\v 10. Carrot seed oil 10%v\v 10. Orange 10%v\v 11. Celery seed oil 10%v\v 11. Peanut butter 10%v\v 12. Citronellyl acetate 10%v\v 12. Pine fragrance 10%v\v 13. Citronellyl butyrate 10%v\v 13. Strawberry 10%v\v 14. Coriander 10%v\v 15. Fennel oil, sweet 10%v\v 16. Fir needle oil 10%v\v 17. Gamma-dodecalactone 10%v\v ) 283

Providers Odorant Name Concentration Providers , Odorant Name Concentration

Aldrich (cont.) International Flavors and Fragrances 18. Gamma-undecalactone 10%v\v 1. Apo patchone 10%v\v 19. Garlic oil, Chinese l%v\v 2. Bergamot super oilffac •10%v\v 20. Grapefruit, Florida 10% v\v 3. Bourgeon d'Avana 10%v\v 21. Isobutyric acid 1% v\v 4. Carento 10%v\v 22. Juniper berry 10% v\v 5. Cedraclaire 10%v\v 23. Lactic acid l%v\v 6. Coniferan 10%v\v 24. Laurie acid 10%w\v 7. Dihydro-cyclacet 10%v\v 25. L-linaloo 10%v\v 8. Dimethyl benzyl carbinyl butyrate 10%v\v 26. L-menthyl acetate 10%v\v 9. Ethoxiff 10%v\v 27. Methyl 2-methylbutyrate 1% v\v 10. Fraistone 10%v\v 28. Methyl benzoate l%v\v 11. Hyacinth body #3 10%v\v 29. Musk ambrette 14.44o/0 w\v 12. Mimosa 10%v\v 30. N-butyl acetate 10%v\v 13. Nepalva 10%v\v 31. Octyl acetate 10%v\v 14. Oreganiff 10%v\v 32. Trans-annamyl propionate 10%v\v 15. Rosamariff 10%v\v 33. Trans-cinamyl-propionate 10%v\v 16. Styrax essence oliffac 10%v\v 34. Trans-cinnamyl butyrate 10%v\v 17. Verdone 10%v\v 35. Vanillin 10% w\v 18. Vertenex 10%v\v 36. Ylang ylang oil extra 10% v\v 284 •'

Providers Odorant Name Concentration Providers Odorant Name Concentration

Fluka Sigma 1. Citral 10%v\v 1. 1-heptanol 10%v\v 2. Oil of cloves l%v\v 2. P-anisaldehyde 10%v\v 3. Phenyl ethyl alcohol 10%v\v 3. Pyridine l%v\v 4. Thymol 7.6% w\v 5. Z-heptanone l%v\v

Unknown company 1. Methyl ionone gamma 10%v\v 2. Mousse de chene 10%v\v Sigma-Aldrich 3. Pine needle oil, Siberian 10%v\v 1. Cineole 10%v\v 2. Eugenol 10%v\v 285

Providers Odorant Name Concentration Providers Odorant Name Concentration

Givaudan-Roure Givaudan-Roure (cont.) 1. 2-methyl butyrc acid l%v\v 16. Eucalyptus oil 10%v\v 2. Allyl caproate 10%v\v 17. Fennel oil 10%v\v 3. Ambrarome ABS cone 10% v\v 18. Fir balsam (oliffac) 10%v\v 4. Amyl acetate 10%v\v 19. Freesia 10%v\v 5. Anisic aldehyde aubepine 10%v\v 20. Galbanum oil 10%v\v 6. Bergamot oil 10%v\v 21. Geraniol 10%v\v 7. Butyric acid 10%v\v 22. Ginger oil 10%v\v 8. Butyric acid l%v\v 23. Guave 10%v\v 9. Castoreum res artessence l%v\v 24. Hydrocardoresin 10%v\v 10. Cedarwood 10%v\v 25. Indole l%v\v 11. Cinnamon bark oil 10%v\v 26. Isovaleric acid l%v\v 12. Cis-3-hexenol 10%v\v 27. Jasmin 10%v\v 13. Civet artificial l%v\v 28. JonquilleRVG 10%v\v 14. Cumin oil 10%v\v 29. Labdanum oil Spanish 10%v\v 15. Ethy-3-methy-3-phenyglicidate 10%v\v 30. L-carvone 10%v\v 286

Providers Odorant name Concentration Providers Odorant name Concentration

Givaudan-Roure (cont.) Givaudan-Roure (cont.) 31. Lentisque ABS esterel 10%v\v 41. Patchouly 10%v\v 32. Lillal 10%v\v 42. Peach 10%v\v 33. Lime oil 10%v\v 43. Pepper oil 10%v\v 34. Methyl pamplemousse 10%v\v 44. Peppermint oil 10%v\v 35. Methyl salicylale 10%v\v 45. Peru balsam ABS 10%v\v 36. Mimosa RGV 10%v\v 46. Sandalwood 10%v\v 37. Muguet 10%v\v 47. Star anise oil 10%v\v 38. Narcisse RGV 10%v\v 48. Tarragon oil 10%v\v 39. Nutmeg oil 10%v\v 49. Vetyver acetate 10%v\v 40. Orange oil bitter 10%v\v 50. Viridine 10%v\v

Note. v\v: volume\volume, w\v: weightYvolume 287

Appendix B Exact Instructions Used with SAM* SMELL, in English and in French

Bl) English Instructions "You will be presented with little bottles containing different odors. You will smell them and evaluate their properties. You will smell each one only once, when the experimenter will place it under your nose. It is really important to be attentive when you smell each odor in order to give accurate ratings.

- You will rate the intensity of the odor (how strong or intense it smelled?) - the pleasantness of the odor (how unpleasant or pleasant you find that odor?) - the familiarity of the odor (how much you had the impression of knowing that odor?) and finally - the arousal of the odor (how intense was your emotional reaction to that odor, how calming or exciting was your reaction to the odor?)

Immediately after smelling each odor, you will give your ratings. You must take a minimum of 30 seconds to do your ratings (or, if you prefer, you cannot smell odors at a faster pace than one every 30 seconds...). You can write your check mark on the SAM drawing or in between two of them, if it represents more accurately what you have felt. *** Be careful to mark your answers to the corresponding odor on the answer sheets!!! Do you have questions?"

B2) French Instructions « Des petites bouteilles contenant diverses odeurs vous seront presentees. Vous devrez les sentir et evaluer leurs proprietes. Vous sentirez chaque bouteille seulement une fois. lorsque l'experimentateur la placera sous votre nez. II est tres important d'etre attentif quand vous sentirez chacune des odeurs, afin d'en faire une evaluation precise.

- Vous evaluerez rintensite.de l'odeur (la force ou l'intensite de ce que vous avez senti) - l'agreabilite de l'odeur (avez-vous trouvez l'odeur deplaisante ou plutot plaisante?) - la familiarite de l'odeur (a quel point aviez-vous l'impression de connaitre l'odeur?) et finalement - l'eveil ou l'intensite emotionelle de l'odeur (quelle etait l'intensite de votre reaction emotionnelle a cette odeur, l'odeur vous a-t-elle plutot calmee ou excitee?)

Immediatement apres avoir senti chaque odeur, vous allez dormer votre evaluation. Vous devez prendre un minimum de 30 secondes pour effectuer votre evaluation (ou, si vous preferez, vous ne pouvez pas sentir plus d'une odeur a toutes les 30 secondes...) Vous pouvez marquer votre reponse sur SAM ou entre deux dessins, si cela represente plus precisement votre reaction. *** Faites attention: inscrivez bien vos reponses a l'odeur correspondante sur les feuilles de reponse!!! Avez-vous des questions? » 288

Appendix C Correlations for Left and Right Amygdala and Odor Memory Measures

Right Left Right d' total d' d' Amygdala Hippocampus Hippocampus nonarousing arousing

Left r(14)= -0.9 0.68 -0.87 -0.19 -0.01 -0.34 Amygdala />=.0001 0.004 0.00001 0.47 0.96 0.2

Right -0.66 0.9 0.28 0.09 0.35 Amygdala 0.005 0.00001 0.3 0.75 0.19

Left -0.54 -0.25 -0.37 0.03 Hippocampus 0.03 0.35 0.16 0.92

Right 0.2 -0.04 0.34 Hippocampus 0.45 0.89 0.19 289 )

Appendix D ANOVA of Mean Ratings in the Different Groups Partitioned for d' and C.

To make sure that the partitioning procedure was efficient in creating groups with different mean ratings, we carried out four similar univariate ANOVAs. The two first ANOVAs were performed on the ratings of intensity and pleasantness of odors partitioned as a function of intensity and pleasantness (intensity and pleasantness were within group variables). The two other ANOVAs were performed on the ratings of arousal and pleasantness of odors partitioned as a function of arousal and pleasantness (here, arousal and pleasantness were the within group variables). All ANOVAs also included subject group as between groups factor (healthy individuals, MTLR patients).

Table Dl ANOVAs for SAM*SMELL Ratings of Intensity and Pleasantness for Odors Partitioned as a function of Intensity (I) and Pleasantness (P) by Subjects (S)

Effect F Differences

Ratings of Intensity P (1,36)=0.57 .46 I (1,36)=1632.84 .0001 * Odors in intense groups were given higher intensity ratings than odors in weak groups. S (1,36)=1.75 .19 P*I (1,36)=16.19 .0001 * Odors in the weak pleasant group were rated as more intense than odors in the weak unpleasant group (p=.01) S*P (1,36)=3.09 .06 S*I (1,36)=0.24 .62 S*I*P (1,36)=0.71 .4 ) 290

Ratings of Pleasantness

p (1,36)= 5946.42 .0001 « Odors in the pleasant group were rated as more pleasant than odors in unpleasant group. I (1,36)=2.03 .16 s (1,36)=1.06 .31 P*I (1,36)=13.71 .007* Odors in the intense unpleasant group were rated as less pleasant than odors in the weak unpleasant group (p=.006). S*P (1,36)=0.007 .93 S*I (1,36)=0.81 .37 S*I*P (1,36)=0.003 .95

Table D2 ANOVAsfor SAM*SMELL Ratings of Arousal and Pleasantness for Odors Partitioned as a function of Arousal (A) and Pleasantness (P) by Subjects (S)

Effect F Differences

Ratings of Arousal

P (1,36)=6.42 .02* Odors in the unpleasant groups were rated as less arousing than odors in the pleasant groups. A (1,36)=1207.2 .0001 * Odors in the nonarousing groups were rated as less arousing than odors in the arousing groups. S (1,36)=0.6 .8 P* A (1,36)=16.31 .0003 * Odors in the unpleasant nonarousing group were rated as less arousing than odors in the pleasant nonarousing group (p=.0001). 291

S*P (1,36)=1.35 .25 S * A (1,36)=3.3 .08 S*A*P (1,36)=0.44 .51

Ratings of Pleasantness

P (1,36)=6281.71 .0001 * Odors in the pleasant group were rated as more pleasant than odors in the unpleasant groups. A (1,36)=0.05 .82 S (1,36)=0.27 .61 P*A (1,36)=34.86 .0001 * Odors in the nonarousing unpleasant group were rated as more pleasant than odors in the arousing unpleasant group (p=.0001) and odors in the nonarousing pleasant group were rated as less pleasant than odors in the arousing pleasant group (p=.0001). S * P (1,36)=0.01 .9 S*A (1,36)=0.001 .99 S*A*P (1,36)=1.03 .32 292

Appendix E

Test for Floor Effect in Odor Memory

We performed Mests to ascertain the absence of a floor effect in odor memory results. In the two subject groups (healthy, MTLR), we compared the mean number of hits (H), hits minus false positive errors (H-FP) and correct rejections (CR) to the value of 0 and the number of misses (M) and false positive errors (FP) to the maximum value of21.

Contrast Healthy participants MTLR

f(18) p f(18) p

HvsO 18.44 .0001 17.67 - .0001

H - FP vs 0 4.57 .0001 5.01 .0001

CRvsO 21.56 .0001 15.05 .0001

Mvs21 18.08 .0001 17.7 .0001

FPvs21 21.56 .0001 15.05 .0001 293

Appendix F

Intensity, Pleasantness, Familiarity and Arousal Ratings and Dilutions of Odorants in Set A and Set B. Mean Ratings are from an Earlier Study (Pouliot, Hudry & Jones-Gotman, 2003).

Mean rating

Intensity Pleasantness Familiarity Arousal Dilution

Odor Set A

1. Ambrarone 5.17 3.02 4.29 4.44 10 % v\v 2. Anise 5.37 4.56 5.44 4.27 10 % v\v 3. Banana 6.56 5.34 6.71 5.46 10%v\v 4. Bergamot 5.71 4.88 5.49 4.39 10 % v\v 5. Black Pepper 4.8 4.41 4.8 3.93 10 % v\v 6. Butyric acid 5.07 2.49 4.12 4.39 10 % v\v 7. Cardamon 6.76 3.93 4.83 5.54 10 % v\v 8. Cineole 6.27 5.68 6.39 5.54 10%v\v 9. Ethy-3-methy-3- 4.85 6.27 5.66 4.85 10 % v\v phenyglicidate 5.9 6.15 6.6 5.08 10 % v\v 10. Freesia 6.93 2.78 5.9 5.75 10%v\v 11. Ham 6 5.68 6.44 4.98 10%v\v 12. Lime 6.48 4.43 5.08 5.45 1 % v\v 13. Methyl 2-methylbutyrate 5.39 4.76 4.93 3.85 1 % v\v 14. Methyl benzoate 5.46 5.68 5.73 4.32 10%v\v 15. Mousse de chene 6.75 6.43 6.98 6.18 10 % v\v 16. Peanut butter 8.1 1.63 3.85 6.9 1 % v\v 17. Pyridine 6.29 6.29 7.07 5.63 10 % v\v 18. Styrax essence 4.88 5.2 5.83 4.02 10%v\v 19. Viridine 6.27 4.24 5.98 4.85 1 % v\v 20. 2-heptanone

Odor Set B

21. Angelica root 5.34 4.66 5.1 4.02 10 % v\v 22. Basil 6.44 4.02 5.51 5.63 10 % v\v 23. Bois de rose 6.44 5.66 6.73 4.98 10%v\v 24. Carrot 6.85 2.95 4.59 5.49 10%v\v 25. Citronellyl butyrate 4.66 2.78 3.85 4.41 10 % v\v 26. Coffee 6.12 5.54 6.73 5.54 10 % v\v 27. Eugenol 6.7 5.28 6.65 5.45 10 % v\v 28. Galbanum oil 4.17 4.59 4.49 3.51 10%v\v 29. Garlic 7.61 3.76 6.49 5.93 10 % v\v 30. Guava 6.05 7.41 7.15 5.51 10 % v\v 31. Mimosa 6.51 6.37 6.8 5.12 10 % v\v 32. Octyl acetate 4.68 4.44 4.41 3.95 10%v\v 33. Orange 5.59 5.98 6.44 5.1 10%v\v 34. Patchouly 5.51 4.63 6.02 4.32 10%v\v 35. Peru balsam 4.83 5.66 6.02 4.39 10 % v\v 36. Pine needles 5.24 4.49 4.8 4.15 10 % v\v 37. Tarragon 4.73 4.49 4.95 3.93 10%v\v 38. Thymol 6.22 4.41 6.54 4.88 7.6% w\v 294

39. Trans-cinnamyl butyrate 6.2 2.58 4.2 5.05 10%v\v 40. Verdone 6.35 4.2 5.38 5.13 10%v\v

Note. v\v: volumeYvolume; w\v: weightYvolume 295

Appendix G

Partitioning of the 40 Test Odors in Different Pleasantness, Arousal and Retention Interval/Learning Instructions Groups for d'

For each experiment, we calculated d' for odors of 8 groups differing in levels of pleasantness, arousal and retention interval (Experiment 1) or learning intention

(Experiment 2).

As a first step, we rank ordered the 10 target odors by pleasantness ratings for each subject. The ranks for odors given identical ratings were decided on the basis of subjects' mean pleasantness ratings for these odors. The 5 odors with the lowest pleasantness ratings were assigned to the unpleasant group, and the other 5 to the pleasant group.

The second step was conducted within each pleasantness group: we ranked odors by their arousal ratings. Again, ties in ranks were broken on the basis of subjects' mean

arousal rating for these odors. The 3 odors with the lowest arousal ratings in the unpleasant group and the lowest 2 in the pleasant group were designated nonarousing

odors; the remaining odors within unpleasant (2) and pleasant (3) groups were

considered the arousing odors (Table Gl).

These rankings produced for each subject four types of memory target odors: unpleasant nonarousing, unpleasant arousing, pleasant nonarousing and pleasant

arousing. The 20 alternate odors presented as foils during the recognition test were ranked ordered in a similar way (in order to calculate the corresponding four types of

incorrect recognition/false positive rate necessary to compute d'), however average

ratings given by subjects who had rated this alternate set at encoding were used. 296

Table Gl Partitioning of the 20 Test Odors in Different Pleasantness and Arousal Groups

10 Target a and 10 Foil b Odors Arousing Nonarousing

Pleasant 3 2

^ Unpleasant 2 3

Note. This procedure was carried out in Experiments 1 and 2, and was done for each of the retention interval and encoding instruction conditions. a Partitioning based on each subject's ratings of every odor, b Partitioning based on average ratings of each odor given by subjects who rated this alternate odor set. Memory Discrimination and Response Bias Indices

Indices Formulae

H (hit rate) - (number of correct recognitions+0.5) (number of targets+1)

FP (false positive rate) = (number of incorrect recognitions+0.5)

(number of foils+1) d' = Z(H) - Z(FP)

C = -.5 * (Z(H) + Z(FP)) Note. From Snodgrass and Corwin, (1988). 298

Permissions and Copyrights

In this thesis, contains previously copyrighted material. Permission for each was obtained.

1. Reproduction of SAM; copyright by Peter J. Lang (1980). On pages 10, 111, 163 and 198 of this thesis. 2. Reproduction of network model of emotions; copyright by G. H. Bower's (1981). On page 13 of this thesis. 3. Reproduction of a figure illustrating phase by phase recall of emotionally arousing and neutral pictures; copyright by Elsevier (1995). On page 18 of this thesis. 4. Reproduction of schematic representation of the current neurobiological understanding of emotional arousal's enhancing effect on memory; copyright by AAAS (2000). On page 49 of this thesis. 5. Reproduction of a figure displaying amygdala activity while watching emotionally arousing films correlates with long-term recall of the films; copyright by L.Cahill (1996). On page 66 of this thesis. 299

From: Peter J. Lang [[email protected]] Sent: 12 avril 2007 11:17 To: Sandra Pouliot Cc: dorothea roebuck Subject: Re: permission Dear Ms. Pouliot, You have my permission to include the figure of SAM (Lang, 1980) in your PhD dissertation. Sincerely, Peter Lang

On Apr 12, 2007, at 8:19 AM, Sandra Pouliot wrote:

Hi Dr. Lang,

My name is Sandra Pouliot and I am a PhD student at the Montreal Neurological Institute of McGill University, Montreal, Canada. I am currently working on the literature review for my PhD dissertation and I am asking for your permission to include a figure of SAM in it. I am referring to this work:

Lang, P. J. (1980). Behavioral treatment and bio-behavioral assessment: Computer applications. In J. B. Sidowski, J. H. Johnson & T. A. Williams (Eds.), Technology in mental health care delivery systems (pp. 119-137). Norwood, NJ: Ablex Publishing.

Thank you very much for your help,

Sandra Pouliot

PLEASE NOTE: New email [email protected] effective 5/20/04

Peter J. Lang, Ph.D., Director NIMH Center for the Study of Emotion and Attention University of Florida Box 112766 HSC Phone: (352)392-2439 Gainesville, FL 32611 Fax: (352)392-6047 300

From: Gordon Bower [[email protected]] Sent: 7 avril 2007 16:40 To: Sandra Pouliot Subject: Re: error

Yes, OK you have my permission to use that figure 7 from Mood & Memory. Gordon Bower On Apr 6, 2007, at 11:47 AM, Sandra Pouliot wrote:

> Dr. Bower, > > My name is Sandra Pouliot and I am a PhD student at the Montreal > Neurological Institute of McGill University, Montreal, Canada. > I am currently working on the literature review for my PhD > dissertation (working title: Recognition memory for emotionally > arousing odors) and I would like permission to include one of your > figures in it. > > I am referring to this work: > > - Bower, G. H. (1981). Mood and memory, American Psychologist, 36(2), > 129-148 > > Figure 7, p. 136 > > > Sincerely, > > Sandra Pouliot > 301

From: Larry Cahill [[email protected]] Sent: 5 avril 2007 12:08 To: Sandra Pouliot Subject: Re: permission

Sandra it is certainly ok with me, but formal permissions, if needed in your case, i presume need to be obtained from the publishers, who own the copyrights. fyi, my work in recent years has begun to reveal sex influences on the neural correlates of emotional memory that, in my view, can no longer be safely ignored, i attach a few papers fyi that i hope prove interesting and useful cordially

dr. cahill

Hi Dr. Cahill, My name is Sandra Pouliot, I am a PhD student at the Montreal Neurological Institute of McGill University, Montreal, Canada. I am currently working on the literature review for my PhD dissertation and I am asking for your permission to include two figures you have published. I am referring to this work:

- Cahill, Haier, Fallon, Alkire, Tang, Keator, Wu, and McGaugh (1996). Amygdala activity at encoding correlated with long-term, free recall of emotional information, PNAS, 93, 8016-8021 Figure 3, p. 8019

- Cahill & McGaugh (1995). A novel demonstration of enhanced memory associated with emotional arousal, Consciousness and cognition, 4, 410-421. Figure 4, p. 417

Thank you very much for your help, Sandra Pouliot

Department of Neurobiology and Behavior and Center for the Neurobiology of Learning and Memory ADDRESS: CNLM, Qureshey Research Lab, University of California, Irvine California, 92697-3800 USA http://darwin.bio.uci.edu/neurobio/Faculty/Cahill/cahill.htm phone 949 824 1937; FAX 949 824 5244 Page 1 of 1

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11 AAAS Permissions Letter Ref# 07-21782 DATE: 6 April 2007

TO: Sandra Pouliot McGill University, Montreal Neurological Institute 3801 University Street Montreal Qu H3A 2B4 Canada

FROM: Emilie David, Rights and Permissions RE: Your request for permission dated 04/05/07

Regarding your request, we are pleased to grant you non-exclusive, non-transferable permission to use the AAAS material identified below in your dissertation or thesis identified below, but limited to print and microform formats only, and provided that you meet the criteria below. Such permission is for one-time use and therefore does not include permission for future editions, revisions, additional printings, updates, ancillaries, customized forms, any electronic forms, braille editions, translations, or promotional pieces. We must be contacted for permission each time such use is planned. This permission does not apply to figures / artwork that are credited to non-AAAS sources. This permission does not include the right to modify AAAS material.

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Permission is valid for use of the following AAAS material only: Fig 2 from James L. McGaugh, SCIENCE 287:248-251 (14 January 2000) In the following work only: Chapter 2. Literature review, RECOGNITION MEMORY FOR EMOTIONALLY AROUSING ODORS published by McGill University in 2007

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