THE ROLE OF ORBITAL FRONTAL CORTEX IN EMOTIONAL REASONING

HOI LING (ELAINE) LAM

A THESIS SUBMITTED TO THE FACULTY OF GRADUATE STUDIES

IN PARTIAL FULFILLMENT OF THE REQUIREMENTS

FOR THE DEGREE OF

MASTER OF ARTS

GRADUATE PROGRAM IN PSYCHOLOGY

YORK UNIVERISTY

TORONTO, ONTARIO

AUGUST 2012

© Hoi Ling (Elaine) Lam, 2012 Library and Archives Bibliotheque et Canada Archives Canada

Published Heritage Direction du 1+1 Branch Patrimoine de I'edition 395 Wellington Street 395, rue Wellington Ottawa ON K1A0N4 Ottawa ON K1A 0N4 Canada Canada Your file Votre reference ISBN: 978-0-494-91745-9

Our file Notre reference ISBN: 978-0-494-91745-9

NOTICE: AVIS: The author has granted a non­ L'auteur a accorde une licence non exclusive exclusive license allowing Library and permettant a la Bibliotheque et Archives Archives Canada to reproduce, Canada de reproduire, publier, archiver, publish, archive, preserve, conserve, sauvegarder, conserver, transmettre au public communicate to the public by par telecommunication ou par I'lnternet, preter, telecommunication or on the Internet, distribuer et vendre des theses partout dans le loan, distrbute and sell theses monde, a des fins commerciales ou autres, sur worldwide, for commercial or non­ support microforme, papier, electronique et/ou commercial purposes, in microform, autres formats. paper, electronic and/or any other formats.

The author retains copyright L'auteur conserve la propriete du droit d'auteur ownership and moral rights in this et des droits moraux qui protege cette these. Ni thesis. Neither the thesis nor la these ni des extraits substantiels de celle-ci substantial extracts from it may be ne doivent etre imprimes ou autrement printed or otherwise reproduced reproduits sans son autorisation. without the author's permission.

In compliance with the Canadian Conformement a la loi canadienne sur la Privacy Act some supporting forms protection de la vie privee, quelques may have been removed from this formulaires secondaires ont ete enleves de thesis. cette these.

While these forms may be included Bien que ces formulaires aient inclus dans in the document page count, their la pagination, il n'y aura aucun contenu removal does not represent any loss manquant. of content from the thesis. Canada Abstract

While it is widely accepted that emotions interact with and affect logical reasoning, very few studies, have explored, the basis of this interaction, particularly at the neural level. Goel and his colleagues’ (Goel & Dolan, 2003) recent study provided initial evidence for differential roles of the dorsolateral prefrontal and ventral medial prefrontal cortex in reasoning about emotionally neutral and emotionally salient material,, respectively. The present study further examined the role of orbital frontal cortex in emotional reasoning. We tested patients with unilateral focal lesions in orbital frontal cortex (i.e., OFC - BA 10 and

11), patients with lesions in parietal cortex,, and normal participants as they made logical inference on emotionally salient and neutral syllogisms. We found only patients with OFC to be impaired in reasoning about emotional material but not in reasoning about neutral material. The subsequent analyses revealed that this impairment was driven by the incongruent syllogisms. The fact that the same patients were reasoning well in the neutral incongruent trials suggested it was the presence of emotion that interrupted the conflict detection system. These results consolidated the findings of the imaging study by demonstrating the necessity of

OFC for reasoning with emotional material. This suggests OFC plays a crucial role in processing or abstracting emotion from the materials before passing on to the logical reasoning engine. Table of Contents

Abstract ...... ii

Table of Contents ...... iii

List of Tables ...... iv

List of Figures ...... v

Introduction ...... 1

Method ...... 20

Results ...... 26

Discussion ...... 34

Conclusion ...... 39

References ...... 41

Appendices ...... 46

Appendix A: List of the syllogisms ...... 46 iv

List of Tables

Table 1: Characteristics of Patient and Normal Control Samples ...... 22

Table 2: Samples of Syllogisms ...... 23 List of Tables

Figure 1: Overlays of 17 patients with lesions in the left and right orbital frontal cortex...... 21

Figure 1: Overlays of 12 patients with lesions in the parietal lobe 21

Figure 3; The interaction between groups and content in accuracy ...... 27

Figure 4: Group’s reaction time as a function of content ...... 29

Figure 5a: Group’s accuracy rate on congruent trials as a function of content....30

Figure 5b: Group’s accuracy rate on incongruent trials as a function of content ...... 30

Figure 6a: Group’s reaction time on congruent trials as a function of content ...... 31

Figure 6b: Group’s reaction time on congruent trials as a function of content ...... 31

Figure 7: Group’s believability rating on incongruent trials as a function of content

Figure 8: The total number of trials each group rated as a function of emotionality in emotional incongruent trials ...... 34 Role of Orbital Frontal Cortex on Emotional Reasoning 1

Introduction

What is logical reasoning? Let us consider the following argument:

Argument 1

All Pad users are Mac supporters

No Mac supporters are PC users

Therefore no PC users are iPad users

Logical reasoning is a process we engage in to draw conclusions (i.e., the third sentence) from the given information (i.e., the premises - the first two

sentences). Argument 1 above is also referred to as deductive reasoning.

Deductive reasoning often is held as a prime example of human intellectual ability

and a key method of gaining knowledge. In the simplest terms, deductive

reasoning starts with a general case and deduces to specific instances. It is a

closed system in which the conclusions are contained within the premises and

are logically independent of the content of the propositions. A deductive

argument is valid if the conclusion follows necessarily from the premises.

Argument formats, such as syllogistic reasoning (e.g., Argument 1) and

conditional reasoning (e.g., If it rains, I get wet. It is raining, therefore I am getting

wet), has been used to explore and examine the ways in which people reason,

and how and why people make mistakes.

Reason, Emotion, and Belief Role of Orbital Frontal Cortex on Emotional Reasoning 2

It is clear that the process of logical reasoning is affected by a number of factors, such as our emotional states and our beliefs. For example, one day I was shopping for vitamins for my son, two brands contained the vitamins I was looking for with exactly the same ingredients. However, one brand was 2/3 of the price of the other brand. As a smart and rational customer, it made perfect sense to get the cheaper one with the same ingredients. However instead of following my rational sense, I decided to buy the more expensive brand because I believed that the more well-known brand was more reliable. In addition to belief, emotion also plays a crucial role in our daily reasoning, even to people who are experts in logical reasoning. My supervisor once shared with us his own experience as follows. He had a broken appliance and found a repair store located 30-45 minutes away from his home. He was told that it would be ready to pick up anytime in the morning of the following day. He dropped by the store in the morning expecting to pick up his appliance as agreed. However, he was told that it was not ready and that he had to come back in the afternoon. In addition to that, the appliance appeared to have never been touched. Despite the unreliable and unprofessional attitude of the store manager, it made more sense just to wait and come back in the afternoon to pick up the appliance in order to save the hassle of traveling around and the additional waiting period. However, my supervisor was upset to the point his logical sense was taken over by his anger. He asked to have his broken appliance back immediately, drove around for hours to look for another repair store and was told to come back a few days Role of Orbital Frontal Cortex on Emotional Reasoning 3

later to pick it up. Whereas there has been much research on the effect of belief

on reasoning, only a limited number of studies have focused on the effect of

mood and emotional content on different forms of reasoning.

Emotion-Reason Interactions

For decades, the relationship between emotion and reasoning has

fascinated people across a wide range of scientific disciplines, including (but not

limited to) cognitive psychology, neuroscience, and economics. Deductive

reasoning in general and syllogistic reasoning (e.g., argument 1 and 2 below) in

particular are prevalent in everyday thinking and representative of the human

potential for logical thinking. However, relatively little empirical research has been

dedicated to examining the effect of emotion on logicality. What is the role of

emotion in logical reasoning? Let us consider the following arguments:

Argument 1 (e.g., Neutral) Argument 2 (e.g., emotional)

All iPad users are Mac supporters All iPad users are smart people

No Mac supporters are PC users No smart people are homosexuals,

Therefore no PC users are iPad users Therefore no homosexuals are iPad users

Argument 1 on the left is the same one as discussed earlier. This argument is an example of an emotionally neutral syllogism. Argument 2 on the

right has an identical logical form as the one on the left, however, it contains emotionally charged content. In everyday reasoning, emotions are likely to be

involved. Are there differences between reasoning about emotionally charged Role of Orbital Frontal Cortex on Emotional Reasoning 4

situations and emotionally neutral situations? A number of studies (e.g.,

Blanchette, 2007; Blanchette & Richards, 2004,; Channon & Baker, 1994;

Oaksford, Morris, Grainger, & William, 1996) have focused on the role of

emotions and demonstrated that they have a detrimental effect on logical

reasoning regardless of whether they are manipulated through the content of logical arguments, mood of participants, or both. Other studies (e.g., Blachette,

Melnyk, Richards, & Layda, 2007) have suggested that the effect also can be beneficial to the reasoning process.

Channon and Baker (1994) reported that people who suffered emotional distress showed impairment in logical reasoning. Compared with the normal group, depressed undergraduate students performed significantly worse when asked to make a logical inference of the form “All A’s are B’s. All B’s are C’s. What can we say about A?” Students then were given a list of possible conclusions and instructed to choose the valid conclusion. Channon and Baker (1994) concluded that the high error rate on syllogisms in the depressed group was due to the inconsistent application of reasoning strategies.

Artificially inducing mood seems to have a similar effect. Oaksford and colleagues (Oaksford et. al, 1996) induced positive and negative moods in different groups of participants and compared their performance on a version of the Wason task (i.e., If a passenger form says “ENTERING” on one side, then the other side must include cholera.) to a neutral mood control group. The participants in the Role of Orbital Frontal Cortex on Emotional Reasoning 5

experimental groups (both positive and negative moods) were less likely to provide

logically valid responses.

A recent study conducted in a naturalistic setting after the terrorist attacks in

London, UK reported slightly different results (Blanchette et at., 2007). Participants were recruited within a week of the attacks of July 7 in London from three cities,

London (UK), Manchester (UK), and London (Canada). London, UK participants reported the highest level of fear. Reasoning trials with three types of content were administered: emotionally neutral, generally emotional, and emotional specific to terrorism. While the overall result showed emotional syllogisms interfered with

logical response across all three groups, the London UK group (i.e., whose experienced the terror attack) provided more logically valid answers in reasoning about terrorism related content. Their finding suggests that emotions can sometimes facilitate logical reasoning.

To determine whether emotionality of content alone may affect reasoning the same way as emotional or mood state, Blanchette and her colleague

(Blanchette, 2007; Blanchette & Richards, 2004) conducted a series of studies manipulating emotionality of the stimuli. Participants were given conditional statements comparing the degree (i.e., emotional vs. neutral) and type (i.e., anxiety, sadness, and happiness) of emotional content. The result suggested that the emotional content of reasoning material may influence people’s responses on conditional reasoning tasks. However the interpretation of the result was difficult due to the entanglement between semantic and emotional components of the argument. To disentangle the semantic and emotional effect on reasoning, neutral Role of Orbital Frontal Cortex on Emotional Reasoning 6 words and nonwords were conditioned to become emotional or remain neutral through repeated presentation with images of negative, positive, and neutral emotional connotation. Again, the results showed that participants were more likely to draw incorrect inferences in response to emotional compared with neutral statements. In a more recent study, Blanchette (2007) again reported that participants tended to provide logically invalid answers when asked “if a child has been sexually abused, then he has behavioral difficulties”, compared to “if a child eats too much sugar, then he has behavioral difficulties”. In their subsequent experiments, neutral words were conditioned with pictures of neutral, negative, and positive emotional valence, and participants were consistently less likely to provide the normative correct answers on the positively and negatively conditioned stimuli.

To conclude, clinical and non-clinical data provide strong evidence that emotion (i.e., both mood state and content of stimuli) influences deductive reasoning. However, how it affects reasoning remains unclear. Most research suggests that emotions interfere with logical reasoning. A few studies, however, suggests that emotions can sometimes facilitate logical reasoning.

Belief-Reason Interactions

One possible mechanism for the effect of emotion on reasoning is the belief bias effect. Although deductive reasoning is a closed system, our beliefs about the world can influence validity judgments. Let us consider the following arguments:

Argument 1 (e.g., Incongruent) No Mac supporters are PC users

All iPad users are Mac supporters Therefore no PC users are iPad users Role of Orbital Frontal Cortex on Emotional Reasoning 7

All Mac supporters are PC users

Argument 3 (e.g., Congruent) Therefore some PC users are iPad users

Some iPad users are Mac supporters

Argument 1 on the left is again the same syllogism as discussed that

contains emotionally neutral content. This argument is also an example of

incongruent syllogism because the logical response is inconsistent with beliefs.

The argument is valid but its conclusion is inconsistent with one’s belief.

Incongruent syllogisms also occur when an argument is logically invalid but its

conclusion consistent with one’s belief. In contrast, argument 3 on the right is an

example of a congruent syllogism because the logical response is consistent with

one’s belief. Argument 3 is logically valid and its conclusion consistent with one’s

belief. Congruent syllogisms also occur when an argument is invalid and its

conclusion inconsistent with one’s belief. Reasoning in accordance with one’s

belief rather than the logical form is referred to as the belief-bias effect.

Unlike emotion, there are many studies on the role of belief in reasoning.

In fact, the belief-bias effect is among the most robust phenomena within the

reasoning literature. In general, reasoners perform more accurately on reasoning

tasks when the logical conclusion is consistent with their beliefs than when the

conclusion is inconsistent with their beliefs (e.g., Evans, Barston, & Pollard,

1983; Goel & Dolan, 2003a). For example, participants are more likely to accept

a valid conclusion when the conclusion statement is consistent with their beliefs

and an invalid conclusion when the conclusion is inconsistent with their beliefs

(i.e., congruent). In contrast, they are more prone to reject a valid conclusion that Role of Orbital Frontal Cortex on Emotional Reasoning 8

is inconsistent with their beliefs and an invalid conclusion that is consistent with their beliefs (i.e., incongruent). In other words, when the logic is congruent with one’s beliefs (i.e., the former case), there will be a facilitative effect and reasoners are far more likely to perform correctly. However, when the logic is incongruent with one’s beliefs, reasoners will have to inhibit the belief-bias effect in order to make a correct inference, resulting in more logically incorrect responses.

Interaction among Emotion, Belief, and Reasoning

As noted above, studies suggested that logical inferences are often influenced by emotion, sometimes to our detriment, sometimes to our advantage.

Given that content results in the belief-bias effect, Goel and Vartanian (2012) proposed that emotional content might affect the reasoning process by increasing or decreasing the influence of beliefs on reasoning process, and this modulation will have differential impact on congruent and incongruent reasoning trials. To test their hypothesis, Goel and Vartanian (2010) instructed participants to reason about syllogisms involving neutral or emotionally charged content. They also manipulated the consistency of beliefs and logical validity (i.e., congruency of the syllogisms). They reported that participants exhibited the belief-bias effect when the content was neutral as well as emotional. However, when confronted with emotionally charged content, participants were less likely to be influenced by their beliefs. They concluded that under certain conditions, negative emotion could actually attenuate the influence of beliefs during logical reasoning. Role of Orbital Frontal Cortex on Emotional Reasoning 9

Consistent with Goel and Vartanian’s (2010) finding in supporting the influence of affective process in reasoning by modulating the belief-bias effect, a neuroimaging study investigated the role of belief on the neural basis of reasoning and reported a strong association between affective processing and belief-bias effect in reasoning. Goel and Dolan (2003a) employed a similar experimental paradigm (i.e., without manipulating the emotion of the content) in explaining how belief modulates reasoning. Fourteen volunteers were asked to make validity judgments, as they performed reasoning tasks under neutral (i.e., belief-neutral baseline trials), facilitatory (i.e., belief-laden congruent trials) and inhibitory conditions (i.e., belief-laden incongruent trials). The authors reported activation in right lateral prefrontal cortex when participants inferred logically by inhibiting belief bias. In contrast, when logical reasoning was overpowered by belief bias, activation in ventral medial prefrontal cortex was found, a region implicated in affective processing. In accordance with Goel and Vartanian

(2010), this finding suggested that belief-bias effects in reasoning might be mediated through an influence of emotional processes on reasoning.

These studies provide evidence and suggest that the interaction between emotion and reasoning can be modulated through beliefs; however, exactly how emotion interacts with reasoning remains unclear. The objective of the present study is to better understand the neural basis of emotion-reason interaction.

Based on the implication of ventral medial prefrontal cortex (VMPFC) on emotion- reason interaction suggested above, we hypothesized that patients with lesions Role of Orbital Frontal Cortex on Emotional Reasoning 10

to the ventral medial orbital frontal region would be impaired when reasoning about the emotional materials but not when reasoning about neutral materials.

The role of prefrontal cortex

Through evolution, humans have acquired higher cognitive skills (i.e., language, reasoning and planning) and complex social behavior. Although evidence from neuropsychological and neuroimaging research indicates that the prefrontal cortex (PFC) underlies much of this higher cognition, it is unclear how and where functions are fractionated within this region. According to a recent review by Wood and Grafman (2003), the PFC can divide into medial and lateral regions, each of which is associated with subcortical brain regions. It is thought that the medial PFC has reciprocal connection with brain regions that are associated with emotional processing (amygdala), memory (hippocampus) and higher-order sensory processing (temporal and visual association areas), whereas lateral PFC has reciprocal connection with brain regions that are associated with motor control (basal ganglia, premotor cortex, supplementary motor area), performance monitoring (cingulate cortex), and higher-order sensory processing (association areas, parietal cortex). The medial PFC is well suited to support functions involving the integration of information about emotion, memory, and environmental stimuli, and the lateral PFC to support the regulation of behavior and control of responses to environmental stimuli. Role of Orbital Frontal Cortex on Emotional Reasoning 11

Overall, our current understanding suggests the medial PFC is implicated in emotional processes and social behavior, and the lateral PFC is related to cognitive processes, such as reasoning and planning.

OFC and Theory of Mind (ToM) reasoning

The implication of orbital frontal cortex including the regions of ventral

medial prefrontal cortex in affective processing is consistent with several related fMRI studies involving affective ToM reasoning, mentalizing, and emotional

perspective-taking. For example, Shamay-Tsoory, Tibi-Elhanany, and Aharon-

Peretz (2006) reported that subjects with ventral medial (vm) damage were less

impaired in the cognitive ToM conditions than in the affective ToM conditions.

There were four types of ToM tasks (i.e., second-order false belief, false attribution, detection of irony, and understanding of lies), each including a cognitive subtask (e.g., cognitive ToM scenario: Person B is operating an object while person A is out of the room. However, person A peeks back and watches what person B does. Person B does not know that person A saw his deed; cognitive ToM questions: What does person B think that person A thinks about the object’s condition, when person A returns to the room? What does person A think about the condition of the object? What is condition of the object?) and

affective subtask (e.g., affective ToM scenario: Person A accidentally spills some wine on person B and leaves the room. However, person A peeks back, sees

person B’s angry reaction and feels guilty. Person B does not know that person

A saw him; affective ToM questions: When person A returns to the room, how Role of Orbital Frontal Cortex on Emotional Reasoning 12

does person B think that person A feels? What does person A think person B feels? How is person B feeling?). Their finding indicated that VM patients were able to represent false beliefs and to understand false attributions, lies, and irony when the task did not involve affective ToM reasoning. However, as compared to healthy controls and patients with posterior damage, subjects with VM damage tended to produce more errors when story comprehension required affective reasoning (e.g., to identify person B’s affective mental state or to express an affective mental state). Another study conduced by Shamay-Tsoory and Aharon-

Peretz (2007) reported a dissociation between cognitive and affective theory of mind. They found that whereas affective ToM was mostly impaired by VM damage, cognitive ToM was mostly impaired by extensive prefrontal damage

(i.e., VM+DLC), suggesting that cognitive and affective mentalizing abilities are partly dissociable. They concluded that the mediating role of the VM in the affective facets of social behavior may underlie the behavioral disturbances observed in these patients. They further proposed that the intimate connections of VMPFC with the anterior insula, temporal pole, inferior parietal region, and amygdala placed it in a position to evaluate and regulate incoming limbic information which could be used to inhibit behavior, regulate emotions and empathize with the experiences of others (Shamay-Tsoory & Aharon-Peretz,

2007).

The medial regions of the orbital frontal cortex often are considered to be crucial areas for empathic processing, which require emotional perspective- Role of Orbital Frontal Cortex on Emotional Reasoning 13

taking. To address this, Hynes, Baird, and Grafton (2006) presented participants with scenarios with and without emotional valence. Emotional perspective-taking focused on what the characters were feeling. For example, participants were

given a scenario such as “Ruth is driving away from Debbie’s place when

Debbie’s cat runs suddenly into the road. She hits the brakes, but feels her car go

over something. She stops and checks to see whether she has killed the cat.

She finds that she ran over a bump in the road, and that the cat is safely on the

other side of the road”. Then they were asked: “How does Ruth feel?” In

contrast, cognitive perspective-taking focused on what the characters are

thinking. For example, participants were presented with a scenario, such as “A

burglar who has just robbed a shop is making his get-away. As he is running

away, a policeman sees him drop a glove. He wants to tell him he dropped his

glove. When the policeman shouts out to the burglar, “Hey, you! Stop!” the

burglar turns round, sees the policeman and gives himself up”. Then the

participants were asked: “Why did the burglar give himself up?” Emotional

perspective-taking was contrasted with cognitive perspective-taking in order to

examine the role of the orbital frontal lobe in a subcomponent of theory of mind

processing. The group results demonstrated that the medial orbitofrontal lobe

was preferentially involved in emotional as compared to cognitive perspective-

taking. They further suggested that the orbitofrontal cortex involvement cannot be

reduced to decision-making processes, and that the orbitofrontal cortex may have

a privileged role in emotional perspective-taking. Role of Orbital Frontal Cortex on Emotional Reasoning 14

A couple of recent review papers also highlighted the role of the medial regions of orbital frontal cortex in mentalizing or “affective ToM”. For example, a review (Gilbert, Spengler, Simons, Steele, Lawrie, Frith, & Burgess, 2006) on the functional specialization within BA 10 reported that studies involving working memory and episodic memory retrieval were disproportionately associated with lateral activations, whereas studies involving mentalizing (i.e., attending to one’s own emotions and mental states or those of other agents) were disproportionately associated with medial activation. Specifically, it appears that activation in medial BA10 was associated with tasks that involved both mentalizing and emotional materials. The activation of medial PFC in contrasts involving emotional materials (at least in Mentalizing tasks) is consistent with previous investigations suggesting that medial and lateral PFC are preferentially involved in emotional and cognitive tasks, respectively.

For example, in a meta-analysis of neuroimaging studies investigating emotion, Phan, Wager, Taylor, and Liberzon (2002) found that medial PFC was more commonly activated than lateral prefrontal regions, consistent with previous reports of strong interconnections between the limbic system and medial prefrontal regions (e.g., Porrino, Crane, & Goldman-Rakic, 1981). In addition, the medial PFC has been suggested as playing a crucial role in self and other evaluation of emotion (Ochsner, Knierim, Ludlow, Hanelin, Ramachandran,

Glover, et al., 2004) and in self-reflection when a protagonist is perceived as similar to the self (Mitchell, Banaji, & Macrae, 2005). Role of Orbital Frontal Cortex on Emotional Reasoning 15

OFC and Moral reasoning

Although traditional accounts of moral development focus on the development of rational and deliberate thinking, recent work in affective neuroscience suggests that moral cognition is tightly related to affective and emotional processing. For example, Greene, Sommerville, Nystrom, Darley, and

Cohen (2001) focused on the specific differences between making judgments

(i.e, appropriate or inappropriate) of moral personal dilemmas (e.g., throwing a person out of a sinking lifeboat to save others), and moral impersonal dilemmas

(e.g., keeping money found in a lost wallet). Moral dilemmas involving a personal component, compared with both impersonal moral dilemmas and nonmoral dilemmas, activated the medial frontal gyrus (BA 9 and 10), the posterior cingulate (BA 31), and both left and right angular gyri (BA 39). This initial study suggested that these structures play a central role in the emotional processes that influence personal moral decision-making. Other studies have confirmed the importance of the medial PFC, angular gyrus, and posterior cingulate in processing moral stimuli. For example, the medial PFC (and the frontal pole, BA

10) is activated by passive viewing of pictures depicting moral vs. nonmoral violations (Moll, Oliveria-Souza, Bramati, & Grafman, 2002a), making judgments with respect to auditory moral vs nonmoral sentences (Oliveira-Souza & Moll,

2000), passive viewing of morally disgusting vs. nonmorally disgusting statements (Moll et al., 2005); moral decision-making vs. semantic decision­ making (Greene, Nystrom, Engell, Darley, & Cohen, 2004), personal vs. Role of Orbital Frontal Cortex on Emotional Reasoning 16

impersonal moral dilemmas (Greene et al., 2004), and judgment about moral vs. non-moral actions (Borg, Hynes, Van Horn, Grafton, & Sinnott-Armstrong, 2006).

Consistently, studies report activation of fronto-polar cortex (particularly the medial aspects of BA 10) in moral judgment tasks.

The above studies provide important clues as to the neural circuit underlying moral emotions and reasoning and decision-making. A different question that can be asked concerns which brain areas are involved in the regulation of moral emotions. In addressing this issue, Harenski and Hamann

(2006) not only assessed activation during unpleasant moral vs. unpleasant nonmoral social picture viewing, but also requested participants to suppress their emotional reactions to both sets of stimuli. As expected, the two brain areas activated by moral (vs. non moral) condition were the angular gyrus and the posterior cingulate. In contrast, suppression of emotion to pictures of normal transgression leads to a reduction in amygdala activation and an increase in polar/medial PFC (BA 10) activation. These findings suggest a unique activation role for area 10 of the PFC in both the process of moral decision-making and in the regulation of moral emotions. Deactivation of the amygdala during down- regulation of moral emotions provides further credence to its active involvement in the generation of moral emotions.

OFC and Decision Making Role of Orbital Frontal Cortex on Emotional Reasoning 17

Damasio offered initial evidence to support the view that rationality requires emotional input (Bechara, Damasio, Tranel, & Damasio, 1997; Damasio,

1994, 1999, 2003). Using brain lesion data, Damasio and his colleagues showed that damage in ventromedial prefrontal cortex causes defects in reasoning/decision making, emotion, and self-feeling. In line with Damasio’s finding, Houde and his colleagues (Houde, Zago, Crivello, Moutier, Pineau,

Mazoer, & Tzourio-Mazoyer, 2001) demonstrated that “emotion and feeling assist reasoning not only when it comes to personal and social matters involving risk and conflict, but also when it comes to deductive logic per se” (p. 1491). In their study, healthy participants were given either a “hot” kind of training (i.e., logicemotional training - training on Wason’s card selection that triggered a perceptual matching bias with emotional warning such as “...not to fall into the trap of the two cards A and 3 mentioned in the rule ... eliminate the wrong ones - the ones that make you fall into the trap...) or a “cold” kind of training (i.e., same as logicemoitonal training without the emotional warning elements). They found the error-to-logical shift occurred only in a group that underwent logicemotional training but not in the other group. The intergroup comparison reported greater cerebral activity in the right ventromedial prefrontal cortex (VMPFC), linking deductive reasoning to a possible mechanism involving emotion and feeling.

They concluded that the VMPFC could be implicated as the emotional component of the brain’s error-correction device. Together with other subcortical areas, such as anterior cingulate cortex, VMPFC may be a part of the brain Role of Orbital Frontal Cortex on Emotional Reasoning 18

network that detects the condition under which logical reasoning errors might occur.

A recent study (Bar-On, Tranel, Denburg, & Bechara, 2003) on whether the severe impairment of patients (i.e., with lesions in the VMPFC, amygdala, and insular regions) in real-life decision making and in coping effectively with environmental and social demands would be reflected in an abnormal level of emotional and social intelligence. They reported that the neural systems that support emotional and social intelligence appear to overlap with the neural systems subserving somatic state activation and personal judgment in decision­ making. They compared the control group (i.e., patients with lesions outside the neural circuitry thought to mediate somatic state activation and decision-making) to the experimental group (i.e., patients with lesions in VMPFC, amgydala, and insular regions). They reported that the experimental group displayed significantly lower emotional intelligence (i.e., Bar-On EQ-i) and poorer judgment in decision-making (i.e., Gambling task) as well as disturbances in social functioning, in spite of normal levels of cognitive intelligence (IQ) and the absence of psychopathology based on DSM-IV criteria. They concluded that emotional and social intelligence are different from cognitive intelligence.

Furthermore, their results suggested that the neural systems supporting somatic state activation and personal judgment in decision making may overlap with critical components of a neural circuitry subseving emotional and social intelligence. Role of Orbital Frontal Cortex on Emotional Reasoning 19

OFC and Reasoning

Goel and Dolan (2003) also stressed that logical responses often are influenced by emotion. To examine directly the neural basis of emotionally

neutral (“cold”) and emotionally salient (‘hot”) reasoning, Goel and his colleague

manipulated the emotional saliency of syllogisms and asked participants to make validity judgments. They showed that reasoning specific to emotionally neutral arguments (e.g., Some policemen are detectives. All detectives are competent.

Some policemen are competent) engaged left Lateral and Dorsal Lateral

Prefrontal Cortex (L/DLPFC). In contrast, reasoning specific to emotionally

salient content (e.g., All murderous people are criminals. All Nazis were

murderous. Some Nazis are criminal.) revealed enhanced activation in

Ventromedial Prefrontal Cortex (VMPFC) and right fusiform gyrus. More

specifically, ‘cold’ reasoning trials resulted in enhanced activity in L/DLPFC and

relative suppression of activity in VMPFC; by contrast, ‘hot’ reasoning trials

resulted in enhanced activity in VMPFC and relative suppression of activity in

L/DLPFC. This reciprocal pattern of activation provides evidence for a dynamic

neural system for reasoning that is modulated by emotional saliency.

The present study explores the effect of emotionality on deductive

reasoning. The imaging studies (e.g., Goel 2003b) provide evidence for the

sufficiency of orbital frontal cortex for reasoning about emotional material. The

present study aims to investigate the necessity of orbital frontal cortex for

emotional reasoning by testing neurological patients with focal lesions limited to Role of Orbital Frontal Cortex on Emotional Reasoning 20

right or left orbital cortex. We hypothesized that patients with lesions to the ventral medial orbital frontal cortex would be impaired when reasoning about the emotional materials but not when reasoning about neutral materials.

Method

Participants

The present study is based on archival data. All participants were war

veterans who served in Vietnam in the late 1960s. The selection criterion for the experimental group was patients with lesions largely restricted to areas BA 10 and 11 (orbital prefrontal cortex) and largely excluding areas BA 45, 46, and 47

(lateral prefrontal cortex). The patient controls were patients with unilateral

lesions largely limited to the parietal lobe. The healthy controls also served in

Vietnam but did not receive any head injuries. There were 3 groups: orbital frontal

lesion (BA 10 and 11) group (total n=17, left n- 9 and right n=8), parietal lesion

group (total n= 11, left n=7, right n= 4) and healthy normal group (n=22). There were nine patients with brain damage in the left orbital frontal cortex, eight

patients with damage in the right orbital frontal cortex, 11 patients with focal

lesions in the left and right parietal cortex, and 22 healthy participants with no

brain injury. All participants were right-handed, ranging in age from 55 to 65. All

participants gave informed consent. The involvement of specific structures for the

experimental (left and right OFC) and patient-control (PL) groups are specified in

Figures 1, and 2, respectively. Role of Orbital Frontal Cortex on Emotional Reasoning 21

0 * 6 & $ (D0 & Figure 1. Overtay of 17 p£atients with lesions in the l< sft and right o

$ $ •

Figure 2. Overlay of 12 patients with lesions in the parietal lobe

Cognitive and Emotion Assessments

Wechsler Adult Intelligence Scale (WAIS-III, Wechsler, 1997) and

Wechsler Memory Scale (WMS-III, Wechsler 1997b) were administrated to

assess participants’ cognitive functioning level. The sensory, motor, and

language functions, of all patients were relatively intact and all patients were functional to casual observation (in terms of language, behavior and sensory-

motor abilities). Participants’ psychological and emotional functioning was also

assessed by Beck Depression Inventory (BDI, Beck, Steer, & Brown, 1988) and

Global Assessment Functioning (SCID-GAF, First, Spitzer, Gibbon, & William,

1996). BDI was used for measuring participants’ severity of depression. Higher

BDI scores indicated more severe depressive symptoms. SCID-GAF was used Role of Orbital Frontal Cortex on Emotional Reasoning 22

to measure a patient’s ability to function in daily life based on the evaluation of the clinician’s judgment. Higher SCID-GAF scores indicated higher level of daily functioning.

The age, education, cognitive profiles (IQ and Working Memory), emotional and psychological measurements (BDI and SCID), along with the size and laterality of lesion are noted in Table 1.

Table 1 Characteristics of Patient and Normal Control Samples OFC Parietal Lobe Normal Controls M(SD) M(SD) M (SD) Number of Patients (n) 17 11 22 Education (Year) 14(1.68) 15(2.71) 15 (2.82) WAIS General (IQ) 103 (9.74) 102(11.45) 107 (11.03) Verbal (IQ) 104(10.89) 105(12.54) 108 (9.89) Performance (IQ) 102(10.74) 97 (10.83) 106 (11.36) Working Memory 97 (9.86) 89 (14.07) 105(13.60) WMS General Memory 103(12.79) 100(10.48) 105(12.34) Working Memory 99(11.98) 92(10.31) 107 (9.89) BDI 13(12.40) 7 (5.35) 11 (8.22) SCID - GAF 76(11.91) 73(13.98) 74(11.60) Lesion Volumes Loss (cc) 21 (10.84) 29 (31.22) 0

WAIS = Wechsler Adult Intelligence Scale; WMS = Wechsler Memory Scale; BDI = Beck Depression Inventory; SCID-GAF = Structural Clinical Interview for DSM-IV - Global Assessment Function.

Tasks

During the reasoning task, participants were presented with syllogistic reasoning arguments and asked to determine whether the conclusion followed logically from the premises. No time limit was set: participants could take as long as they wished to respond. After completion of the reasoning task, participants Role of Orbital Frontal Cortex on Emotional Reasoning 23

were asked to rate the believability and emotionality for each conclusion of the syllogisms.

Experimental Design

Twenty emotionally salient and 20 emotionally neutral syllogisms were organized into a 3 by 2 by 2 factorial design. All emotional salient syllogisms contained negative emotion. The assignment of items to emotional and neutral was based on a priori decision. The first factor was subject group, consisting of

OFC group, PL group and healthy control group. The second factor was content, in which half of the arguments contained emotionally neutral content, whereas the other half contained emotionally salient content. The logical forms in both conditions were identical. The third factor was congruency, with 10 congruent

(i.e., 4 Valid & True + 6 Invalid and False) and 10 incongruent (i.e., 4 Valid &

False + 6 Invalid & True) trials. Congruent trials were either valid arguments with a true or believable conclusion or invalid arguments with a false or unbelievable conclusion. Incongruent trials were either valid arguments with a false or unbelievable conclusion or invalid arguments with a true or believable conclusion.

Table 2 Samples of Syllogisms Neutral Content Emotional Content Congruent No skiers are smokers. No Americans read the Bible. Syllogism Some men are not skiers. Some Americans are homosexuals. All men are smokers All homosexual read the Bible. Incongruent No coffee contains nicotine. All Americans are brave people. Syllogism No nicotine is found in tea. No brave people are Vietnam Veterans. No tea contains coffee. No Vietnam Veterans are Americans Role of Orbital Frontal Cortex on Emotional Reasoning 24

Task Presentation

Both reasoning and rating tasks were presented via a computer script. For the reasoning task, the stimuli were presented with a syllogism. No time limit was set. Once participant’s response was entered, the next trial followed.

For the believability rating, participants were presented with the last sentence of each of the arguments (e.g., All men are smokers) and asked to rate the believability by entering the corresponding keyboards, scaling from 1 to 5

(i.e., from most unbelievable to most believable). For the emotional rating, participants were presented with the sentence of each of the conclusions on emotional materials only (e.g., All homosexual read the Bible.) and were given a categorical rating on valence and arousal (i.e., 1 for negatively aroused, 2 for negatively calm, 3 for positively calm and 4 for positively aroused).

Post-Experiment Data Adjustment

It is important to note that, in the experimental design described above, the congruency of the task was balanced by an equal number of trials. However, a few adjustments were made before conducting the statistical analysis. Firstly, due to technique error, participants’ responses in one of congruent syllogisms with neutral content was not recorded properly, resulting with 19 trials left in the neutral category. Secondly, we adjusted the congruency of the syllogisms according to each individual’s response. For example, an argument (e.g., Some animals eat children. All animals are pets. Some pets eat children) was initially categorized as an incongruent syllogism (i.e., valid but unbelievable). However, Role of Orbital Frontal Cortex on Emotional Reasoning 25

depending on each participant’s believability rating, the same argument could be categorized as a congruent syllogism if a participant found the conclusion to be

believable instead. The average number of congruent and incongruent trials in each of the content remained relatively balanced after the adjustment [i.e.,

neutral congruent vs. neutral incongruent = 9.62 (1.47) vs. 9.32 (1.30); emotional congruent vs. emotional incongruent = 9.38 (1.41) vs. 10.6 (1.41).] However, to account for the unequal number between the valid and invalid trials within the congruency category, we adjusted our data by weighting the invalid and invalid trials equally [i..e, congruent trials = 0.5 (valid trials) + 0.5 (invalid trials]

In terms of emotional rating, as explained above, the participants were asked to categorize the emotional content of the conclusion of each syllogism

into negatively calm, negatively arousing, positively calm or positively arousing.

One of the possible concerns of this was that we were essentially forcing

participants to treat valence (i.e., Negative = negatively calm + negatively

arousing; Positive = positively calm + positively arousing) and arousal (i.e.,

Aroused = negatively arousing + positively arousing; Calm = negatively calm +

positively calm) independently and orthogonally, which could bias the results and

make interpretation of these data difficult. We addressed this by collapsing together any trials that concern either negative valence or aroused [i.e., high

emotional saliency = Negative + Aroused) and any trials that concern either positive valence or calm [i.e., low emotional saliency = Positive + Calm), and

created the rating of emotionality (i.e., high vs. low emotional saliency). Creating Role of Orbital Frontal Cortex on Emotional Reasoning 26

this new variable also allowed us to 1) keep the simplicity and parsimony of our work, and 2) be consistent with previous studies (e.g., Goel & Dolan, 2003a, Goel

& Vartamian, 2010) which participants were asked to rate the emotionality using a scale ranging from 0 (not at all emotional) to 5 (extremely emotional).

Results

Variables such as years of education, IQ scores, Working Memory (WM)

scores and lesion volume loss are highly correlated with logical reasoning in the

literature. Likewise, Beck Depression Inventory (BDI) scores and GAF scores from Structural Clinical Interview for DSM-IV (SCID) are significant correlates for emotion and mood. To control for any confoundings, we tested for group

differences on these measures. The results indicated that there were no

significant group differences for volume loss [i.e., F(1, 27) = 1.291, p = 0.266],

year of education [i.e., F (2, 46) = 1.145, p = 0.0.327], WAIS III IQ score [i.e., F(2,

49) = 1.449, p = 0.234], SCID-GAF [i.e., F(2, 48) = 0.188, p = 0.829] and BDI

[i.e., F(2, 49) = 2.987, p = 0.069]. Only WM scores were found to be significantly

different across groups, F(2, 48) = 5.845, p = 0.005. WM scores were also

significantly correlated with accuracy scores in reasoning in both neutral [r(50) =

0.496, p > 0.001] and emotional [r(50) = 0.454, p = 0.001] items. Since BDI was

close to significance, both variables BDI and WM were entered into the following

series of statistical analyses as covariates to control for possible confounding.

Overall accuracy in reasoning task performance was 72.4% (SD = 15.4%), Role of Orbital Frontal Cortex on Emotional Reasoning 27

indicating that participants were able to infer accurately at above chance level

(i.e., 50%) and were engaging in the reasoning tasks.

Group by Content by Congruency

Based on the imaging and patient studies, we hypothesized that the OFC patients would be more likely to reason poorly with emotional materials relative to the PL group and the normal control group. Data were first analyzed using a 3 X

2 X 2 mixed ANOVA, which included the variables Group (OFC, PL, and Normal

Control), Content (Neutral and Emotional) and Congruency (Congruent and

Incongruent). There was no main effect of content, F (1, 44) = 0.078, p = 0.781, revealing no significant difference in accuracy for emotionally neutral (M =

73.94%, SD = 14.09%) and emotionally salient ( M = 71.29%, SD = 16.29%) syllogisms. No significant group differences were found [F(2, 44) = 1.183, p =

0.316, suggesting patients with lesions in OFC and PL, and participants with no brain injury performed similarly on the reasoning task. There was an expected significant main effect for congruency [F (1, 44) = 5.997, p = 0.018], confirming that all participants tended to provide more logical responses on the congruent

(M = 82.57%, SD = (14.37%) than incongruent (M = 60.42%, SD = (22.79%) syllogisms. 0.8

0.75

■OFC 0.7 & •Control 2 u3 0.65 u ■PL < 0.6 Neutral Emotional

Figure 3. The interaction between groups and content in accuracy Role of Orbital Frontal Cortex on Emotional Reasoning 28

However, the critical test for our hypothesis was the two-way interaction between Content and Group. This interaction was significant, F (2, 44) = 4.661, p

= 0.015 (Figure 3 above). Specifically, in the neutral items there was no significant group difference [F(2, 49) = 0.28, p = 0.972, ns]. In contrast, there was a significant difference among the groups, F(2,49) = 5.229, p = 0.009 on the emotional items. The post hoc t-tests showed that there was a significant difference between the OFC group and the normal controls, but no difference between the PL group and normal controls, or between the OFC group and PL group. Furthermore, there was no statistical difference in the PL and the normal control groups in reasoning with neutral vs emotional materials, however the OFC group performed significantly worse on the emotional trials than on the neutral trials. These tests suggested that only the OFC patients provided significantly more correct responses on the emotionally neutral than emotional salient syllogisms. This in turn implicates the crucial involvement of OFC on emotional reasoning. No other interaction was found to be significant [i.e., Congruency by

Group, F(2,44) = 1.686, p = 0.197; Content by Congruency, F(1,44) = 0.849, p =

0.362; Group by Content by Congruency. F(2, 44) = 1.543, p = 0.225].

As for the reaction time (RT), we tested whether emotion might foster a more deliberate and analytical information-processing style, predicting longer reaction times in reasoning with the emotionally salient relative to emotionally neutral items (Goel & Vartanian, 2010). We conducted a 3 X 2 X 2 mixed

ANOVA including variables Group (OFC, PL, Normal Control), Content (neutral, Role of Orbital Frontal Cortex on Emotional Reasoning 29

emotional), and Congruency (congruent and incongruent) with RT as the dependent variable. The analysis revealed no significant main effect of content,

F(1, 44) = 1.927, p = 0.172, or congruency, F(1,44) = 1.027, p = 0.316 or main effect of Group, F(1, 44) = 0.134, p = 0.875. No interaction effect on Content by

Group, F(2, 44) = 1.658, p = 0.202, or on Congruency by Group, F(2, 44) = 0.506, p = 0.607, or on Content by Congruency, F(1,44) = 0.329, p = 0.569 or Content by Group by Congruency F(2,44) = 4.505, p = 0.117. Figure 4 below shows that both control and PL groups tended to take longer to reason with neutral materials than with emotional materials, however, OFC patients spent about the same amount of time in reasoning about the emotional trials as the other groups, and even took longer to reason with the neutral items.

30000 U

Control 15000 “ -“ -PL

10000

5000 Neutral Emotional

Figure 4. Groups’ reaction time as a function of content

To investigate if the congruency of the syllogisms plays any role on the effect of interest, we further examined the data by looking the congruent and incongruent trials separately. Three-way interaction of Group by Content by

Congruency was found to be not significant. However, there was difference in Role of Orbital Frontal Cortex on Emotional Reasoning 30

the pattern of the results when the OFC patients reasoned about the congruent

and incongruent trials (Figure 5). Additionally, studies (e.g., Goel & Vartarnian,

2010) have shown that mediation between belief and emotion could have a

differential impact on congruent and incongruent reasoning trials. To examine

whether there was a differential impact on congruence, we conducted a Group by

Content analysis on the congruent trials and the incongruent trials separately.

We found, in incongruent trials, that there was a significant interaction between

the groups and the content of the syllogisms, F(2, 65) = 4.655, p = 0.013, but no

significant interaction was found in congruent trials. The fact OFC patients

performed significantly worse on emotional material than on neutral material in

only incongruent trials suggests the emotional content of the material hindered

patients’ ability to reason when conflict occurred between belief and logic.

0.90 0.90

0.80 0.80

0.70 0.70

•OFC •OFC 0.60 0.60 —— Control Control i 0.50 PL 0.50

0.40 0.40 Neutral Neutral Emotional

Congruent Trials Incongruent Trials

Figure 5. b) Group’s accuracy rate on congruent trials as a function of content; b) Group’s accuracy rate on incongruent trials as a function of content.

In terms of the reaction time, there was a significant interaction [F(2, 44) =

4.558, p = 0.016] of Group by Content in the congruent trials. No significant

mean effect on Content [F( 1,44) = 0.613, p = 0.438, ns] or interaction effect [F(2,

44) = 0.080, p = 0.928, ns] was found in incongruent trials. Reaction Time fmsecl n incongruent functiontrialsa as of content. on Figure 6. Figure 21000 23000 17000 19000 25000 27000 29000 15000 others, in which case the effect of interest could be explained in terms of belief- of terms in explained be interestcould of effect the case which inothers, selectivelyimpairedin reasoning with otn a as nt infcn, (1 4) 337 p 07 A Fgr 7 below 7 Figure As 0.78 = p 3.317, = significant, not F( 42) also1, contentwas incongruent trials,emotional in rating believability the on Content and Group significant between interaction the than believable moreitems of category groupsone patientfound the of one Maybe material. emotional with do nothing to have may items neutral the and ocue htte eivblt rtn o h ocuin fte ruet cannot arguments conclusion believability ofthe the rating of the concludedthat in conclusion the of believability the perceived patients OFC the showed, Belief Belief Ratings nogun rassmlryt h P ptet (.. sm lp ad atr) We pattern), slope and same (i.e., patientsincongruent PL trialssimilarly the to subjects’ondata Our believabilityno ratings indicatedwas there that biaseffect. provideexplanationan for effect interest.theof a) Group’s reactionGroup’soncongruenta functiontime content; as of a) trialsreactiontime group's b) i psil ta te ifrne i promne ewe te emotional the between performance in differences the that possible is K the that conclude to us led analyses our summary, In Neutral Congruent Trials Congruent Role of Orbital Frontal Cortex on Emotional Reasoning Emotional on Cortex Frontal Orbital of Role Emotional F( , 2 = .0, = .9. h mi efc of effect main The 0.997. = p 0.003, = 42) 2, t P - -Control -OFC emotionally incongruent 15000 19000 21000 23000 25000 27000 29000 17000 eta | Emotional | Neutral Incongruent Trials Incongruent I syllogisms. F patients OFC are PL -P -Control -OFC 31

Role of Orbital Frontal Cortex on Emotional Reasoning 32

5.00

4.80 O) C 4.60 to VC OFC > 4.40 n CO 4.20 PL >

Incongruent Trials

Figure 7. Group’s believability rating on incongruent triats as a function of content

Emotional Ratings

Another possibility is that our effect of interest could have something to do with differences in emotional response to trials. As mentioned in the method section, we measured the participants’ perception of the emotional valence and emotional arousal of the emotional syllogisms by categorizing the emotional trials into different categories. However, to simplify the interpretation, we collapsed the two together and created a new variable “emotionality” as explained above.

Independent variable “emotionality” consisted of two levels, high and low emotional saliency. Dependent variable was the total number of trials that participants perceived as having low or high emotional saliency. We conducted a

3 (Group) X 2 (Emotionality) mixed ANOVA with covariate BDI only because there was no reason to believe that there was any correlation between working memory and the perception of the emotionality of content. The results (i.e.,

Figure 8) indicated there was no significant interaction between group and emotion of the content in the incongruent trials, F(2, 43) = 1.843, p = 0.171. No significant main effect of emotionality was found, F(1, 43) = 0.881, p = 0.350. Role of Orbital Frontal Cortex on Emotional Reasoning 33

* Control

high emotional saliency low emotional saliency

Incongruent trials

Figure 8. The total number of trials each group rated as a function of emotionality in emotional incongruent trials. Asymmetric Functionality of OFC

As explained above, the experimental OFC group in the present study

consisted of the patients with unilateral left and right lesion on OFC region. To

test whether the patients with lesion on the left and right OFC region responded

differently to the neutral and emotional syllogisms, we conducted a 3 by 2

between and within measure ANOVA, which included the variables Group (Left

OFC, right OFC, and Normal Control), and Content (Neutral and Emotional).

Figure 9 below indicated that the left and right OFC revealed a similar pattern

when reasoning about the neutral and emotional syllogisms, only the left OFC

group showed a more pronounced effect. Statistically, we found no significant

interaction between group (i.e., L-OFC vs. R-OFC) and content (i.e., neutral vs.

emotional), F(1, 13) = 2.337, p = 0.150, indicating the left OFC and right OFC

responded similarly to the neutral and emotional syllogisms . Additionally, the

simple f-tests revealed similar patterns when compared the left and right OFC with controls separately. Specifically, there were significant differences between Role of Orbital Frontal Cortex on Emotional Reasoning 34

the left OFC and controls (i.e., t (29) = -2.139, p = 0.041), and between the right

OFC and controls (i.e., t (28) = -2.679, p = 0.012) on emotional trials, whereas there was no significant differences between the left OFC and controls (i.e., t (29)

= 1.119, p = 0.272), and between the right OFC and controls (i.e., t (28) = -1.177, p = 0.249) on neutral trials.

0.85

0.8

0.75 L-OFC

0.7 u3 <( j PL 0.65

0.6 Neutral

Figure 9. The interaction between groups and content in accuracy

Discussion

The performance of our normal controls is consistent with that reported in the literature (e.g., Blanchette et al., 2007; Goel & Vartanian, 2010). They performed well in the neutral condition and improved slightly in the emotional condition. The crucial finding of our study is that patients with lesions in focal orbital frontal cortex are impaired in reasoning about emotional materials, but not in reasoning about neutral material. In the neutral condition, the OFC patients performed the same as normal controls. However patients’ performance dropped significantly with the introduction of emotional saliency. Our finding has replicated Goel and Dolan’s (2003a) study and provided evidence for the role of Role of Orbital Frontal Cortex on Emotional Reasoning 35

OFC in emotional reasoning. In particular, our results consolidated their finding by demonstrating the necessity of OFC for reasoning with emotional material.

Consistent with this role, the OFC has been implicated in a series of affective processing including the affective ToM reasoning (e.g., Shamay-Tsoory et al.,

2006), mentalizing (e.g., Shamay-Tsoory & Aharon-Peretz, 2007), emotional perspective-taking (e.g., Hynes et al., 2006), moral reasoning/decision making

(e.g., Borg et al., 2006; Greene et al., 2000, 2001, 2004; Harenski & Hamann,

2006; Oliveria-Souza & Moll, 2000), and decision making (e.g., Bar-On et al.,

2003; Bechara et al, 1997; Houde et al.., 2000). Additionally, we found that the effect was being driven by the particularly poor performance in the incongruent trials. This finding is in accordance with a study that reported activation in

VMPFC was found only when logical response was overcome by belief bias in the incongruent trials (i.e., when participants responded on the basis of personal

beliefs rather than the logic of the situation)(Goel & Dolan, 2003a).

Given that the statistical results we reported used WM and BDI as covariates, the impairment of these OFC patients on reasoning about emotional

materials cannot be explained in terms of these variables. No other group

differences were found in other variables, such as IQ score, year of education, volume loss etc. Additionally, we know from the reasoning literature that

variables, such as negation and congruency, can have an impact on reasoning

task performance. To account for this, 1) the negation was counterbalanced in

our experimental design (i.e., 10 out of 19 conclusions on neutral materials Role of Orbital Frontal Cortex on Emotional Reasoning 36

contained negation vs 9 out of 20 conclusions on emotional materials contained negation), and 2) the unequal number of validity in congruent and incongruent trials was addressed by weighting the data accordingly. We can confidently discount these variables in contributing to our effect of interest and conclude the impairment on emotional reasoning is as a function of lesion on OFC region.

What are the Possible Factors Driving our Effect of Interest?

Our analyses led us to conclude that the OFC patients are selectively impaired in reasoning with emotionally incongruent syllogisms. The imaging and patient studies and reviews aforementioned so far only provided evidence that the medial regions of OFC are playing a role in emotional processing. However, we still do not understand why the OFC patients were having difficulty in reasoning only about emotional, incongruent syllogisms.

Several possible explanations addressing this question are explored below. One possibility for the differences in performance between the emotional and the neutral (items) may have nothing to do with emotion. Maybe one of the patient groups found one category of items more believable than the others, in which case the effect of interest could be explained in terms of belief-bias effect.

To account for the effect of belief-bias, we asked our participants to rate the believability of each of the conclusion. We found no significant main effect of content and no significant interaction between the groups and the content in participants’ believability rating. Given that 1) all participants tended to find the Role of Orbital Frontal Cortex on Emotional Reasoning 37

neutral incongruent trials to be more believable than the emotional incongruent

trials and, 2) the OFC patients perceived the believability of the conclusion in

incongruent trials similarly to the PL patients (i.e., same slope and pattern, refer

to Figure 7), the believability rating of the conclusion of the arguments cannot

provide an explanation on the effect of interest.

Another reasonable possibility is that our effect of interest could have

something to do with emotion, for example, the perception of the emotionality of

the syllogisms. The results indicated there was no significant interaction between

the group and judgments of emotionality of the content in the incongruent trials.

No significant main effect of emotionality or group difference was found. In other words, participants’ perception of the emotionality of the syllogisms did not

contribute to the our effect of interest.

Why are the OFC Patients Having Difficulty when Reasoning about the Emotional

Incongruent Syllogisms?

There are four key findings: 1) only the OFC patients were impaired when

reasoning about the emotional materials; 2) it was only the incongruent trials; 3)

there was no difference in perceiving the emotionality of the content among the

groups; and 4) no difference was found on the believability of the conclusions.

As discussed before, finding #3 and #4 eliminated belief and emotionality of the

content as the possible factors driven our effect of interest. What about finding

#2? To get the incongruent trials correct, we have to 1) recognize there is a Role of Orbital Frontal Cortex on Emotional Reasoning 38

conflict between belief and logic; 2) inhibit a prepotent response associated with

belief-bias; and 3) engage a formal reasoning process to correctly complete a

logical task. The fact that OFC patients perform well in neutral materials

suggested that the impairment in emotional materials could not be explained simply by the deficit on the conflict detection system, but could be explained in terms of the presence of the emotional saliency of the syllogisms. One possible

interpretation is that when the material is emotionally charged, the presence of

emotion disrupts the optimal condition for logical reasoning. As some studies we

discussed above (e.g., Blanchette, 2007; Channon & Baker, 1995) suggested

emotion or affective state could hinder the reasoning ability and the optimal condition for logical reasoning when the content is neutral. In case of OFC

patients, the emotion of the material may not get abstracted from the content or

processed before passing on to the reasoning processes. In other words, our finding suggests that emotion needs to be abstracted or processed from the

materials and this abstraction needs to occur in the medial region of PFC before

passing on to the reasoning processes.

The Limitations

There are several limitations in the present study. Firstly, our results only

demonstrated OFC lesion selectively impaired reasoning with emotional material.

Many studies have proposed a dissociable functionality between the OFC and

the lateral PFC, it would be fruitful to introduce patients with lesions on lateral

OFC regions into the present study and examine whether there would be a Role of Orbital Frontal Cortex on Emotional Reasoning 39

double dissociation between the medial and lateral OFC on neutral and emotional materials. We were unable to include these patients into our present due to the insufficient numbers available for study. Secondly, our emotional saliency was

manipulated by the content of syllogisms. It would be interesting to see whether there would be any difference in results if we induced the emotional states of

patients with pictorial or auditory stimuli. Thirdly, participants were asked to categorize the emotionality of the emotional syllogisms based on valence and

arousal. It would be more helpful and simpler if the rating was a numeric scale.

Conclusion

The findings on our initial analyses were consistent with the imaging study

conducted by Goel & Dolan (2003a). It supports the claim that the medial PFC is

necessary in reasoning about emotional materials. The crucial finding in the

present study was that the OFC patients were selectively impaired in reasoning

about emotional incongruent material. In other words, in the absence of

emotional material, the OFC patients were able to detect the conflict between the

belief and the logic, suppress the belief and switch back to the reasoning mode when reasoning about the incongruent trials. However, in the presence of

emotional material, this conflict mechanism seemed to be interrupted. The fact

that they were reasoning well on the neutral items suggested that this conflict

mechanism remained intact in these patients. Our finding suggests that emotion

needs to be abstracted or processed from the materials and this abstraction

needs to occur in the medial region of PFC before passing on to the logical Role of Orbital Frontal Cortex on Emotional Reasoning 40

reasoning processes. Our results are also consistent with neuroanatomical evidence that “the VMPFC receives projections from the amygdala and medial temporal and thalamic structures and in turn is robustly interconnected to the lateral prefrontal cortex [Barbas, 2000]” (Goel & Dolan, 2003b, p2320). We provide evidence for a dynamic neural system for reasoning, the configuration of which is strongly influenced by emotional saliency (Goel, 2007; Goel & Dolan,

2003). Role of Orbital Frontal Cortex on Emotional Reasoning 41

References

Adolphs, R. (1999). Social cognition and the human brain. Trends in Cognitive Sciences. 3(12), 469 - 579.

Badcock, P. B. T., & Allen, N. B. (2003). Adaptive social reasoning in depressed mood and depressive vulnerability. Cognition and Emotion, 17(4), 647- 670.

Bar-On, R., Tranel, D., Denburg, N. L., & Bechara, A. (2003). Exploring the neurological substrate of emotional and social intelligence. Brain, 126, 1790-1800.

Bechara, A., Damasio, H., & Damasio, A. R. (2000). Emotion, Decision Making and the Orbitofrontal Cortex. Cerebral Cortex, 10, 295-307.

Beck, A. T., Steer, R. A., & Brwon, G. K. (1998). Manual for the Beck Depression Inventory II. San Antonio, TX: Psychological Corporation.

Blanchette, I. (2006). The effect of emotion on interpretation and logic in a conditional reasoning task. Memory and Cognition, 34(5), 1112-1125.

Blanchette, I., & Richards, A., (2004). Reasoning About Emotional and Neutral Materials: Is Logic Affected by Emotion. Psychology Science, 15(11), 745- 752.

Blanchette, I., Melnyk, L., Richards, A., & Lavda. A. (2007). Reasoning About Emotional Content Following Shocking Terrorist Attack: A Tale of Three Cities. Journal of Experimental Psychology: Applied, 13(1), 47-56.

Borg, J.S., Hynes, C., Van Horn. J., Grafton, S., & Sinnott-Armstrong (2006). Consequences, action, and intention as factors in moral judgments: an fMRI investigation. Journal of Cognitive Neuroscience, 18, 803-817.

Bruent-Gouet, E. & Decety, J. (2006). Social brain dysfunctions in schizophrenia: A review of neuroimaging studes. Psychiatry Research Neuroimaging, 148, 75-92.

Bush, G., Luu, P., & Posner, M. I. (2000). Cognitive and emotional influences in anterior cingulated cortex. Trends Cognitive Science, 215-222 5,

Canessa, N., Gorini, A., Cappa, S. F., Piattelli-Palmerini, M., Danna, M., Fazio, F., & Perani, D. (2005). Human Brain Mapping, 26, 30-43.

Chang, A. & Wilson, M. (2004). Recalling emotional experiences affects performance on reasoning problems. Evolution and Human Behavior, 25, 276-276. Role of Orbital Frontal Cortex on Emotional Reasoning 42

Channon, S. (2004). Frontal lobe dysfunction and everyday problem-solving: Social and non-Social contributions. Acta Psychologies, 115, 235-254.

Clark, L., Manes, F., Antoun, N., Sahakian, B. J. & Robbins, T.W. (2003). The contribution of lesion laterality and lesion volumes to decision-making impairment followed frontal lobe damage. Neuropychologia, 41, 1474- 1483.

Crichley, H., Elliott, R., Mathias, C. J. & Dolan, R. (2000). Neural activity relating to generation and representation of SCR in functional magnetic resonance imaging. Journal of Neuroscience, 20, 2033-2040.

Damasio, A. (1994). Descartes’ error. New York: Harcourt.

Davidson, R. J. (1992). Emotion and affective style: Hemispheric substrates. American Psychological Society, 3(1), 39-43. de Jong, P., Weertman, A., Horselenberg, R. & van den Hout, M. A. (1997). Deductive Reasoning and Pathological Anxiety: Evidence for a Relatively Strong “Belief Bias" in Phobic Subjects. Cognitive Therapy and Research, 21(6). 647-662.

Decety, J., Michalska, K. J., & Kinzler, K. D. (2011). The developmental Neuroscience of Moral Sensitivity. Emotion Review, 3(3), 305-307.

Drevets, W. C., & Raichle, M. E. (1998). Reciprocal suppression of regional cerebral blood flow during emotional versus higher cognitive processes: implications for interactions between cognition and emotion. Cognition and Emotion, 12, 353-385.

Duncan, S., & Barrett, L. F. (2007). Affect is a form of cognition: A neurobiological analysis. Cognition and Emotion, 21(6), 1184-1211.

First, M.B., Spitzer, R. L., Gibbon, M., & William, J. B. (1996). Structural Clinical Interview For DSM-IV Axis I Disorders: Non-patient Edition (DCID-1/NP). New York: New York State Psychiatric Institute.

Evans, J. St. B. T. (2003). In two minds: dual-process accounts of reasoning. Trends in Cognitive Sciences, 7(10), 454-459.

Frogas, J. P. (1995). Mood and Judgment: The affect infusion model (AIM). Psychological Bulletin, 117, 39-66.

Gilbert, S. J., Spengler, S., Simons, J. S., Steele, J.D., Lawrie, S. M., Frith, C. D. & Burgess, P. W. (2006). Functional specialization with rostral prefrontal cortex (Area 10): A meta-analysis. Journal of Cognitive Neuroscience, 18(6), 932-948. Role of Orbital Frontal Cortex on Emotional Reasoning 43

Goel, V. (2007). Anatomy of deductive reasoning. Trends in Cognitive Sciences, 11(10), 435-442.

Goel, V. (2008). Pedagogy revealed through functional anatomy. Trends in Cognitive Sciences, 12(5), 174

Goel, V., & Dolan, R.J. (2003a). Explaining modulation of reasoning by belief. Cognition 87(1), B11-22.

Goel, V., & Dolan, R. J. (2003b), Reciprocal neural response within lateral and ventral medial prefrontal cortex during hot and cold reasoning. Neurolmaing 20, 2314-2321.

Goel, V., Shuren, J., Sheesley, L.& Grafman, J. (2004). Asymmetrical involvment of frontal lobes in social reasoning. Brain, 127, 783-790.

Goel, V., & Vartanian, O. (2010). Negative emotional can attenuate the influence of belief on logical reasoning. Cognition and Emotion, in press.

Greene, J.D., Nystrom, L.E., Engell, A.D., Darley, J.M. & Cohen, J.D. (2004). The neural bases of cognitive conflict and control in moral judgment. Neuron, 44, 389-400,

Greene, J.D., Sommerville, R.B., Nystrom, L.E., Darley, J.M. & Cohen, J.D. (2001). An fMRI investigation of emotional engagment in moral judgment. Science, 293, 2105-2108.

Harris, S., Sheth, S. A., & Cohen, M. S. (2008). Functional Neuroimaing of Belief, Disbelief, and Uncertainty. Annals of Neurology, 63(2), 141-147.

Houde, O. (2008). Pedagogy, not (only) anatomy of reasoning. Trends in Cognitive Sciences, 12(5), 173-174.

Houde, O. (2007) First insights on “neuropedagogy of reasoning”. Thinking and Reasoning. 13(2), 81-89.

Houde, O., Zago, L., Crivello, F., Moutier, S., Pineau, A., Mazoyer, B., and Tzourio-Mazoyer. (2001). Access to Deductive Logic Depends on a Right Ventromedial Prefrontal Area Devoted to Emotion and Feeling: Evdience from a Training Paradigm^Neurolmaing 14, 1486-1492.

Hynes, C. A., Baird., A. A., Grafton, S. T. (2006). Differential role of the orbital frontal lobe in emotional versus cognitive perspective-taking. Neuropsychologia, 44, 374-383.

Melton, R. J. (1995). The role of positive affect in syllogism performance. Personality and Social Psychological Bulletin 788-794.21, Role of Orbital Frontal Cortex on Emotional Reasoning 44

Mesulam, M. M. (1990). Large-scale neurocognitive networks and distributed processing for attention, language and memory. Annals of Neurology, 28, 597-613.

Mitchell, J. P., Banaji, M. R-, & Macrae, C. N, (2005). The link between social cognition and self-referential thought in the meidal prefrontal cortex. Journal of Cognitive Neuroscience, 17, 1306-1315.

Moghanddam, B., & Homayoun, H. (2008). Divergent plasticity of prefrontal cortex networks. Neuropsychophamacology Review, 33,42-55.

Moll.J., Oliveria-Souza, R., Bramati, I.E., Grafman, J. (2002). Functional metworks in emotional moral and nonmoral social judgments. Neuroimage, 16, 969-703.

Moll, J., Oliveria-Souza, R., Moll, F.T. (2005). The moral affiliations of disgust-A functional fMRI study. Cognitive and Behavioural Neurology, 18, 68-78.

Moretto, G., Ladavas, E., Mattioli, F., & di Pellegrino, G. A Psychophysiological Investigation of Moral Judgment after Ventromedial Prefrontal Damage. Journal of Congitive Neuroscience, 22(8), 1888-1899,

Muris, P., Rassin, E., Mayer, B., Smeets, G., Huijding, J., Remmerswaal, D., & Field, A. (2009). Effect of Verbal Information on Fear-related Reasoning Biases in Children. Behavioral Research and Therapy 47, 206-214.

Oaksford, M., Grainger, B., Morris, F., & William, J. M. G. (1996). Mood, Reasoning, and Central Executive Processes. Journal of Experimental Psychology: Learning, Memory, and Cognition. 22(2), 476-492.

Ochsner, K. N., Knierim, K., Ludlow, D. H., Hanelin, J., Ramachandran, T., Glover, G., et al. (2004). Reflecting upon feelings: An fMRI study of neural systems supporting attribution of emotion of self and others. Journal Cognitive Neuroscience, 16, 1746-1772.

Oliveria-Souza, R., Moll, J. (2000). The moral brain: functional MRI correlates of moral judgement in normal adults. Neurology, 54, 252.

Osman, M. (2004). An evaluation of dual-process theories of reasoning. Psychonomic Bulletin & Review, 11(6), 988-1010.

Pelissier, M. C., & O’Connor, K. P. (2002). Deductive and inductive reasoning in obsessive-compulsive disorder. British Journal of Clinical Psychology, 41, 15-27.

Pham. M. T. (2007). Emotion and Rationality: A Critical Review and Interpretation of Empirical Evidence. Review of General Psychology, 11(2), 155-178. Role of Orbital Frontal Cortex on Emotional Reasoning 45

Phan, K. L., Wager, D., Taylor, S. F., & Liberzon, I. (2004). Functional Neuroimaging studies of human emotions. CNS Spectrums, 9(4), 258-266.

Phillips, M.L., Drevets, W.C., Rauch, S.L., & Lane, R. (2003). Neurobiology of emotion perception II: implications for major psychiatric disorders, Society of Biological Psychiatry, 54, 515-528.

Prado, J., Chadha, A., & Booth, J. R. (2011) The Brain Network for Deductive Reasoning: A Quantitative Meta-analysis of 28 Neuroimaging Studies. Journal of Cognitive Neuroscience, 23(11), 3483-3497.

Raine, A., & Yang, Y. (2006). Neural foundations to moral reasoning and antisocial behavior. SCAN, 1, 203-213.

Ramnani, N., & Owen, A. M. (2004). Anterior prefrontal cortex: insights into function from anatomy and neuroimaging. Nature Reviews Neuroscience, 5(3), 184-194.

Saxe, R., Carey. S., & Kanwisher, N. (2004). Understanding Other Minds: Linking Developmental Psychology and Functional Neuroimaging. Annual Reivew Psychology, 55, 87-124.

Shamay-Tsoory, S. G., & Aharon-Peretz, J. (2007). Dissociable prefrontal networks for cognitive and affective theory of mind: A lesion study. Neuropsychologia, 45, 3054-3067.

Shamay-Tsoory, S. G., Tibi-Elhanany, Y., & Aharon-Peretz, J. (2006). The ventromedial prefrontal cortex is involved in understanding affective but not cognitive theory of mind stories. Social Neuroscience, 1(3-4), 149-166.

Simpson, J., Cove, J., Fineberg, N., Msetfi., & Ball, L. J. (2007). Reasoning in people with obsessive-compulsive disorder. British Journal of Clinical Psychology, 46, 397-411.

Stone, V. E., Baron-Cohen, S., & Knight, R. T. (1998). Frontal lobe contributions of theory of mind. Journal of Cognitive Neurosciences, 640-656.10,

Wechsler, D. (1997). Wechsler Adult Intelligence Scale - Third Edition: WAIS-III. San Antonio, TS: The Psychological Corporation.

Wechsler. D. A. (1997b). Wechsler Memory Scale - Third Edition. San Antonio, TX: The Psychological Corporation.

Wood, J. N., & Grafman, J. (2003). Human prefrontal cortex: processing and representational perspectives. 4 (2), 139-147. Role of Orbital Frontal Cortex on Emotional Reasoning 46

Appendix A - List of syllogisms

Neutral items: All bikes are red. Some bikes are broken. No broken bikes are red. Some felines are panthers. All felines are quadrupeds. No quadrupeds are panthers. All fruits are pears. All bananas are fruit. No bananas are pears. No skiers are smokers. Some men are not skiers. All men are smokers. No liquids are red. All paints are liquids. Some paints are red. No men are children. Some men are girls. All girls are children. No coffee contains nicotine. No nicotine is found in Tea. No Tea contains coffee. Some Italian are not Martians. No French are Italians. Some French are Martians. No Olympic runners are smokers. Some smokers are not men. Some men are Olympic runners. Some mice are not rabbits. Some cats are not mice. Some cats are not rabbits. No Cuban cigars are dogs. No Cuban cigars are cats. No cats are dogs. No fruit are blue. Some apples are fruit. All apples are blue. All gods are immortal. No immortal beings are men. No men are gods. Some apples are sweet fruit. All sweet fruit are grapes. Some grapes are apples. Some dogs do not have ears. All dogs are Germen Shepherds. Some German Shepherds do not have ears. All cars have four wheels. No scooters have four wheels. No scooters are cars. No cats have strips. Some tigers are cats. Some tigers do not have strips. All airplanes cal fly. Some boats cannot fly. Some boats are not airplanes. No poisons are sold at the grocers. Some mushrooms are sold at the grocers. Some mushrooms are not poisonous. Some felines have gills. All felines are cats. Some cats have gills.

Emotional items: All skyscrapers are at risk of terrorism. No big cities have skyscrapers. No big cities are at risk of terrorism. All stupid people are Republicans. Some stupid people are Democrats. No Democrats are Republicans. No Arabs bleed when they are bombed by Israel. All Palestinians are Arabs. Some Palestinians bleed when they are bombed by Israel. All Americans read the Bible. Some Americans are homosexuals. All homosexual read the Bible. All Americans are evil. Some serials killers are Americans. All serials killers are evil. Some poodles are good to eat. All poodles are dogs. All dogs are good to eat. No wars are terrorist acts. Some terrorist acts are not good for society. Some things good for society are wars. No wars are justified. No wars involve raping of women. Some raping of women is justified. No negroes are Whiles. No Whites are slaves. No slaves are negroes. Some saints are not prostitutes. No Arab women are prostitutes. Some Arab women are prostitutes. Role of Orbital Frontal Cortex on Emotional Reasoning 47

Some priests are not pedophiles. No Arab women are saints. Some Arab women are prostitutes. Some women are liers. No American Presidents are women. Some American Presidents are liers. All decent girls are Christian. No lesbians are Christian. No lesbians are decent girls. All Americans are brave people. No brave people are Vietnam Veterans. No Vietnam Veterans are American. No little girls die of Aids. Some children are little girls. Some children do not die of Aids. Some terrorists are Iraqis. All Iraqis are Arabs. Some Arabs are terrorists. Some animals eat children. All animals are pets. Some pets eat children. All thieves are Chinese. Some women are not Chinese. Some women are not thieves. No killers are of innocent people are American. Some Al-Queda bombers are Americans. Some Al-Queda bombers are killers of innocent people. Some Mexicans are dirty. All Mexicans are immigrants. Some immigrants are dirty.