Draft for SYDNEY Conference

Social Neuroscience - 1

Affective Influences on Social Cognition and Behavior:

A Social Neuroscience Perspective

Piotr Winkielman

University of California, San Diego

John T. Cacioppo

University of Chicago

Running head: Social Neuroscience

Chapter to appear in Forgas, J.P. (Eds.). Hearts and minds: Affective influences on social thinking and behavior. Philadelphia, PA.: Psychology Press.

Correspondence should be addressed to Piotr Winkielman, Department of Psychology,

University of California, San Diego, 9500 Gilman Drive, La Jolla, CA 92093-0109, e-mail: [email protected], fax: (858) 534-7190., or to John T. Cacioppo, Center for Cognitive and

Social Neuroscience, University of Chicago, 5848 S. University Avenue, Chicago, IL 60637, email: [email protected], fax: (773) 702-4580. We thank Joe Forgas, and Jenny Truillo.

Preparation of this chapter was supported by the National Science Foundation grant BCS-

0350687 and the National Institute on Mental Health grant P50 MH72850. Social Neuroscience - 2

Overview

Psychological research on mechanisms underlying affect and social cognition goes back several decades, and has generated a rich and exciting theoretical and empirical literature, as illustrated by other chapters in this book. More recently, our understanding of these mechanisms been enriched by advances in social neuroscience (e.g., Cacioppo, Berntson, Adolphs et al.,

2000; Harmon-Jones & Winkielman, in press). A premise underlying work in social, as well as affective and cognitive neuroscience is that our understanding of information processing mechanisms can be informed by studying the operation of the central nervous system (brain) and the peripheral nervous system (body).1 Consequently, social neuroscientists study how stimulation or lesion of a circumscribed nervous circuit influences a specific mental function and how performing a specific mental function influences activity of a circumscribed nervous circuit.

In neuroscience, just like in psychology, there are often theoretical disputes regarding what precisely constitutes a system responsible for a function. However, there is general agreement regarding several broad domains of processing that can be distinguished from one another. Besides the traditional domain of cognitive neuroscience, object knowledge, the two intensely investigated domains include affect and social cognition. In our chapter, we review some of what we know about nervous circuits underlying affect and social cognition and illustrate conceptual advances that psychologists can obtain from considering the neuroscience

1 Until recently, most models in social psychology followed the traditional computer metaphor, which assumes that the software of the mind is independent of the hardware of the body and the brain (Block, 1995; Dennett, 1969). Thus, cognitive operations are arbitrarily related to their physical instantiations, so that any sufficiently complex physical system could have human intelligence. In principle, the software that constitutes the mind (including the "social mind”) could run on anything -- neurons, silicon, or even wooden gears -- as long as the elements were arranged in proper functional relations. Research in cognitive and social neuroscience has led to a growing appreciation that most phenomena are best understood by jointly considering neural and psychological constraints (e.g., Kosslyn, 1994; Winkielman, Berntson, & Cacioppo, 2001). Social Neuroscience - 3 perspective. Our chapter is structured as follows. First, we place the biological organization of the brain in the evolutionary context, emphasizing how neural systems represent affective processes across multiple-levels of organization. Second, we review the particular roles of major subcortical and cortical structures in elicitation, experience, and affect regulation. Third, we explore the implications of these data for the question of conscious and unconscious affective influences. Fourth, we explore the implication of brain organization for the relationship between affective and social processing. Finally, we close with some open questions and a few opinions about exciting directions for future research.

1. Evolution and multi-level organization of affect throughout the brain.

To appreciate the biological underpinnings of affective influences on social behavior, it is worth noting that millions of years of evolution has resulted in a heterarchical structure of the brain, with networks that process affect at multiple levels of neural organization (Jackson,

1884/1958; Berntson & Cacioppo, in press). Thus, the most primitive protective responses to immediate nocicetive and aversive stimuli are organized at the level of the spinal cord. This is demonstrated by the fact that withdrawal reflexes to noxious (e.g., pain) stimuli can be seen even after spinal transsections. Those spinal mechanisms could possibly be as old as simple vertebrates, which emerged over 500 million years ago (mya). The primitive protective reactions are expanded at higher levels of the nervous system. Thus, the networks of the brain stem and limbic system endow organisms with an expanded behavioral repertoire, including basic pleasure/displeasure reactions, escape reactions, aggressive responses, and even a rudimentary ability to anticipate and avoid aversive encounters. In fact, reptiles, which emerged over 300 mya, already have networks responsible for specific affective behaviors, such as aggression, fear, play, mating (Allman, Panksepp;). Although those networks have been expanded upon and Social Neuroscience - 4 modified in mammals, there are remarkable similarities between fish, reptiles, birds, and mammals in both affective neurochemistry and neuroanatomy (Goodson & Bass, 2001;

Martinez-Garcia, Martinez-Marcos, & Lanuza, 2002). The emergence of primates (about 60 millions years ago) and particularly hominids (10 millions years ago, or the last 0.2 % of the evolutionary history of vertebrates) is, of course, associated with rapid encephalization, or the growth of the neocortical mantle. Our own species, which emerged only about 100,000 mya, has a particularly large neocortex (particularly prefrontal white matter) even compared to other advanced mammals (Dorus et al., 2004; Schoenemann, Sheehan, & Glotzer, 2005). Presumably, this neural hardware endows us with the ability for symbolic representation, transformations and computations, rapid learning, language, complex social interaction, as well as a rich sense of self-awareness (Dunbar, 2003).

No doubt, much of the emotional and social life of humans is “cortical.” This is evident in the profound impact of cortical damage in humans. A rat can lose its entire neocortex and continue to live a remarkably normal life (Berridge, 2003), whereas even seemingly mild damage to the neocortex in humans can result in significant affective, cognitive, and behavioral changes (National Institutes of Health Consensus Statement, 1998). Nevertheless, the biological underpinnings of affective influences on social behavior are best understood as reflecting a multiplicity of older and newer mechanisms, which are not localized to a single neural level, but are represented and operate together across levels of the nervous system. At progressively higher levels of organization, there is a general expansion in the range and complexity of contextual controls and in the breadth and flexibility of responses (Berntson et al., 1993).

However, as Berntson and colleagues have shown, though the higher level systems certainly confer greater flexibility, they do not eliminate lower behavioral mechanisms (e.g., Berntson et Social Neuroscience - 5 al., 1998; Berntson & Cacioppo, in press). Furthermore, even though evolutionary forces have rigidly canalized some aspects of behavior, these forces also forged many interacting neural systems. For these reasons, any explanation that restricts its focus to only one system or level is necessarily incomplete (e.g., explanations that focus entirely on the “low” route or on the evolutionarily oldest mechanisms). This is also the case for explanations that posit the operation of some limited number of sharply different systems (e.g., the currently popular “two-system” explanations). After all, as we will discuss later, there are few sharp “cuts” between the levels of mechanisms and there is great amount of interactivity in processing (we return to this point later).

In the forthcoming sections, we will focus more specifically on what research reveals about the contribution of various subcortical and cortical structures to affective processing. The approximate locations of the most important structures we discuss are indicated in Figure 1. We also wish to note that our presentation here is simplified and does not capture their complex neuroanatomy and neurochemistry and several additional role these structures play in affect and cognition (for more info see Adolphs 1999, Berridge, 2003; Ochsner and Barrett, XXXX).

2) Subcortical and cortical networks underlying affective reactions and experience.

Affective influences on judgment and behavior encompass a wide spectrum of phenomena and mechanisms. At the bottom end of the spectrum, affective influence may involve automatic modulation of perception, attention, and memory (Bower & Forgas, ;

Cacioppo & Gardner, 1999; Lang; Niedenthal & Kitayama, ). At the top end of the spectrum, affective influence may involve complex inferences from conscious feelings and strategic attempts at mood regulation (Erber; Baumeister; Schwarz & Clore, 19XX). Recent work in affective neuroscience has identified some critical structures and pathways underlying these Social Neuroscience - 6 various types of affective influence. Below we review some illustrative findings. For convenience and clarity, we organize our presentation by the critical brain structures, though as mentioned earlier, the underlying mechanisms typically involve multiple networks instantiated across multiple structures.

Brain stem. Many psychologists think of the brain stem as merely a reflexive structure – perhaps controlling slightly more complex reactions than the spinal cord. However, the brainstem is critically involved in multiple affective phenomena, including elicitation of basic facial expressions, reactions to pleasurable and painful stimuli and affective modulation of memory.

A particularly poignant demonstration of brainstem’s role in basic affective reactions is offered by a cruel experiment of nature. As a result of a birth defect, some infants have a congenitally malformed brain, possessing only a brainstem, but no cortex and little else of the forebrain (i.e., no amygdala, nucleus accumbens, etc). Yet, in these anencephalic infants (as well as decorticated rats), sweet taste of sugar still elicits facial expressions that resemble normal

‘liking’ reactions, such as lip sucking and smiles, whereas bitter tastes elicit facial expressions that resemble “disliking” reactions, such as mouth gapes or nose wrinkling (Steiner, 1973). This finding is consistent with observations that positive facial expressions to sweetness are emitted by chimpanzees, orangutans, and gorillas, various monkeys, and even rats (Berridge, 2000;

Steiner et al., 2001). The pattern of positive facial expression becomes less and less similar to humans as the taxonomic distance increases between a species and us. But all of these species share some reaction components that are homologous to ours, suggesting common evolutionary ancestry and a similar neural mechanism that might be anchored in the brain stem.

The brainstem is also critically involved in processing of hedonic value of basic sensory Social Neuroscience - 7 stimuli. For example, the brainstem’s parabrachial nucleus (PBN) receives ascending signals from many sensory modalities, including taste sensations from the tongue.2 Not surprisingly,

PBN plays a role in generating positive responses to tasty foods. Thus, when a rat’s PBN is tweaked by microinjections that activate its benzodiazepine/GABA receptors, the rat produces greater ‘liking’ reactions to sugar, such as tongue protrusions and lip licking (Berridge & Pecina,

1995). In the domain of negative affect, brainstem’s periaqueductal gray (PAG) modulates human and animal responses to pain (Willis & Westlund, 1997).

Finally, the brainstem is critically involved in memory-potentiating effects of emotional activation (Berntson, Sarter, & Cacioppo, 19XX). Specifically, it is well-known that under many conditions emotion enhances memory of important events (McGough, 2003). This effect is at least partially attributable to the impact that viscera have on the brainstem’s nucleus of the solitary tract (NTS). Specifically, during emotional activation, the adrenal medulla releases the hormone epinephrine into the bloodstream causing the well-known "fight-or-flight" response in the viscera (heart, lungs, stomach, etc). This visceral response activates the ascending fibers of the vagus nerve, which stimulate the NTS. In turn, the NTS neurons, via their ascending projections, cause the release of the neurotransmitter norepinephrine into to the amygdala and hippocampus, enhancing encoding of memory (Hassert, Miyashita, & Williams, 2004).

Amygdala

The amygdala consists of a pair of almond-shaped structures located in the medial temporal lobe, just anterior to the hippocampus. The amygdala is richly and reciprocally connected to a variety of cortical areas involved in cognitive and affective processing, as well as subcortical structures involved in physiological regulation (sympathetic and parasympathetic

2 Some have suggested that in humans the PBN participates in generating the ‘protoself’, an unconscious but coherent representation of the momentary state of the body (Damasio, 1999). Social Neuroscience - 8 regulation of cardiovascular activity, respiration, hormone levels, muscular responses, etc).

Accordingly, the amygdala is involved in several interesting phenomena, including generation of rapid responses to affectively-tagged stimuli, affective modulation of perception and memory as well as affect regulation. We’ll discuss these phenomena now, but will return to amygdala’s involvement in other aspects of social cognition later.

Animal and human studies suggest that amygdala receives sensory input via a variety of pathways, including a slow ventral cortical pathway and a faster, more direct pathway from the thalamus (LeDoux, 1996). Presumably, this direct pathway allows amygdala to quickly respond to rudimentary features of survival-relevant stimuli, including highly blurred fear faces

(Vuilleumier, Armony, Driver, & Dolan, 2003) or even sclera (whites) of eyes (Whalen et al.,

2005). Interestingly, amygdala response can be triggered even without conscious stimulus recognition. Thus, amygdala activates to subliminally presented expressions of fear (Whalen et al., 1998) or previously pre-conditioned expressions of anger (Morris), presumably via a direct pathway from the visual thalamus (Morris, Öhman, & Dolan, 1999). Amygdala can also be activated with anger expressions that are presented under conditions of binocular suppression

(Williams et al., 2004) or are shown to a blindsight patient (DeGelder,xxx). Of course, these demonstration do not imply that the direct or “low” route is the exclusive or even a primary source of amygdala effects on perception and behavior, only that the amygdala has multiple connections, including those specified by the notion of the “low route” (Adolphs; Clore).

The amygdala not only receives input from the sensory areas but is also reciprocally connected to them, allowing for affective modification of perception, attention, and memory.

For example, patients with damage to the amygdala do not show the typical reduction of attentional blink to emotionally-charged stimuli (Phelps et al., 1999). Earlier, we have already Social Neuroscience - 9 mentioned that amygdala plays a critical role in the phenomenon of emotionally-enhanced memory (Cahil, 19XX). Amygdala is also involved in the most basic form of affective learning

– acquisition of conditioned fear responses. The now classic studies demonstrated that patients with congenital and acquired amygdala damage, yet intact hippocampus, show impairments in acquisition of conditioned fear responses, as measured by skin conductance, while showing relatively unimpaired declarative memory (Bechara et al., 1995; Phelps).

The amygdala is also connected to the higher cortical areas, including the prefrontal cortex, involved in symbolic processes and executive functions. This connectivity plays a role in downstream induction and regulation of affect. Thus, a verbal induction of fear (e.g., “you will receive a shock upon seeing a blue slide”) leads to amygdala activation and physiological arousal response, an effect that is reduced in amygdala-damaged patients (Phelps, ). In normal participants, the amygdala response to affectively-charged pictures can be modulated instructions emphasizing affect regulation (Ochsner & Gross).

Finally, it is important to emphasize that patients with damage to the amygdala show little, if any, impairment in their subjective experience of emotion, at least as measured by the magnitude and frequency of self-reported positive or negative affect (Anderson & Phelps, 2002).

This suggests a relative independence of the amygdala from the mechanisms underlying generation of conscious feelings, which, as we discuss shortly, are more associated with cortical mechanisms.

Nucleus accumbens and related structures

Near the bottom of the front of the brain, in the area called the basal forebrain, lie several nuclei rich in dopamine and opioid neurotransmitters. One of those nuclei, the nucleus accumbens, sometimes referred to as the ventral striatum, is famous for its association with Social Neuroscience - 10 reward. In fact, many affective neuroscientists view activation of dopamine projections to the accumbens and related targets as a neural “common currency” for reward. Presumably, this common coding of qualitatively different rewards allows the brain to represent a variety of different pleasures on a similar hedonic metric (Cabanac, 1992). There is actually evidence that accumbens reflect not “pleasure”, or “liking” of the stimulus, but rather an incentive salience, or

“wanting” of the stimulus (Berridge & Robinson, 1998). However, for our purposes here it is only important to highlight the role of accumbens in modulation of positive affective reactions to a variety of simple and complex social and non-social stimuli. For example, brain microinjections of drug droplets that activate opioid receptors in nucleus accumbens cause increased ‘liking’ for sweetness in rats (Pecina & Berridge, 2000). In fMRI studies on humans, accumbens and related areas activate not only to drug cues, but also other rewarding stimuli, including foods, drinks, sexual partners, attractive faces, and even money (Knutson et al., 2001;

O’Doherty). In fact, recent research has suggested the involvement of these areas in coding the rewarding aspects of even complex social behavior. Thus, the accumbens and related structures activate to signals of cooperation in the prisoner’s dilemma games (Rilling, 2003), and even during “altruistic punishment”, or when a person punishes a transgressor against her group by sacrificing her own benefit (De Quervain et al., 2004).

Cortical networks

Of course, one cannot talk about the emotions of humans without discussing the many functions of the cortex. Below we focus on two areas, the somatosensory cortices, and the prefrontal cortex, and highlight their roles in the “embodiment” of emotion, generation and regulation of conscious affective experience, as well as their role in integrating emotional and cognitive information. Social Neuroscience - 11

Somatosensory Cortices and Insula

The primary somatosensory cortex (S1) runs top-down behind the central sulcus and is responsible for body sensation (e.g., touch) and proprioception (i.e., state of muscles and joints).

S1 is organized in a roughly topographic fashion, containing a receptive field for every body part, with larger receptive fields devoted to more highly innervated parts (e.g., lips). The secondary somatosensory cortex (S2) lies inferior to S1 and is mostly buried in the lateral sulcus.

Functionally, S2 serves as a higher order association area for body sensations and may be involved in the creation of “body image” (Ramachandran & Blakeslee, 1998). Near the bottom of the somatosensory cortex, almost at the intersection of the frontal, parietal and temporal lobes, lies the insula (Adolphs et al., 2000). The insula receives inputs from limbic structures, such as the amygdala, and cortical structures, such as prefrontal cortex and the anterior cingulate.

Functionally, the insula appears particularly important for introception, or monitoring the state of internal organs (Craig, 2003; Critchley et al. 2004) as well as subjective reactions to pain

(Peyron et al., 2000) and rewards (O’Doherty et al., 2002).

There is some reason to believe that somatosensory cortices may be involved in “emotion embodiment” effects, many of which have been initially reported by social psychologists. For example, processing of affective stimuli often facilitates congruent bodily responses whereas congruent bodily responses facilitate processing of affective stimuli (Cacioppo & Priester;

19XX; Niedenthal, Barsalou, Winkielman, Krauth-Grubber, & Rick, in press; Strack &

Neumann; 2004). For example, participants free to mimic facial expressions of the stimulus person are more efficient in detecting changes in the person’s expression than participants prevented from mimicking (Niedenthal, Brauer, Halberstadt, & Innes-Ker, 2001). There is evidence that somatosensory cortices may be causally involved in this effect. For example, Social Neuroscience - 12 patients with lesions in somatosensory cortex show poorer performance in classifying facial expressions than controls (Adolphs, Damasio, Tranel, Cooper, and Damasio (2000).

Presumably, simulating emotional expressions on one’s own face, and experiencing the resulting somatosensory feedback, facilitates the process of recognition (similar results have also been obtained for perception of emotion from the body, Heberlein & Adolphs, 2004).

Interestingly, the insula tends to activate during both experience, as well as observation of affective states with high somatosensory and “visceral” component. For example, human studies show involvement of insula in experience and observation of pain (Singer et al, 2004), experience and observation of disgust (Wicker et al. 2003).

Finally, there is also evidence that somatosensory cortices might be critically involved in conscious emotional experience, perhaps by generating a model of the current body state. For example, neuroimaging studies show that recall of emotional memories is associated with extensive activation of somatosensory cortex (Damasio et al., 2000). More importantly, lesions to the somatosensory cortices are associated with reduction of intensity of conscious affective experience (Prinz, 2004).

Prefrontal cortex.

Prefrontal cortex lies, not surprisingly, at the very front of the brain. The ventral or bottom one-third of prefrontal cortex is called the orbitofrontal cortex (OFC) and is most elaborately developed in humans and other primates. As we review next, prefrontal cortex is involved in flexible learning of stimulus value, the use of somatosensory feedback in decision, as well as in generation and regulation of subjective emotional experience

Much research attention on the role of OFC in emotion has focused on its role in associating higher-level representation of stimulus with its reward value. Thus, neurons in the Social Neuroscience - 13

OFC that code for a reward-value of a particular food (e.g., a banana) fire only when the animal is hungry (Rolls, 1999). Importantly, the OFC neurons are highly flexible in their coding properties, and will not fire when the reward properties of the stimulus change (e.g., the red square previously associated with food deliver is no longer associated with food).

A more circumscribed section of the prefrontal cortex --- the ventral-medial prefrontal cortex (vmPFC) – has been the focus of extensive research. According to some proposals, this part of the brain underlies the ability to incorporate bodily feedback (somatosensory and visceral) into judgments and decisions (Damasio, 1994). For example in one study, vmPFC lesioned and control patients were asked to make money in a gambling game that required them to select cards from different decks (Bechara, Damasio, Tranel & Damasio, 1997). Some cards were associated with a payment, whereas others were associated with a substantial loss. The rules of the game were complex enough to prevent the players from easily figuring out payoffs associated with each deck. Interestingly, after playing the game for a while, normals started to show anticipatory skin-conductance response to decks associated with a loss and began to avoid taking cards from these decks. The vmPFC patients, however, showed no anticipatory SCR responses to these decks and continued to take cards from them. Interestingly, these autonomic and behavioral differences emerged even though controls and prefrontal patients did not differ in their explicit understanding of the payoff rules at this point of the game. Bechara et al. (1997) interpreted these results to mean that the ability to make good decisions is at least partly dependent on intact mechanisms of affective feedback.

Prefrontal cortex is also important for affect regulation, presumably via descending projections to the amygdala and the accumbens (Damasio, 1999; Phan, Wager, Taylor, &

Liberzon, 2004). For example, orbitofrontal cortex projects back to the accumbens (Davidson, Social Neuroscience - 14

Jackson, & Kalin, 2000) and the dorsolateral prefrontal cortex projects back to the amygdala

(Ochsner & Gross, 2004).

Bar-on, Tranel, Denburg, and Bechara (2003) examined the potential role of the vmPFC in social intelligence. The study involved 12 patients with focal, stable bilateral lesions of the vmPFC or with right unilateral lesions of the amygdala or the right insular cortices, and 11 patients with focal, stable lesions in structures outside the neural circuitry thought to mediate somatic state activation and decision-making. Both groups of patients completed measures of various aspects of emotional and social intelligence, the just described gambling task, social functioning, personality and psychopathology, and standardized neuropsychological tests to assess their cognitive intelligence, executive functioning, perception and memory. Cognitive intelligence, executive functioning, perception, memory, personality, and psychopathology were comparable for the two patient groups, but patients with lesions in the vmPFC, amygdala, or insula performed more poorly on the measures of emotional intelligence, decision-making, and social functioning.

Finally, there is some evidence that subcortical projections to the prefrontal cortex contribute to conscious affective experience. For example, the intense feeling of pleasure experienced by heroin users appears to involve accumbens-to-cortex signals (Wise, 1996). In another example, self-reports of “excitement” in typical participants are related to the degree of activation in the nucleus accumbens and prefrontal cortex (Knutson et al, 2004).

3) Contribution of subcortical and cortical networks to conscious and unconscious affective influences.

As our brief review indicates, both subcortical systems, and cortical systems participate in emotion as a complex set of interconnected loops. Accordingly, any isolated focus on Social Neuroscience - 15 subcortex or cortex cannot do justice to the wide spectrum of human emotion. However, within those loops, the subcortical systems seem essential for basic affective reactions, and for mobilizing physiological support for the behavioral response. In contrast, the cortical systems seem essential for supporting symbolic appraisal processes, integrating the affective reactions with cognitive representations of the stimulus, affect regulation, and for generation of conscious affective experience. Specifically, the conscious experience, the phenomenal aspect of emotion, appears to involve the interaction between cortical and subcortical nuclei, as the cortex hierarchically re-represents and feeds back on the subcortical processes.3

Doing without feeling

The just described organization of the brain raises the possibility for functional decoupling, possibly allowing for cases where an emotional stimulus has an impact on behavior, without manifesting itself in conscious feelings. This possibility is consistent with our research on “unconscious affect” (Winkielman, Berridge & Wilbarger, 2005). Specifically, we conducted two studies assessing participants’ behavior towards a novel beverage after exposing them to several subliminal emotional facial expressions (happy, neutral, or angry). Immediately after the subliminal affect induction, participants rated their feelings (mood and arousal) and consumed and evaluated the beverage, with order of feeling ratings and behavior counterbalanced. In both studies, there was no evidence of any change in conscious mood or arousal. Yet subliminal expressions influenced participants’ behavior and evaluation, particularly when participants were

3 Note that our point about conscious experience is not about anatomical separation – a neat division of labor where subcortical networks instantiate unconscious processes whereas cortical networks instantiate conscious processes. Our point is that the mechanisms of consciousness, including affective consciousness, are computationally demanding and require ability to re-represent the input, integrate across multiple sources of input, and probably create some rudimentary representation of the self (Dennett, 1991). On that view, different mechanisms could be mixed together in the same brain divisions, or the same brain divisions could have both conscious and unconscious modes. Social Neuroscience - 16 thirsty. Specifically, after happy faces thirsty participants poured more drink from the pitcher, and drank more from their cup than after angry faces (Study 1). Thirsty participants were also willing to pay more for the drink after happy, rather than angry expressions (Study 2). These results suggest that under some conditions an affective process strong enough to influence behavior can occur without producing a conscious experience.

To give a neuroscientific account of a possible mechanism, we speculate that subliminal facial expressions might activate the amygdala, which then might project to the adjacent accumbens and related structures responsible for processing of natural incentives (Berridge,

2003; Rolls, 1999; Whalen et al., 1998). Altered neuronal activity in the nucleus accumbens

(constituting unconscious 'liking') could then change the human affective reaction to the sight and taste of a drink, leading to differential behavior and ratings. In other words, we propose a mechanism that is not unlike what happens when a morphine microinjection into a rat’s shell of accumbens enhances the rat’s affective reaction to sweetness, and leads to behavioral reaction of greater ‘liking’. All this can happen without “conscious feelings”, which presumably involve mechanisms of mapping the current body state, perhaps in the insula and somatosensory cortices, and integrating this information with the representation of the self.

One implication of this finding for social psychological theory is that the impact of basic affective reactions can fall outside the domain of models that postulate a critical role for conscious feelings in affective influence (e.g., the “feeling-as-information” model; Schwarz &

Clore, 1996). Instead, we propose that basic affective stimuli can sometimes act via unconscious processes to directly alter the target’s incentive value.

Finally, it is worth emphasizing that affect is not unique in its ability to drive behavior independent of conscious experience. As documented in research on “vision for action” Social Neuroscience - 17

(Goodale & Milner, 2004) and in research on “blindsight” (Weiscranz, 1996), under certain conditions, visual information can feed into the action system without ever reaching brain areas responsible for conscious vision. For example, a patient with a visual form agnosia caused by damage to the ventral stream regions of the temporal lobe is unable to provide a correct perceptual report of the orientation of a letter slot. However, when the patient is asked to insert a letter into the slot, she shows no difficulty (Goodale & Milner, 2004).

4) Interaction of social and cognitive information across subcortical and cortical networks.

There is little in a typical human life that does not involve some interplay between social cognition and emotion. For example, in going about our daily business, we need to recognize faces of familiar people and remember new people, with many of these faces carrying an emotional expression. We also need to make inferences regarding people’s reasons for doing things, and these inferences are often either triggered by, or lead to an emotional response. In yet another example, social life is filled with deliberations about group membership, with many strong positive and negative sentiments deriving from it.

Because of the inherent connections between, and the importance of social and emotional information, Cacioppo and colleagues have argued that social and emotional processes may interact, as well as share some basic neural mechanisms (Norris, Chen, Zhu, Small, & Cacioppo,

2004). More specifically, the adaptive advantage of discerning social signals, and organizing flexible behavioral responses may have been achieved in part by co-opting and building on selected neural systems that evolved originally for dealing with hedonic events (threats, appetitive stimuli). Although circuits rather than individual nuclei are better thought of as the substrates of feelings and emotions, various localized nuclei have been associated with specific behavioral functions. In this section, we provide a brief overview of this literature. Social Neuroscience - 18

Amygdala

Earlier we described the involvement of amygdala in affective processes. Research also highlights importance of this structure in social cognition. One of the first hints of this comes from research that examined the extent of amygdala damage on social behavior. Kluver and

Bucy (1939/1997) first reported disturbances in the social behavior of primates with extensive amygdala damage (but see Amaral et al. 2004 for a reevaluation of some claims). More recent research suggests that the amygdala is involved in many subtle aspects of social cognition. In one study a patient with bilateral damage to the amygdala fails to spontaneously provide a social interpretation of the famous Heider & Simmel film (Heberlein and Adolphs). Interestingly, SM performed normally on direct questions regarding the film that rely on social attributions (e.g.,

“What was the large triangle like?”), suggesting that her impairment lies in automatically inferring social meaning from a nonsocial stimulus and that the amygdala may play an important role in these social inferences. Other research suggests amygdala involvement in making judgments regarding the trustworthiness of unknown individuals (Adolphs, Tranel, & Damasio,

1998; Winston, Strange, O’Doherty, & Dolan, 2002); and in the attribution of internal states, beliefs, and desires to other people (Baron-Cohen et al., 2000).

However, it is important to note that each of these studies confounds social and emotional processes. For example, as determining the emotion expressed by a conspecific requires distilling emotional information from a social context, an impairment in one necessarily affects the other. To address this concern, one recent study has compared amygdala activation in response to emotional faces and emotional scenes (Hariri, Tessitore, Mattay, Fera and

Weinberger (2002). Specifically, in this study fMRI measured amygdalar activation while participants viewed fearful and threatening faces and ‘scenes’ taken from the IAPS (Lang, Social Neuroscience - 19

Bradley, & Cuthbert, 1997). Importantly, none of the IAPS pictures contained human faces, but rather included natural threats (i.e., dogs, snakes, spiders, sharks) and other threats (i.e., guns, car accidents, plane crashes, explosions). The authors report that the amygdala showed significant activation to both types of stimuli; however, activation of the right amygdala was significantly greater when participants viewed fearful and threatening faces than scenes. These results suggest that the amygdala is involved in processing both emotional and social stimuli, consistent with the hypothesis that social cognition may have co-opted existing neural networks underlying hedonic processes.

The study conducted by Hariri et al. (2002) contained a number of design features that limit its interpretation. For instance, the authors suggest that differences in complexity, arousal, or similarity of the stimuli across conditions could potentially account for observed differences in activation for faces and scenes (Hariri et al., 2002); none of these explanations can be ruled out. Furthermore, the study by Hariri et al. does not directly address the question of whether the amygdala is involved in processing emotional stimuli, or whether activation would be observed in response to neutral stimuli, as well.

We recently conducted an fMRI study to investigate the interactive and independent effects of social and emotional processes in the brain in which we controlled for the confounding factors in the Hariri et al. study and included neutral stimuli to allow a test of effects due to emotionality (Norris, Chen, Zhu, Small, & Cacioppo, 2004). Participants viewed a set of IAPS pictures that varied in two dimensions, such that each picture was either neutral or emotional

(collapsed across positive and negative valence), and was either social (i.e., contained one or more faces or bodies of conspecifics) or nonsocial (i.e., scenes, objects). Animals were excluded from the design, and all four groups of stimuli were matched on complexity and arousal. Results Social Neuroscience - 20 for the amygdala, one of our regions of interest, indicated two main effects, such that amygdalar activation was greater for emotional than for neutral stimuli, and greater for social than for nonsocial stimuli (Norris et al., 2004). Thus, the amygdala, a central component of many neuroanatomically-based theories of emotion, is also clearly implicated in social cognition.

These findings suggest that the amygdala may be involved in general attentional and motivational processes – for instance, in directing sensory and attentional processes to stimuli that upon a rudimentary analysis appear to have potential motivational significance.

Accordingly, emotional (negative and positive) and social stimuli can have additive effects on amygdala activation.

Cortical regions

The hypothesis that social information processing co-opted neural organizations that are involved in emotional information processing is also in line with our finding that the amygdala was not alone in being affected by social stimuli. Norris et al. (2004) found the medial prefrontal cortex (mPFC) and the middle occipito-temporal cortex (i.e., visual association cortex), neural regions often reported as being activated by emotional pictures, were also more active when participants viewed pictures that depicted conspecifics than those that did not. Phan, Wager,

Taylor, & Liberzon’s (2002) meta-analysis indicated that the mPFC was commonly activated in studies of emotion. Specifically, they found mPFC to be active during experience of happiness, fear, anger, sadness, and disgust, regardless of whether elicitation occurred visually, auditorially, or through guided recall.

Although the specific role of mPFC in emotional processes has yet to be specified, it is noteworthy that the mPFC appears also to be more active to social than nonsocial stimuli matched for extremity, arousal, visual complexity, and luminance (Norris et al., 2004) and more Social Neuroscience - 21 active in response to controllable than uncontrollable stressors (Amat et al., 2005). Amat et al.

(20005), for instance found that the ventral portion of the mPFC is involved in the detection of whether a stressor is under the organism’s control and in the diminution of the inhibitory effects of the mPFC on brainstem nuclei (e.g., dorsal raphe nucleus) when the stressor controllable.

Moreover, a good deal of research supports the claim that portions of the occipital cortex are more active to emotionally arousing pictorial stimuli than to neutral, unarousing stimuli (cf. Phan et al., 2002; Lane, Chua, & Dolan, 1999; Lang, Bradley, Fitzsimmons, Cuthbert, Scott, Moulder,

& Nangia, 1998). Norris et al. (2004) replicated this effect and further found that the middle occipito-temporal cortex was also more active to social than to nonsocial stimuli (Norris et al.,

2004), suggesting that both emotional and social information garner attentional resources.

Interestingly, complementary findings suggest that neural regions implicated in social cognition (e.g., gaze pursuit, perception of biological motion, face perception and recognition) are also sensitive to the motivational significance (e.g., emotional content) of stimuli. One of the first studies to demonstrate this pattern was a PET study conducted by Geday, Gjedde, Boldsen,

& Kupers (2003) in which participants viewed a set of pictures that varied both in social complexity, from low (e.g., faces) to high (e.g., social situations), and in emotional valence

(positive, negative, neutral). Results demonstrated that regional cerebral blood flow (rCBF) in the fusiform gyrus, a neural region previously implicated in face perception (cf. Kanwisher,

McDermott, & Chun, 1997), was not only greater when participants viewed more complex versus less complex social stimuli, but was also greater when participants viewed emotional (i.e., positive and negative) as compared to neutral stimuli (see also Dolan, Fletcher, Morris, Kapur,

Deakin, & Frith, 1996; Vuilleumier, Armony, Driver, & Dolan, 2001). In other words, neural Social Neuroscience - 22 structures involved in processing social signals, such as eye gaze, faces, and biological motion, may have evolved to also be sensitive to motivational significance.

We recently replicated the finding that the fusiform gyrus is more active to emotional than to neutral stimuli; furthermore, this pattern was driven by activation to social stimuli, consistent with the proposed role of the fusiform in social cognition (Norris et al., 2004). In addition, our results indicated that two other neural regions implicated in processing social information were also sensitive to emotional content: the superior temporal sulcus (STS) and the inferior frontal gyrus (IFG). Although the STS is most often considered to be involved in the perception of biological motion (cf. Puce & Perrott, 2003; Grossman & Blake, 2001), a growing literature supports the conclusion that the STS is also sensitive to emotional content. Narumoto,

Okada, Sadato, Fukui, & Yonekura (2001) showed that selective attention to emotional expression versus to the face itself enhanced activation of the right STS. In a study examining the neural correlates of basic and moral emotions, Moll, de Oliveira-Souza, Eslinger, Bramati,

Mourao-Miranda, Andreiuolo, & Pessoa (2002) reported that the STS was recruited by viewing scenes evocative of moral emotions. Kilts, Egan, Gideon, Ely, and Hoffman (2003) demonstrated that whereas dynamic emotional displays of anger expressions elicit greater activation of the STS than do static emotional displays of anger, this finding does not generalize to expressions of happiness. Thus, the STS is not just activated by dynamic (i.e., moving) stimuli, but is also selectively responsive to different emotional content, and particularly to emotional stimuli that may have stronger motivational significance for the observer (anger versus happiness).

The IFG has also been implicated in social cognition, particularly face processing, as evidenced by studies examining visual imagery of famous faces (Ishai, Haxby & Ungerleider,

2002), integration of visual faces and names (Campanella, Joassin, Rossion, De Volder, Bruyer, Social Neuroscience - 23

& Crommelinck, 2001), viewing of unfamiliar faces (McDermott, Buckner, Petersen, Kelley, &

Sanders, 1999), and performing a face matching task (Haxby, Horwitz, Ungerleider, Maisog,

Pietrini, & Grady, 1994). In addition, regions of the IFG in the left hemisphere are critically important for speech perception, and potentially for the integration of heard speech and speech read from a moving face (Calvert & Campbell, 2003). Rizzolatti and his colleagues (cf.

Rizzolatti, Fadiga, Gallese, & Fogassi, 1996) have argued that the human inferior frontal gyrus may correspond to area F5 of the monkey premotor cortex, which contains mirror neurons that discharge both when an action is performed and observed (cf. Rizzolatti, Fogassi, & Gallese,

2001; Gallese, Fadiga, Fogassi, & Rizzolatti, 1996; Koski, WOhlschlager, Bekkering, Woods,

Dubeau, Mazziotta, & Iacoboni, 2002). These findings taken together have led some researchers to suggest that the IFG is involved in empathy, an emotion that derives its meaning from the social context and may function through imitative mechanisms (cf. Carr, Iacoboni, Dubeau,

Mazziotta & Lenzi, 2003; Metlzoff & Decety, 2003).

In sum, converging evidence supports the notion that many of the neural structures involved in social information processing, such as perception of faces and biological motion, are also involved in emotional processing. The fusiform gyrus, superior temporal sulcus, and inferior frontal gyrus have all been shown to be recruited both when individuals process social stimuli and when stimuli have emotional significance.

Finally, it is also possible that social and emotional information may be interactively processed in the brain, such that emotional stimuli that depict or implicate conspecifics may elicit much stronger activation than either social or emotional stimuli alone. In our recent fMRI study (Norris et al., 2004), three neural regions showed evidence of the interactive processing of social and emotional information: the thalamus, middle occipito-temporal cortex, and STS all Social Neuroscience - 24 exhibited the same pattern, such that pictures that were both emotional in nature and contained social cues elicited greater activation than those that were either emotional, social or neither.

Importantly, these three neural regions are relatively early in the processing stream, suggesting that emotional stimuli depicting conspecifics may garner greater attentional resources. Thus, emotional and social information appear to interact at very early stages of processing, consistent with the evolutionary significance of social and emotional stimuli.

Interactivity in processing of emotion and memory

Our final example of interactive nature of brain representation of emotion and cognition comes for research on the relationship between affect and memory. Earlier in the chapter, we discussed several emotion and memory phenomena, such as emotionally-potentiated encoding.

However, research shows that affect and memory can interact even in a more subtle way, as when a perceiver’s affective response accompanies the very act of stimulus recognition. Thus,

Tichener (1910) wrote that familiar stimuli elicit a “warm glow”. Nearly a century later, a host of studies have demonstrated that generally variables which enhance familiarity also enhance positive affect (Reber, Winkielman, & Schwarz, 1998; Winkielman & Cacioppo, 2001;

Winkielman, Nowak, & Schwarz, 2002). Thus, familiarity and liking are enhanced by (i) repeated exposure to a stimulus (mere-exposure effect), (ii) exposure to category exemplars that converge on a prototype (beauty-in-averages effect), (iii) presenting the target with higher clarity or at longer durations, or (iv) by preceding the target with perceptual or semantic primes. In addition to these commonalities, familiarity and affect are both fast processes. Familiarity judgments are often faster than recognition judgments (Mandler, 1980) and preference judgments are often faster than judgments about other attributes (Zajonc, 1980). Finally, not only are familiar things positive, but positive things are also familiar, as demonstrated by the work of Social Neuroscience - 25

Mackie, Monin, Phaf and others (cites).

Work in cognitive and affective neuroscience helps to makes sense of these findings.

Many brain structures, including prefrontal cortex, anterior cingulate, amygdala, and hippocampus, are critically involved in cognitive and affective processing, with both types of processing often occurring in parallel (Elliot and Dolan; Damasio, 1999; Fernandez-Duque,

Baird, & Posner, 2000; Lane, Reiman, Axelrod, Yun, Holmes, & Schwartz, 1998; LeDoux,

1996; Rolls, 1999). Reflecting on these observations, Winkielman and colleagues proposed that perhaps affect is one of the ways organisms internally monitor changes in cognitive processing and memory (Winkielman et al., 2004). Specifically, their “hedonic fluency model” proposes that high and unexpected ease (fluency) of processing leads to a positive affective reaction.

There are several reasons for this assumption. First, easy processing indicates good progress towards the goal of successful recognition and coherent interpretation of the target (Carver &

Scheier, 1990; Vallacher & Nowak, 1999). Experiencing such progress as pleasant may be not only informative, but also rewarding and hence play a motivational role in bringing a cognitive activity to completion (Ramaschandran & Hirstein, 1999). Second, easy processing is pleasant because it indicates the availability of appropriate knowledge structures to deal with a current situation (Bless & Fiedler, 1995; Schwarz, 1990). Conversely, difficult processing signals a potential problem or threat, signaling the need for either additional limited resources and effort

(e.g., active coping), or disengagement and withdrawal to minimize risks and aversion (e.g., passive coping). In short, fluency signal might be positively marked because it says something about a positive state of affairs, either within the cognitive system, or in the world. We were able to support this assumption in a variety of studies using physiological measures, such as facial electromyography. Specifically, participants are more likely to “smile” to items that are Social Neuroscience - 26 made easy to process using a variety of manipulations (Winkielman & Cacioppo, 2001,

Winkielman et al., 2004).

CONCLUSION

In this chapter, we have reviewed some of the neural circuits underlying affect elicitation, experience, and regulation. We also highlighted pathways by which affect can interact with cognition. In the course of reviewing we emphasized the following points (1) affective processes are represented across multiple levels of processing, (2) under certain conditions, affective stimuli can have independent effects on behavior and conscious experience, (3) there are many ties between social and affective processing. Social Neuroscience - 27

References

Adolphs, R., Damasio, H., Tranel, D., Cooper, G., & Damasio, A. R. (2000). A role for

somatosensory cortices in the visual recognition of emotion as revealed by 3-D lesion

mapping. Journal of Neuroscience, 20, 2683-2690.

Amat, J., Baratta, M. V., Paul, E., Bland, S. T., Watkins, L. R., & Maier, S. F. (2005). Medial

prefrontal cortex determines how stressor controllability affects behavior and dorsal

raphe nucleus. Nature Neuroscience, 8, 365-371.

Anderson, A.K. & Phelps, E.A. (2002). Is the human amygdala critical for the subjective

experience of emotion? Evidence of intact dispositional affect in patients with lesions of

the amygdala. Journal of Cognitive Neuroscience, 14, 709-20.

Bar-On, R., Tranel, D., Denburg, N. L., & Bechara, A. (2003). Exploring the neurological

substrate of emotional and social intelligence. Brain, 126, 1790-1800.

Baron-Cohen, S., Ring, H.A., Bullmore, E.T., Wheelwright, S., Ashwin, C. & Williams, S.C.R.

(2000). The amygdala theory of autism. Neuroscience and Biohavioral Reviews, 24, 355-

Bartoshuk, L.M. (2000). Psychophysical advances aid the study of genetic variation in taste.

Appetite, 34, 105.

Berntson, G. G., & Cacioppo, J. T. (in press). The neuroevolution of motivation. In J. Shah &

W. Gardner (Eds.), Handbook of motivation science. New York: Guilford.

Berntson, G. G., Sarter, M., & Cacioppo, J. T. (1998). Anxiety and cardiovascular reactivity:

The basal forebrain cholinergic link. Behavioural Brain Research, 94, 225-248.

Berridge, K. C. (2000). Measuring hedonic impact in animals and infants: microstructure of

affective taste reactivity patterns. Neuroscience & Biobehavioral Reviews, 24, 173-198 Social Neuroscience - 28

Berridge, K.C. (2003). Comparing the emotional brain of humans and other animals. In

Handbook of Affective Sciences, R.J. Davidson, H.H. Goldsmith, & K. Scherer (Eds.), pp.

25-51, Oxford University Press.

Berridge, K. C., & Pecina, S. (1995). Benzodiazepines, appetite, and taste palatability.

Neuroscience and Biobehavioral Reviews, 19, 121–131.

Berridge, K. C., & Robinson, T. E. (1998). What is the role of dopamine in reward: Hedonic

impact, reward learning, or incentive salience? Brain Research—Brain Research

Reviews, 28, 309–369.

Berridge, K. C., & Winkielman, P. (2003). What is an unconscious emotion: The case for

unconscious 'liking'. Cognition and Emotion, 17, 181-211.

Cabanac M (1992) Pleasure: the common currency. Journal of Theoretical Biology 155: 173-

Cabanac, M. (1999). Emotion and Phylogeny. Journal of Consciousness Studies, 6, 176-90

Cacioppo, J. T., & Berntson, G. G. (2002). Social neuroscience. In Cacioppo, J. T., Berntson,

G. G., Adolphs, R., Carter, C. S., Davidson, R. J., McClintock, M. K., McEwen, B. S.,

Meaney, M. J., Schacter, D. L., Sternberg, E. M., Suomi, S. S. & Taylor, S. E. (Eds.).

Foundations in social neuroscience. Cambridge, MA: MIT Press.

Cacioppo, J. T., & Gardner, W. L. (1999). Emotion. Annual Review of Psychology, 50, 191-

Cacioppo, J. T., Larsen, J. T., Smith, N. K., & Berntson, G. G. (2004). The affect system: What

lurks below the surface of feelings? In A. S. R. Manstead, N. H. Frijda, & A. H. Fischer

(Eds.), Feelings and emotions: The Amsterdam conference. New York: Cambridge

University Press. Social Neuroscience - 29

Clore, G. L. (1994). Why emotions are never unconscious. In P. Ekman & R. J. Davidson (Eds.),

The nature of emotion: Fundamental questions (pp. 285-290). New York: Oxford

University Press.

Cosmides, L. & Tooby, J. (2000). Evolutionary psychology and the emotions. In M. Lewis & J.

Haviland-Jones (Eds.) Handbook of emotion (2 nd ed.) pp. 91-115.

Craig, A. D. (2003). Interoception: the sense of the physiological condition of the body. Current

Opinion in Neurobiology, 13, 500-505.

Crick, F. & Koch, C. (2003). A framework for consciousness. Nature Neuroscience, 6, 119-126

Critchley H.D., Wiens, S., Rotshtein, P., Oehman, A., Dolan, R.J. (2004). Neural systems

supporting interoceptive awareness. Nature Neuroscience, 2, 189-195

Cromwell, H. C., & Berridge, K. C. (1993). Where does damage lead to enhanced food aversion:

The ventral pallidum/substantia innominata or lateral hypothalamus? Brain Research,

624, 1–2, 1–10.

Damasio, A. R. (1999). The feeling of what happens: body and emotion in the making of

consciousness. New York: Harcourt Brace.

Damasio, A. R., Grabowski, T. J., Bechara, A., Damasio, H., Ponto, L. L., Parvizi, J., & Hichwa,

R. D. (2000). Subcortical and cortical brain activity during the feeling of self-generated

emotions. Nature Neuroscience, 3, 1049-1056.

Davidson, R. J., Jackson, D. C., & Kalin, N. H. (2000). Emotion, plasticity context, and

regulation: Perspectives from affective neuroscience. Psychological Bulletin, 126, 890–

Davis, M. (1997). The neurophysiological basis of acoustic startle modulation: Research on fear

motivation and sensory gating. In P. Lang, R. Simons, & M. Balaban (Eds.), Attention Social Neuroscience - 30

and orienting: Sensory and motivational processes. (pp. 69-98). Mahwah, NJ: Lawrence

Erlbaum.

Dennett, D. (1991). Consciousness Explained. Boston. Little Brown.

Dimberg, U., Thunberg, M., & Elmehed, K. (2000). Unconscious facial reactions to emotional

facial expressions. Psychological Science, 11, 86-89.

Dorus, S., Vallender, E. J., Evans, P. D., Anderson, J. R., Gilbert, S. L., Mahowald, M.,

Wyckoff, G. J., Malcom, C. M., & Lahn, B. T. (2004). Accelerated evolution of nervous

system genes in the origin of Homo sapiens. Cell, 119, 1027-1040.

Dunbar (2003). The social brain: mind, language and society in evolutionary perspective. Ann.

Rev. Anthrop. 32: 163-181. PDF

Enns, J.T., DiLollo, V. (2000). What's new in visual masking. Trends in Cognitive Sciences, 4,

345-352.

Frank, R. (1988). Passions within Reason. The Strategic Role of the Emotions. New York:

Norton.

Freud, S. (1950). Collected papers (J. Riviere, Trans. Vol. 4). London,: Hogarth Press and The

Institute of Psychoanalysis.

Frijda, N. H. (1999). Emotions and hedonic experience. In D. Kahneman, E. Diener & N.

Schwarz (Eds.), Well-being: The foundations of hedonic psychology (pp. 190-210). New

York: Russell Sage Foundation.

Funayama, E.S., Grillon, C.G., Davis, M. and Phelps, E.A. (2001). A double dissociation in the

affective modulation of startle in humans: Effects of unilateral temporal lobectomy.

Journal of Cognitive Neuroscience, 13, 721-729.

Goodson J.L, & Bass A.H. (2001). Social behavior functions and related anatomical Social Neuroscience - 31

characteristics of vasotocin/vasopressin systems in vertebrates. Brain Research Reviews,

35, 246-265.

Goodale, M.A. & Milner, M.A. (2004). Sight Unseen: An Exploration of Conscious and

Unconscious Vision. Oxford: Oxford University Press.

Hassert, D.L., Miyashita, T., & Williams, C. L. (2004). The Effects of Peripheral Vagal Nerve

Stimulation At A Memory Modulating Intensity on Norepinephrine Output in the

Basolateral Amygdala. Behavioral Neuroscience, 118, 79-88.

Heyes, C. M. & Huber, L. Eds. (2001) Evolution of Cognition. Cambridge, MA: MIT Press.

Hobson, P. (1993). Understanding persons: The role of affect. In S. Baron-Cohen, H. Tager-

Flusberg, & D. J. Cohen (Eds.), Understanding other minds: Perspective from autism

(pp. 204-227). New York: Oxford University Press.

Insel, T. R., & Fernald, R.D. (2004) How the Brain Processes Social Information: Searching for

the Social Brain. Annual Reviews: Neuroscience, 27, 697-722

James, W. (1884). What is an emotion. Mind, 9, 188-205.

Kasari, C., Sigman, M., Yirmiya, N., & Mundy, P. (1993). Affective development and

communication in children with autism. In A.P. Kaiser & D.B. Gray (Eds.), Enhancing

children's communication: Research foundation for early language interventions (pp.

201-222). New York: Paul H. Brooks.

Katkin, E.S., Wiens, S., & Öhman, A. (2001). Nonconscious fear conditioning, visceral

perception, and the development of gut feelings. Psychological Science, 12, 366-370.

Kihlstrom, J. F. (1999). The psychological unconscious. In L. A. Pervin & O. P. John (Eds.),

Handbook of personality: Theory and research (2 ed., pp. 424-442). New York: The

Guilford Press. Social Neuroscience - 32

Knutson, B., Adams, C.M., Fong, G.W., & Hommer, D. (2001). Anticipation of increasing

monetary reward selectively recruits nucleus accumbens.Journal of Neuroscience,21,1-5.

Knutson, B., Bjork, J. M., Fong, G. W., Hommer, D. W., Mattay, V. S., & Weinberger, D. R.

(2004). Amphetamine modulates human incentive processing. Neuron, 43, 261-269.

Konorski, J. (1967). Integrative activity of the brain: An interdisciplinary approach. Chicago:

University of Chicago Press.

Lambie, J. A., & Marcel, A. J. (2002). Consciousness and the varieties of emotion experience: A

theoretical framework. Psychological Review, 109, 219-259.

Lane, R. D. (2000). Neural correlates of conscious emotional experience. In R. D. Lane and L.

Nadel (Eds.), Cognitive neuroscience of emotion (pp. 345-370). New York, NY: Oxford

University Press.

Lang, P.J. (1995). The emotion probe: Studies of motivation and attention. American

Psychologist, 50, 372-385.

Larsen, R. J. & Fredrickson, B. L. (1999). Measurement issues in emotion research. In D.

Kahneman, E. Diener & N. Schwarz (Eds.) Well-being: Foundations of hedonic

psychology (pp. 40-60). New York: Russell Sage.

Lazarus, R. S., & McCleary, R. A. (1951). Autonomic discrimination without awareness: a study

of subception. Psychological Review, 58, 113-122.

LeDoux, J. (1996). The emotional brain: The mysterious underpinnings of emotional life. New

York: Simon & Schuster.

Martinez-Garcia F, Martinez-Marcos A, Lanuza E. (2002). The pallial amygdala of amniote

vertebrates: evolution of the concept, evolution of the structure. Brain Research Bulletin,

57, 463-469. Social Neuroscience - 33

McGaugh, J. (2003). Memory and Emotion: The Making of Lasting Memories. Columbia

University Press.

Mesquita, B., & Markus, H.R. (2004). Culture and emotion: Models of agency as sources of

cultural variation in emotion. In N.H. Frijda, A.S.R. Manstead, & A. Fisher (Eds.),

Feelings and emotions: The Amsterdam symposium. (pp. 341-358). Cambridge , MA :

Cambridge University Press.

Miyawaki, E., Perlmutter, J. S., Troster, A. I., Videen, T. O., & Koller, W. C. (2000). The

behavioral complications of pallidal stimulation: A case report. Brain & Cognition, 42,

417–434.

Monahan, J. L., Murphy, S. T., & Zajonc, R. B. (2000). Subliminal mere exposure: Specific,

general and diffuse effects. Psychological Science, 11, 462-466.

Morris, J. S., Öhman, A., & Dolan, R. J. (1999). A subcortical pathway to the right amygdala

mediating "unseen" fear. Proceedings of the National Academy of Sciences, 96, 1680-

National Institutes of Health. (1998). Rehabilitation of ersons with traumatic brain injury. Paper

presented at the NIH consensus statement, Washington, DC.

Nielsen, L. & Kaszniak, A.W. (in press). Conceptual, theoretical, and methodological issues in

inferring subjective emotion experience: recommendations for researchers. In J.A. Coan

and J.J.B. Allen (Eds.), The Handbook of Emotion Elicitation and Assessment. New

York, NY: Oxford University Press.

Norris, C. J., Chen, E. E., Zhu, D. C., Small, S. L., & Cacioppo, J. T. (2004). The interaction of

social and emotional processes in the brain. Journal of Cognitive Neuroscience, 16,

1818-1829. Social Neuroscience - 34

Ochsner, K. N., & Gross, J. J. (2004). Thinking makes it so: A social cognitive neuroscience

approach to emotion regulation. In R. F. Baumeister & K. D. Vohs (Eds.), Handbook of

self-regulation: Research, theory, and applications (pp. 229-255). New York: Guilford

O'Doherty J., Deichmann, R., Critchley H.D., & Dolan R.J. (2002). Neural responses during

anticipation of a primary taste reward. Neuron, 33, 815-26

Öhman, A., Flykt, A., & Lundqvist, D. (2000). Unconscious emotion: Evolutionary perspectives,

psychophysiological data and neuropsychological mechanisms. In R.D. Lane, L. Nadel &

G. Ahern (Eds.), Cognitive neuroscience of emotion (pp. 296-327). New York: Oxford

University Press.

Öhman, A., & Soares, J. J. F. (1994). "Unconscious anxiety": Phobic responses to masked

stimuli. Journal of Abnormal Psychology, 103, 231-240.

Panksepp, J. (1998). Affective neuroscience: the foundations of human and animal emotions.

Oxford, U.K.: Oxford University Press.

Pecina, S., & Berridge, K. C. (2000). Opioid eating site in accumbens shell mediates food intake

and hedonic ‘liking’: Map based on microinjection Fos plumes. Brain Research, 863, 71–

Peyron, R., Laurent, B., & Garcia-Larrea, L. (2000). Functional imaging of brain responses to

pain. A review and meta-analysis (2000). Clinical Neurophysiology, 30, 263-288.

Phan K.L, Wagner T, Taylor S.F., Liberzon, I. (2002). Functional neuroanatomy of emotion: a

meta-analysis of emotion activation studies in PET and fMRI. Neuroimage 16, 331–348.

Porges, S.W. (1997). Emotion: An evolutionary by-product of the neural regulation of the

autonomic nervous system. In C. S. Carter, B. Kirkpatrick, & I.I. Lederhendler (eds.), Social Neuroscience - 35

The Integrative Neurobiology of Affiliation, Annals of the New York Academy of

Sciences, 807, 62-77.

Ramachandran, V. S., & Blakeslee, S. (1998). Phantoms in the Brain. William Morrow, N.Y

Rauch, S. L., Shin, L. M., Dougherty, D. D., Alpert, N. M., Orr, S. P., Lasko, M., Macklin, M.

L., Fischman, A. J., & Pitman, R. K. (1999). Neural activation during sexual and

competitive arousal in healthy men. Psychiatry Research, 91, 1–10.

Robles, R., Smith, R., Carver, C.S. & Wellens, A. R. (1987). Influence of subliminal images on

the experience of anxiety. Personality and Social Psychology Bulletin, 13, 399-410.

Rolls, E. T. (1999). The brain and emotion. Oxford: Oxford University Press.

Russell, J. A. (2003). Core affect and the psychological construction of emotion. Psychological

Review, 110, 145-172.

Schoenemann, P. T., Sheehan, M. J., & Glotzer, L. D. (2005). Prefrontal white matter volume is

disproportionately larger in humans than in other primates. Nature Neuroscience, 8, 242-

Schooler, J. W. (2002). Re-representing consciousness: dissociations between experience and

meta-consciousness. Trends in Cognitive Sciences, 6, 339-344.

Schooler, J. W. & Schreiber, C. A. (2004). Consciousness, meta-consciousness, and the paradox

of introspection. Journal of Consciousness Studies, 11, 17-29.

Schwarz, N., & Clore, G.L. (2003). Mood as information: 20 years later. Psychological Inquiry,

14, 296-303.

Searle, J. (1997). The Mystery of Consciousness. New York, New York Review Press.

Simons, D. J., and Chabris, C. F. (1999). Gorillas in our midst: Sustained inattentional blindness

for dynamic events. Perception, 28, 1059-1074. Social Neuroscience - 36

Steiner, J. E. (1973). The gustofacial response: observation on normal and anencephalic newborn

infants. Symposium on Oral Sensation and Perception, 4, 254-278.

Steiner, J. E., Glaser, D., Hawilo, M. E., & Berridge, K. C. (2001). Comparative expression of

hedonic impact: Affective reactions to taste by human infants and other primates.

Neuroscience and Biobehavioral Reviews, 25, 53-74.

Tindell, A.J., Berridge, K.C., & Aldridge, J.W. (2004) Ventral pallidal representation of

Pavlovian cues and reward: Population and rate codes. Journal of Neuroscience, 24 ,

1058-1069.

Watson, D., & Tellegen, A. (1985). Toward a consensual structure of mood. Psychological

Bulletin, 98, 219-235.

Weiskrantz, L. (1996). Blindsight revisited. Current Opinion in Neurobiology, 6, 215-220.

Whalen, P.J. (1998) Fear, vigilance and ambiguity: initial neuroimaging studies of the human

amygdala. Current Directions in Psychological Science, 7, 177-188.

Whalen, P. J., Rauch, S. L., Etcoff, N. L., McInerney, S. C., Lee, M. B., & Jenike, M. A. (1998).

Masked presentations of emotional facial expressions modulate amygdala activity

without explicit knowledge. Journal of Neuroscience, 18, 411-418.

Williams, M.A., Morris, A.P., McGlone, F., Abbott, D.F., & Mattingley, J.B. (2004). Amygdala

responses to fearful and happy facial expressions under conditions of binocular

suppression. Journal of Neuroscience, 24, 2898-2904.

Willis, W. D., & Westlund, K. N. (1997). Neuroanatomy of the pain system and of the pathways

that modulate pain. Journal of Clinical Neurophysiology, 14, 2–31.

Winkielman P., Berntson G. G., & Cacioppo J. T. (2001). The psychophysiological perspective

on the social mind. In A. Tesser & N. Schwarz (Eds.), Blackwell Handbook of Social Social Neuroscience - 37

Psychology: Intraindividual Processes. (pp. 89-108). Oxford: Blackwell.

Winkielman, P. & Berridge, K. C. (2004). Unconscious emotion. Current Directions in

Psychological Science, 13, 120-123.

Winkielman, P., Berridge, K. C., & Wilbarger, J. (in press). Unconscious affective reactions to

masked happy versus angry faces influence consumption behavior and judgments of

value. Personality and Social Psychology Bulletin.

Winkielman, P., Zajonc, R. B., & Schwarz, N. (1997). Subliminal affective priming resists

attributional interventions. Cognition and Emotion, 11, 433-465.

Wise, R. A. (1996). Addictive drugs and brain stimulation reward. Annual Review of

Neuroscience, 19, 319–340. Social Neuroscience - 38

Figure 1: Generalized Emotional Brain in Mammals

Somatosensory Cortex Cingulate Cortex

Insular Cortex

Prefrontal Cortex

Thalamus

Brainstem Nucleus (dotted outline) Accumbens Amygdala Ventral Pallidum

Periacqueductal Grey Parabrachial Nucleus