Social Cognition

Behavioral and Cognitive Neuroscience Reviews
http://bcn.sagepub.com Social Cognition and the Prefrontal Cortex

Jacqueline N. Wood Behav Cogn Neurosci Rev 2003; 2; 97 DOI: 10.1177/1534582303002002002 The online version of this article can be found at: http://bcn.sagepub.com/cgi/content/abstract/2/2/97
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10.1177/1534582303253625 BEHAVIORAL AND COGNITIVE NEUROSCIENCE REVIEWS Wood / SOCIAL COGNITION
ARTICLE
Social Cognition and the Prefrontal Cortex

Jacqueline N. Wood National Institute of Neurological Disorders and Stroke, National Institutes of Health, Bethesda, MD Social cognitive neuroscience is a rapidly emerging field that utilizes cognitive neuroscientific techniques (e.g., lesion studies, neuroimaging) to address concepts traditionally in the social psychological realm (e.g., attitudes, stereotypes). The purpose of this article is to review published neuroscientific and neuropsychological research into social cognition. The author focuses on the role of the prefrontal cortex in social behavior and presents a framework that provides cohesion of this research. The article proposes that this framework will be useful in guiding future social cognitive neuroscientific research. Key Words: social cognition, behavior, prefrontal cortex, knowledge The purpose of this review is to bring together what we know so far about social cognition and the brain by drawing on neuropsychological and functional neuroimaging research. I will begin with a brief introduction to social psychology and cognitive neuroscience before proceeding to discuss existing social cognitive neuroscientific research. Discussion will be restricted to published studies exploring the relationship between social cognition and the brain. The focus will be on the role of the prefrontal cortex in human social cognition, although I will also discuss nonhuman primates and other animals. Although much has been learned from genetic and physiological studies of social cognition, this is beyond the scope of the present review (for a recent review, see Cacioppo, Berntson, Sheridan, & McClintock, 2000). Finally, I will introduce a theoretical framework that I believe will be useful in tackling the vast question of how the brain controls social cognition. Although some aspects of social cognitive neuroscience have been addressed in recent reviews (Adolphs, 1999; Cacioppo, 2002; Ochsner & Lieberman, 2001), these have not been comprehensive in the breadth of research reviewed (e.g., by considering only human research or a subset of social cognition). SOCIAL COGNITIVE NEUROSCIENCE: AN INTRODUCTION Human cognitive neuroscience explores the relationship between the brain and cognitive concepts such as episodic memory encoding and retrieval (Andreasen et al., 1995; Fletcher & Henson, 2001; Lee, Robbins, Pickard, &
Authors Note: Correspondence and reprint requests should be addressed to Dr. Jacqueline N. Wood, Cognitive Neuroscience Section, National Institute of Neurological Disorders and Stroke, National Institutes of Health, Building 10/Room 5C205, 10 Center Drive, Bethesda MD 20892-1440; or email woodj@ninds.nih.gov. Behavioral and Cognitive Neuroscience Reviews Volume 2 Number 2, June 2003 97-114 DOI: 10.1177/1534582303253625 2003 Sage Publications
Social cognition is part of our lives every dayfrom
interactions with your spouse and child to a job interview or formal presentation. The smooth running of our society depends on people following established social rules, and there are mechanisms in place to deal with those who do not follow these rules. As such, social cognition is a large but important area for study. Those who behave in a way that is deemed inappropriate or different are a source of fascination for many people. Perhaps the most famous case study in neuropsychology is that of Phineas Gage, the railroad worker who experienced extreme changes in social behavior following damage to his frontal lobes (Harlow, 1868). Although Gages story has been exaggerated during the years (Macmillan, 2000), clinical observations have shown that socially inappropriate behavior is common following frontal lobe injury, particularly if the orbitofrontal cortex is compromised (Cummings, 1995; Fuster, 1997; Masterman & Cummings, 1997). Until recently, social cognition has been the exclusive domain of social psychologists and sociologists. However, this research area has much to offer to the cognitive neuroscientific endeavor to understand the human mind and behavior; cognitive neuroscientists equally have much to offer to social psychology. The resulting field of social cognitive neuroscience is expanding rapidly. 97
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BEHAVIORAL AND COGNITIVE NEUROSCIENCE REVIEWS report measures and behavioral measures such as response times and error rates. Some of these questions are more accessible to cognitive neuroscientific analysis than others. There is a growing number of researchers who consider themselves to be social cognitive neuroscientists who have begun to use the neuroscientific techniques described above to address questions about the brains role in, for example, attitudes (Johnson, Kim, & Risse, 1985; Lieberman, Ochsner, Gilbert, & Schacter, 2001; Park et al., 2001), stereotypes (Milne & Grafman, 2001; Phelps et al., 2000, 2001), and aggression (Blair & Cipolotti, 2000; Grafman et al., 1996; Pietrini, Guazzelli, Basso, Jaffe, & Grafman, 2000). It is this research that I intend to address. At first sight, the research interests of cognitive neuroscience and social psychology may seem unrelated. However, the concepts explored in social psychology must, at some level, be represented in the brain and be a function of activation of networks of brain regions. Considering the importance of social interactions in our day-to-day lives, social psychological concepts must affect cognition. It has even been suggested that social cognition has been a driving force in our evolutionary development (Duchaine, Cosmides, & Tooby, 2001; Povinelli & Preuss, 1995). Recent research has demonstrated cultural differences in social behavior between colonies of chimpanzees (Whiten et al., 1999), suggesting that we are not the only animals with complex social interactions and cultural differences. There is a long history of research into social cognition in animalsfor example, at the beginning of the past century, scientists were addressing questions of changes in behavioral and emotional responses following frontal lobotomies in monkeys (Franz, 1907). Therefore, there is much that we can learn about social cognition and the brain from the study of nonhuman animals. In general, these data complement and extend those resulting from human research. I believe that it is only through integration of social psychology, cognitive psychology, and behavioral neuroscience that we will begin to understand the relationship between the brain, the mind, and behavior. PREFRONTAL CORTEX STRUCTURE AND CONNECTIVITY As stated above, the focus of the present review is the role of the prefrontal cortex in social cognition. The prefrontal cortex constitutes approximately one third of human cortex and is smaller and less sophisticated in most other species (Rilling & Insel, 1999; Semendeferi, Armstrong, Schleicher, Zilles, & van Hoesen, 2001; Semendeferi, Lu, Schenker, & Damasio, 2002). It is also the last part of the human brain to become fully devel-
Owen, 2000; Wagner et al., 1998), semantic processing (Demonet et al., 1992; Martin & Chao, 2001; Poldrack et al., 1999; Thompson-Schill, DEsposito, Aguirre, & Farah, 1997), executive functions (Carter et al., 2000; Hartley & Speer, 2000; Hughes, Russell, & Robbins, 1994), and attention (Casey et al., 2000; Coull, Frith, Buchel, & Nobre, 2000; Nagahama et al., 2001). The experimental methodology of cognitive neuroscience utilizes functional neuroimaging (positron emission tomography [PET]; functional magnetic resonance imaging [fMRI]; for a review of methodology and techniques, see Gazzaniga, 2000; Moonen & Bandettini, 2000), electroenencephalography (EEG) (Krakow, Allen, Lemieux, Symms, & Fish, 2000; Pivik et al., 1993), transcranial magnetic stimulation (Pascual-Leone, Grafman, Cohen, Roth, & Hallett, 1997), and neuropsychological testing of patients with brain injuries. These provide information about the brains activity while subjects perform cognitive tasks. There has been some exploration of social cognition in cognitive neuroscientific experiments; for example, studies exploring event knowledge representations have compared emotional and neutral social events (Partiot, Grafman, Sadato, Wachs, & Hallett, 1995) and have contrasted localization of social and nonsocial representations of event knowledge (Wood, Romero, Makale, & Grafman, 2003). These studies have implicated the prefrontal cortex in the storage of social event knowledge. This is in addition to a wealth of functional neuroimaging research into processing of emotional faces and pictures (Harmer, Thilo, Rothwell, & Goodwin, 2001; Kawasaki et al., 2001; Leube, Erb, Grodd, Bartels, & Kircher, 2001; Thomas et al., 2001; Vuilleumier, Armony, Driver, & Dolan, 2001; Winston, Strange, ODoherty, & Dolan, 2002). Although these studies have dipped into social cognition, there have been few studies directly addressing social psychological concepts. Social psychology, on the other hand, seeks to address questions regarding aggression (Anderson & Bushman, 2002; Bettencourt & Miller, 1996; Huesmann & Guerra, 1997), attitudes (Bargh, Chaiken, Govender, & Pratto, 1992; Fazio, Sanbonmatsu, Powell, & Kardes, 1986; Greenwald & Banaji, 1995), stereotypes (Devine, 2001; Greenwald, McGhee, & Schwartz, 1998; Wittenbrink, Judd, & Park, 2001), prejudice (Dovidio, Kawakami, & Gaertner, 2002; Duckitt, Wagner, du Plessis, & Birum, 2002; Lowery, Hardin, & Sinclair, 2001), attributions (Calam, Bolton, & Roberts, 2002; Dieser & Ruddell, 2002), group dynamics (Abrams, Marques, Brown, & Dougill, 2002; Battegay, 2001; Morgan & Scott, 2002), and social behavior and development (Avgitidou, 2001; Cameron, Alvarez, Ruble, & Fuligini, 2001). The experimental methodology of social psychology utilizes self-
Wood / SOCIAL COGNITION oped, with maturation occurring in late childhood (Huttenlocher & Dabholkar, 1997). The human prefrontal cortex can be divided into orbitofrontal and dorsolateral regions, which have reciprocal connectivity with each other as well as with posterior and subcortical brain regions. Although many authors use the terms ventromedial prefrontal cortex and orbitofrontal cortex interchangeably, the latter refers to most of the underside of the prefrontal cortex, whereas the former refers more specifically to the medial regions of the ventral prefrontal cortex (Krawczyk, 2002). As such, the orbitofrontal cortex includes both ventromedial and ventrolateral prefrontal cortex. Dorsolateral prefrontal neurons show connectivity with regions associated with motor control (premotor cortex, supplementary motor area, basal ganglia), performance monitoring (anterior cingulate), and sensory processing (parietal cortex, association areas). Orbitofrontal neurons, on the other hand, show connectivity with regions associated with emotional processing (amygdala), memory (hippocampus), and sensory processing (inferior temporal visual association regions). Taken together, the connectivity suggests that dorsolateral prefrontal cortex is particularly suited to the regulation and control of behavior and responses to environmental stimuli, and the orbitofrontal cortex to the integration of information about emotion, memory, and the environment. Therefore, one might expect that the orbitofrontal cortex is important in brain networks controlling social cognition with the implementation and control of behavior requiring dorsolateral prefrontal networks. AGGRESSION AND VIOLENCE Aggression is behavior toward another person with the intention of harming that person (for a recent review of the social cognition of aggression and violence, see Anderson & Bushman, 2002). An association between the frontal lobes and aggressive and violent behavior has been reported in many studies (Amen, Stubblefield, Carmichael, & Thisted, 1996; Blair & Cipolotti, 2000; Goyer, Andreason, & Semple, 1994; Grafman et al., 1996; Raine, Lencz, Bihrle, LaCasse, & Colletti, 2000). Patients with reduced blood flow (or reduced brain volume) in temporal and frontal regions have also demonstrated increased aggression (Hirono, Mega, Dinov, Mishkin, & Cummings, 2000; Raine, Buchsbaum, & LaCasse, 1997; Volkow & Tancredi, 1987; Volkow et al., 1995; Woermann et al., 2000). Given the strong association between frontal damage and aggression, however, it is likely that the increased aggression is a result of the damage to frontal rather than temporal regions.
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The Vietnam Head Injury Study investigated violent and aggressive behavior in 279 head-injured veterans of the Vietnam War (Grafman et al., 1996). They found that patients with mediofrontal or orbitofrontal lesions reported a higher incidence of aggressive/violent behavior. Interestingly, patients with left dorsolateral prefrontal cortex lesions also reported more aggressive behavior, although reports by friends/family members did not support this. Other researchers have also reported an association between left prefrontal cortex damage and self-reported levels of aggression (Raine et al., 2000; Woermann et al., 2000). These findings highlight the importance of obtaining independent assessments of behavior from friends or family members rather than relying solely on the patients own assessments. The neuropsychological evidence for frontal lobe pathology in aggression is strong. There has, however, been little neuroimaging research exploring aggression in healthy individuals. One such PET study required healthy individuals to imagine scenes in which they witnessed the assault of their mother in an elevator (Pietrini et al., 2000). There were three versions of the scene: passively watching the assault, being physically restrained by one of the perpetrators, and violently attacking the perpetrators. Reduced activation of medial prefrontal cortex was observed in all three conditionsthe effect was greatest for the scene in which the subject imagined violently attacking the perpetrators. A recent fMRI study reported activation of this same region when subjects viewed violent relative to neutral interpersonal interactions (Nakic, Makale, Wood, & Grafman, 2001). These findings are consistent with those of the Vietnam Head Injury Study discussed above. Taken together, these studies suggest that medial prefrontal cortex is important in the response to violent behavior. Aggression and violence have also been explored in animal research. Lesions of orbitofrontal cortex in oldworld monkeys have been shown to result in increased (Raleigh, Steklis, Ervin, Kling, & McGuire, 1979) and decreased (Butter & Snyder, 1972) aggression toward human observers. The data regarding aggression toward other monkeys following orbitofrontal lesions are equally mixed with some studies suggesting increased (Butter & Snyder, 1972) and others decreased aggression (Bowden, Goldman, & Rosvold, 1971; Deets, Harlow, Singh, & Blomquist, 1970). Increased aggression has also been reported following lesions of dorsolateral prefrontal cortex in monkeys (Miller, 1976). Increased aggression has been reported following lesions of orbitofrontal cortex in rats (Kolb, 1974; Kolb & Nonneman, 1974; Lubar, Herrmann, Moore, & Shouse, 1973) and decreased aggression following such lesions in cats (Warren, 1964). These studies are consis-
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BEHAVIORAL AND COGNITIVE NEUROSCIENCE REVIEWS but not left, frontal EEG asymmetry (Henderson, Fox, & Rubin, 2001). As in human studies, the prefrontal cortex seems to be important in regulating social cognition in nonhuman primates, with prefrontal cortex lesions resulting in abnormal social behaviorfor example, monkeys with prefrontal cortex lesions are described as withdrawn and less explorative (Deets et al., 1970; Peters & Ploog, 1976) and socially isolated after reintegration to the colony (Myers, Swett, & Miller, 1973). One study explored the effects of lesions to the prefrontal cortex and anterior temporal cortex on the social behavior of free-ranging monkeys (Franzen & Myers, 1973). On reintroduction to the colony, the monkeys failed to reestablish relationships with family members, approached other animals irrespective of dominance status, and no longer used facial expressions in social interactions. Similar problems have been reported following amygdala lesions in monkeysloss of dominance status and development of associated submissive behavior in lesioned monkeys (Emery et al., 2001; Kling & Cornell, 1971; Rosvold, Mirsky, & Pribram, 1954). Loss of dominance status has also been reported following orbitofrontal lesions in monkeys (Butter & Snyder, 1972). In terms of maternal behavior, female monkeys with prefrontal cortex lesions are indifferent to their infant, whereas those with anterior temporal lesions are aggressive (Franzen & Myers, 1973). Social impairments have also been reported in young monkeys following lesions to the medial temporal lobe, including the amygdala (Bachevalier, 1991, 1994). These data are consistent with those of studies into aggression and violence in demonstrating the role of the orbitofrontal cortex in the regulation of appropriate social behavior. Taken together, these studies support the role of prefrontal and temporal networks in social behavior and suggest that approach behaviors may be mediated by the left and withdrawal by the right hemisphere. With respect to nonhuman primates, damage to the orbitofrontal cortex or amygdala leads to change in social behavior. The network in humans extends to the ventromedial prefrontal cortex. These structures are reciprocally connected and it may be the case that disruption of this circuitry is the key, rather than damage to a particular structure. The studies also suggest that this network needs to be intact for appropriate behavior to be acquired during development. ATTITUDES AND STEREOTYPES Attitudes may be defined as a type of predisposition toward behavior (Rosenberg & Hovland, 1960; Yuker, 1965). This widely accepted view suggests that attitudes are biases toward or against behaviors or decisions and that they influence our decision making and behavior in
tent in reporting changes in levels of aggression following prefrontal cortex damage. Given that the size and structure of the prefrontal cortex varies greatly between species (Fuster, 1997; Petrides & Pandya, 1994, 1999), the possibility of species-specific differences (in terms of increased vs. decreased aggression) cannot be ruled out. Taken together, these data suggest that the orbitofrontal and medial prefrontal cortex are particularly important in regulating social behavior with respect to aggression and violence. In terms of neuroanatomy, orbitofrontal cortex has strong reciprocal connections to limbic regions, such as the amygdala, that process the emotional significance of stimuli (e.g., Ghashghaei & Barbas, 2002; Zald, 2003). An orbitofrontal-amygdala network is well-suited to identifying the threat (whether physical or social) posed by an object or individual and responding aggressively, if needed. SOCIAL BEHAVIOR There is a wealth of research documenting socially inappropriate behavior following damage to the prefrontal, particularly orbitofrontal and ventromedial, cortex (Anderson, Bechara, Damasio, Tranel, & Damasio, 1999; Blumer & Benson, 1975; Eslinger, Grattan, Damasio, & Damasio, 1992; Masterman & Cummings, 1997). Examples of socially inappropriate behavior include making lewd comments or asking strangers highly personal questions. Specific behavioral problems that have been reported following ventromedial prefrontal cortex damage include social inappropriateness, lack of insight, lack of initiative, poor judgment, and inappropriate affect (Barrash, Tranel, & Anderson, 2000). These data point to the importance of prefrontal cortex in regulating social behavior. There is some evidence suggesting that medial prefrontal regions are necessary for the acquisition of social rules, as early damage to these regions can result in severe impairment of social behavior (Anderson et al., 1999). There is some suggestion in the literature of laterality effects on social behavior with left frontal regions being associated with approach behaviors and right frontal regions with withdrawal behaviors (Davidson, 2001; Fox & Davidson, 1984; Harmon-Jones & Sigelman, 2001; Kinsbourne, 1978; Kinsbourne & Bemporad, 1984). Developmental studies have provided support for laterality differences, with EEG findings of anxietyrelated increases in right frontal activity in children during stressful social situations (Davidson & Fox, 1989; Fox, Bell, & Jones, 1992; Schmidt, Fox, Shulkin, & Gold, 1999). Furthermore, a recent prospective study reported that the presence of distress signals as an infant was predictive of social wariness in infants who displayed right,
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TABLE 1:
Congruent and Incongruent Conditions for Commonly Used Versions of the Implicit Association Task (IAT) Response 1 Response 2
Gender IAT Congruent Incongruent Race IAT Congruent Incongruent
Female names, weak words Female names, strong words African American names, unpleasant words African American names, pleasant words
Male names, strong words Male names, weak words Caucasian names, pleasant words Caucasian names, unpleasant words
NOTE: Congruent trials are consistent and incongruent trials inconsistent with the stereotype.
social situations. I consider attitudes to be a special form of associative knowledge that enables rapid access of an emotional or behavioral response on presentation of the attitude-objectat the most basic level, one might have approach and withdrawal behaviors associated with the attitude-object. There has been little neuropsychological or neuroimaging research into attitudes. The social psychology literature has focused on priming studies with healthy volunteerssuch studies typically focus on the closely linked concepts of attitude accessibility and automaticity (Bargh et al., 1992; Fazio, Chen, McDonel, & Sherman, 1982; Fazio et al., 1986). The majority of these studies have suggested that there is a continuum of accessibility with accessible attitudes being automatically activated and characterized, for example, by faster categorization as good or bad. However, this view of the relationship between accessibility and automaticity may seem rather circular. In a rare neurobehavioral study, Park and his colleagues reported a single case study addressing automatic attitude activation in a patient with bilateral frontal and temporal damage (Park et al., 2001). The patient showed no impairment when the attitudes were intentionally accessed, but showed impaired performance on negative but not positive attitudes when the attitude was automatically accessed. Park et al. (2001) proposed that the patients impairment was due to damage to a module that automatically processes negative evaluative information (p. 16). They suggest that this was due to frontal rather than temporal damage, although the extent of the lesion makes it difficult to draw any strong conclusion about localization. Two studies of patients following medial temporal lobe damage demonstrated intact attitude formation and change coupled with impaired episodic memory (Johnson et al., 1985; Lieberman et al., 2001). These data suggest that episodic memory and attitudes are independent representations and also that attitude representation does not implicate medial temporal regions. A stereotype is a socially shared set of beliefs about traits that are characteristic of members of a social category (Greenwald & Banaji, 1995, p. 14). These may be
considered a specialized instance of an attitude and, as such, they guide behavior toward members of the social category. Stereotypes have been explored extensively in the social psychology literature using the Implicit Association Test (IAT) (Greenwald et al., 1998). This task provides a measure of association between concepts and their attributes. Subjects are presented two tasks: one requires categorization of words into one of two possible categories, the other requires evaluation of words describing attributes. The response keys are shared across the task in a condition-dependent way (see Table 1). For example, in the congruent condition of the gender IAT shown in Table 1, subjects would press response key 1 if the words were female names or weak words (e.g., helpless, feeble) and response key 2 if the words were male names or strong words (e.g., brave, tough). The typical finding is that subjects respond faster to congruent (e.g., female-weak) than incongruent (e.g., maleweak) trials. Generally, the interpretation of the results is that subjects respond fastest when stereotype-compatible responses are mapped to the same response key. As for attitudes, there has been little research exploring the representation of stereotypes in the brain. One recent neuropsychological study examined gender stereotypes. Milne and Grafman (2001) explored accessibility of gender stereotypes in patients with frontal lobe lesions using a modified version of the IAT. Patients with lesions of the ventromedial prefrontal cortex showed impaired automatic priming of the stereotypic knowledge relative to healthy controls and patients with lesions of the prefrontal cortex that did not involve ventromedial regions. These data strongly suggest a role for the ventromedial prefrontal cortex in stereotype representation. There have been few neuroimaging studies exploring stereotypes. A study of the amygdalas response to processing of out-group and in-group faces showed that the activation associated with in-group faces (White faces for White subjects, Black faces for Black subjects) habituated over time (Hart et al., 2000). However, for outgroup faces (White faces for Black subjects, Black faces for White subjects), the amygdala activation did not show habituation. Phelps et al. (2000) replicated this
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BEHAVIORAL AND COGNITIVE NEUROSCIENCE REVIEWS prefrontal cortex that enables recognition of ones own face (Keenan, Wheeler, Gallup, & Pascual-Leone, 2000; Kircher et al., 2001). There appears to be some dissociation in the neural networks implicated in the processing of emotional facial expressions; for example, studies have consistently reported involvement of the amygdala in fear (e.g., Breiter et al., 1996; Hariri et al., 2000; Morris, deBonis, & Dolan, 2002; Morris et al., 1998; Phillips et al., 1998, 2001; Whalen et al., 1998), the striatum in disgust (e.g., Calder, Keane, Manes, Antoun, & Young, 2000; GornoTempini et al., 2001; Phillips et al., 1998; Sprengelmeyer, Rausch, Eysel, & Przuntek, 1998; Sprengelmeyer et al., 1996), and the orbitofrontal cortex in happiness (e.g., Gorno-Tempini et al., 2001; ODoherty et al., 2003). As for stereotypes, the amygdalas response to fearful faces appears to be modulated by verbal processing of the stimulus (Hariri et al., 2000). Some imaging studies report amygdala activation for emotional facial expressions in general (e.g., Gur et al., 2002; Hariri et al., 2000; Iiadaka et al., 2001; Killgore & Yurgelun-Todd, 2001; Yang et al., 2002), although this is not a consistent finding. It is important to note that additional brain regions have been associated with emotional facial expressions, but these are less consistent across studies. Social judgment is closely related to social perception, especially as many studies require people to make evaluative judgments about others based on their appearance (particularly their faces). In a study of social judgment, relative to healthy controls, patients with bilateral damage to the amygdala rated people as looking more approachable and trustworthy (Adolphs, Tranel, & Damasio, 1998). Furthermore, impaired moral reasoning has been reported following damage to prefrontal cortex (Anderson et al., 1999; Eslinger et al., 1992). Consistent with these findings, fMRI studies have reported medial prefrontal cortex involvement in moral emotional processing (Greene, Sommerville, Nystrom, Darley, & Cohen, 2001; Moll et al., 2002) and correlations between activation of bilateral amygdala and judgments of trustworthiness of faces (Winston et al., 2002). The superior temporal sulcus has also been implicated in fMRI studies of trustworthiness judgments (Winston et al., 2002) and moral emotions (Moll et al., 2002). Taken together, these data suggest that an amygdalaprefrontal-temporal network is important for social perception and judgment. Much of this network is likely to be involved in processing the visual features and meaning of facial stimuli (Haxby et al., 2000). The role of the amygdala is likely to be evaluation of the emotional significance of a stimulus and the prefrontal cortex to be integration of this information and determination of an appropriate behavioral response.
finding of amygdala activation to out-group faces in a group of White subjects. They also extended the findings by demonstrating that amygdala and anterior cingulate activation correlated with performance on the race IAT but not with an explicit measure of racial stereotypes. Furthermore, these effects were not evident when famous Black faces were presented, suggesting that the brains response to faces reflects an implicit bias against a social out-group that may be modulated by experience or familiarity with certain members of the out-group. There is also evidence from fMRI that naming the stereotype label reduces the amygdalas response to stereotypic stimuli (see Ochsner & Lieberman, 2001), suggesting that amygdala activation may be modulated by verbal processing of stereotypic information. Although few in number, these neuropsychological and fMRI studies suggest that cognitive neuroscientific methods are useful in furthering our knowledge of social cognition beyond the localization of knowledge in the brain. For example, such research can also inform about the effects of experience on stereotypes (Phelps et al., 2000). These studies also point to the importance of ventromedial prefrontal cortex and amygdala in stereotype representation and processing. The involvement of these structures highlights an important point about social cognitive neuroscienceit is likely that each social process is not dependent on a unique neural network, rather, there are likely to be commonalities between social cognitive functions and already established cognitive functionsfor example, the amygdalas involvement in stereotypes, social behavior, and violence/ aggression is likely to reflect a common process of evaluating the emotional significance of a stimulus. Similarly, the emotional evaluation component of attitudes is likely to implicate this same process. A behavioral response must be associated with the evaluation to determine the response to the stimulusorbitofrontal and ventromedial prefrontal cortex may mediate the integration between the evaluation and the response, whether this be aggression or another type of social behavior. SOCIAL PERCEPTION AND JUDGMENT The majority of research on social perception has focused on face recognition. Neuropsychological and neuroimaging studies of face perception and recognition have consistently demonstrated the involvement of the fusiform gyrus (e.g., Gorno-Tempini & Price, 2001; Hariri, Bookheimer, & Mazziotta, 2000; Kesler/West et al., 2001; Tarr & Gauthier, 2000) and superior temporal sulcus (e.g., Haxby, Hoffman, & Gobbini, 2000; Perrett, Rolls, & Caan, 1982; Perrett et al., 1985). Furthermore, it has been suggested that although the fusiform gyrus may be central to the recognition of others faces, it is the
Wood / SOCIAL COGNITION MENTAL STATE REPRESENTATION Social behavior also requires understanding of other peoples behavior and emotional states; this requires the representation of others mental states and enables reasoning about and prediction of others behavior, a concept known as theory of mind (Premack & Woodruff, 1978). It has been proposed that the ability to represent the mental states of others is a function of the prefrontal cortex (Frith & Frith, 1999) and amygdala (Adolphs, Sears, & Piven, 2001; Baron-Cohen et al., 1999). Impairment on theory of mind tasks in patients with prefrontal cortex damage supports the proposal of prefrontal involvement in mental state representation (Channon & Crawford, 2000; Gregory et al., 2002; Happe, Malhi, & Checkley, 2001; Rowe, Bullock, Polkey, & Morris, 2001). Similar impairment has been reported in patients with amygdala damage (Fine, Lumsden, & Blair, 2001). Such theory of mind tasks generally require an inference to be made about another persons mental state based on information presented in either pictorial or verbal form. Autism is a developmental disorder characterized by impaired social communication and behavior (World Health Organization, 1992) and has been proposed to be the result of impaired theory of mind (Baron-Cohen, Leslie, & Frith, 1985; Leslie, 1987). A range of brain regions, including prefrontal and temporal, have been implicated in autism (see Table 2). In addition to these studies of individuals with autism, functional neuroimaging of healthy volunteers during performance of mental state tasks have implicated the right orbitofrontal cortex (Baron-Cohen et al., 1994). Other studies have implicated medial prefrontal cortex and temporal regions (Brunet, Sarfati, Hardy-Bayle, & Decety, 2000; Fletcher et al., 1995; Gallagher et al., 2000; Goel, Grafman, Sadato, & Hallett, 1995). The neuropsychological and imaging findings are supported by primate research. Social impairments resembling those exhibited by children with autism have been reported in young monkeys following lesions to the medial temporal lobe, including the amygdala (Bachevalier, 1991, 1994). As can be seen from Table 2, many neuroanatomical studies have reported reduced cerebellar volume in people with autism, relative to controls, with few functional imaging studies implicating this structure in mental state representation. Taken together, this converging evidence points to a role for prefrontal cortex and temporal regions in mental state representation, whereas the role of the cerebellum in the spectrum of symptoms evident in autism is not yet clear. Although the study of theory of mind has largely focused on humans, others have proposed its existence in nonhuman primates (Premack & Woodruff, 1978).
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Furthermore, some researchers have suggested that theory of mind, and hence mental state representation, in humans may be an adaptation of executive function (Russell, Saltmarsh, & Hill, 1999) or of other abilities such as shared attention and representation of goaldirected action (Frith & Frith, 1999). Similar arguments have also been leveled at observations of theory-of mindlike behavior in nonhuman primates, with suggestions that such behavior is the result of associative learning, inferential processing, and even coincidence (for a review of this debate and evidence, see Heyes, 1998). Some recent neuropsychological research is relevant to this issue of mental state representation in the brain. There are neurons in the prefrontal cortex of primates that fire when the monkey performs an action and also when the monkey observes another performing the same actionthese have been termed mirror neurons (Gallese, Fadiga, Fogassi, & Rizzolatti, 1996). Similar regions have been activated in humans when observing and performing actions (Grafton, Arbib, Fadiga, & Rizzolatti, 1996; Rizzolatti et al., 1996). It has been suggested that the role of mirror neurons in monkeys is to facilitate social understanding of other monkeys, that is, mental state representation (Gallese & Goldman, 1998). Furthermore, abnormal development of this mirror neuron system would lead to impaired formation of selfother representations and consequently to impairment of social behavior (Williams, Whiten, Suddendorf, & Perrett, 2001). In their review, Williams and colleagues argue that impairment to the mirror neuron system could lead to the constellation of social impairments evident in individuals with autism. In summary, there is some question as to whether theory of mind is a unique, dissociable ability to represent mental states or simply an ability that has arisen from other higher cognitive abilities, such as shared attention and representation of goal-directed actions. Irrespective of the mechanism, representation of others behavior and hence of the associated mental states seems likely to be mediated by the prefrontal cortex (Stuss, Gallup, & Alexander, 2001) with involvement of temporal regions, such as the amygdala (Bachevalier, 1994; Howard et al., 2000). The proposal of networks of regions supporting social cognition is perhaps most relevant to mental state representation. Many brain regions have been implicated in the complex tasks used to assess theory of mind. If one considers that different parts of a network might support different cognitive processes, then one can begin to address the complex question of how theory of mind is instantiated in the brain. Theory of mind is likely to involve recognition of an individuals emotional state and the integration of information from memory and other environmental stimuli to formulate an appropriate response to the person (uti-
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TABLE 2:
Studies Addressing the Brains Role in Mental State Representation Finding Brain Region(s) Implicated
Neuroanatomy Abell et al. (1999)
volume volume metabolism volume cell density volume volume Abnormal gyrification volume volume volume volume Hypoplasia
Hazneder et al. (1997) Howard et al. (2000) Bauman and Kemper (1985) Courchesne, Press, and YeungCourchesne (1993) Piven et al. (1990) Piven, Bailey, Ranson, and Arndt (1997) Courchesne, Yeung-Courchesne, Press, Heeselink, and Jernigan (1988) Hashimoto et al. (1995) Courchesne (1997); meta-analysis
Left amygdala, bilateral cerebellum, and temporal regions Left inferior frontal gyrus and occipitotemporal junction, right paracingulate sulcus Right anterior cingulate Bilateral amygdala Amygdala, hippocampus Cerebellum Parietal cortex, posterior prefrontal cortex, cerebellum Prefrontal cortex, parietal-occipital, and temporaloccipital regions Corpus callosum Cerebellum Cerebellum, brainstem Bilateral parietal Bilateral cerebellum, brainstem; no abnormalities at postmortem Prefrontal cortex Medial prefrontal cortex Medial and middle prefrontal cortex, thalamus Medial temporal lobe, basal ganglia Fronto-parietal regions Amygdala Left amygdalohipopocampal region, cerebellum Left superior temporal gyrus and peristriate visual cortex Right fusiform cortex
Neuroimaging Zilbovicius et al. (1995) Happe et al. (1996) Siegel, Nuechterlein, Abel, Wu, and Buchsbaum (1995)
blood flow aged 3-4 years, normal 3 years later blood flow during ToM task
metabolism/attentional task metabolism/attentional task Horwitz, Rumsey, Grady, and Rapoport (1988) functional associations Baron-Cohen et al. (1999) activation during appraisal of mood from eyes Critchley et al. (2000) activation during implicit processing of emotional faces activation during explicit processing of emotional faces activation during explicit processing of emotional faces
NOTE: Neuroanatomical studies of individuals with autism that have suggested abnormal development of the brain and comparisons of autistic and healthy volunteers using neuroimaging during the performance of mental state tasks are reported (increases and decreases are relative to controls).
lizing the amygdalas evaluation of the facial stimulus emotional significance and the orbitofrontal cortexs integrative properties). Additional cognitive processes are likely to be necessary, such as inferential reasoning and representation of the other persons behavior. Understanding of the neural instantiation of theory of mind is likely to require consideration of these cognitive processes in contributing to a network of regions that, when activated, enable inferences to be made about another individuals mental state, that is, theory of mind. SOCIAL DECISION MAKING Many patients with lesions of the prefrontal cortex demonstrate poor planning and decision making, together with socially inappropriate behavior (Fuster, 1997; Goel, Grafman, Tajik, Gana, & Danto, 1997; Masterman & Cummings, 1997; Sirigu et al., 1995).
Although these behavioral and cognitive problems are well established, they are difficult to assess in a controlled manner. One paradigm in particularthe Iowa gambling taskhas been used to assess real-world social decision making in a laboratory environment. In this task, subjects select cards from decks, each selection costs a predetermined amount of money, and each deck is associated with rewards and punishments (winning and losing money). The subjects goal is to make the most money while losing the least (Bechara, Damasio, Tranel, & Damasio, 1997). The appropriate strategy is to reject decks that are associated with high immediate rewards but long-term losses in favor of those associated with low immediate rewards but long-term gains. Patients with lesions of the ventromedial prefrontal cortex (relative to those with lesions of the dorsolateral prefrontal cortex and healthy subjects) or amygdala are impaired on this task, choosing decks that provide high
Wood / SOCIAL COGNITION immediate rewards with long-term losses (Bechara, Damasio, Damasio, & Lee, 1999; Bechara, Damasio, Tranel, & Anderson, 1998; Bechara, Tranel, & Damasio, 2000; Saver & Damasio, 1991). Anderson et al. (1999) reported cases of patients, one with bilateral ventromedial prefrontal cortex damage and the other with right dorsomedial prefrontal cortex damage, who showed an inability to learn to choose the appropriate strategy. These studies demonstrate that ventromedial prefrontal cortex is important in social decision making, with the amygdala being particularly important in evaluating the emotional significance of the reward (Bechara et al., 1999). These findings are consistent with those of the studies discussed above and, once more, highlight the need to consider social cognitive functions in light of other social cognitive researchI believe that it would be naive to consider the ventromedial prefrontal cortex amygdala network to be specific to social decision making. Rather, social decision making appears to utilize the same networks implicated in emotional evaluation of stimuli and the control of social behavioral responses. REPRESENTATION OF SOCIAL KNOWLEDGE Throughout this review, I have suggested that there may be networks underlying social behavior that are common to ostensibly different social cognitive functions. Taking this proposal as a starting point, I would like to propose that there may be knowledge representations that are stored in prefrontal networks that are common to many of the different functions outlined above. THE STRUCTURED EVENT COMPLEX FRAMEWORK Elsewhere, Grafman and I have proposed that a variety of complex behaviors may be controlled by representations that are stored in networks in the prefrontal cortex (see Grafman, 2002; Wood & Grafman, 2003). These are structured event complexes (SECs)stored representations of sequential event knowledge that have been described elsewhere as scripts or schemas (Casson, 1983; Eldridge, Barnard, & Bekerian, 1994; Schank & Abelson, 1977). SECs store information about event sequences and goals, and are composed around thematic activities. For example, an SEC of going out to dinner would include the events of making a reservation, reading the menu, ordering the food, and paying the bill. SECs are stored in networks in the prefrontal cortex, although they likely interact with knowledge representations in other brain regions, such as the basal ganglia and cerebellum.
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According to this viewpoint, SECs are the underlying knowledge representations that control social cognition, with social event knowledge implicating ventromedial prefrontal cortex (Wood & Grafman, 2003). One could argue that a special example of the SEC in action is the complexity of our social interactions. Given the suggestion that SECs control behavior, much of social behavior should be explicable with recourse to this framework. There is evidence that emotional and social event knowledge is stored in the prefrontal cortex (e.g., Partiot et al., 1995; Wood et al., 2003) and that this is distinct from semantic knowledge about the same events (Wood et al., 2003). The neurophysiological properties of the prefrontal cortex are also consistent with its role in event knowledge representationthe prefrontal cortex contains neurons that are capable of sustained firing (Bodner, Kroger, & Fuster, 1996; Fuster & Alexander, 1971; Kojima & Goldman-Rakic, 1982; Levy & Goldman-Rakic, 2000) as well as neurons that respond to observed action sequences (Gallese et al., 1996; Gallese & Goldman, 1998; Rizzolatti et al., 1996). There are many aspects of social cognition that need to be accounted for if the SEC framework is to be of use in understanding representation of social knowledge. As the SEC framework has recently been described in detail (Wood & Grafman, 2003), I will now consider the relationship between SECs and attitudes, aggression, mental state representation, and relationship development. The following discussion is based on the review of the literature presented above. SECS AND ATTITUDES There may be several routes from a stimulus to its associated behavior and, in addition to SECs, there may be other types of knowledge representation that can influence social behavior. One such representation type is attitudesthese provide a fast route from a stimulus to a behavior. Attitudes, stereotypes, and prejudice are closely related concepts (Dovidio et al., 2002; Lowery et al., 2001). I consider stereotypes to be a specialized instance of an attitude and prejudice to be the affect associated with negative stereotypic beliefs about a particular social group. Therefore, the ideas regarding attitude representations that are presented below also apply to stereotypes and prejudice. Attitudes consist of representations of the attitudeobject with its associated evaluation and behavioral response (Pratkanis, 1989). The presentation of an attitudeobject will activate semantic information about the attitude-object in addition to attitude-based evaluations and responses. The evaluation may be simple, such as whether the attitude-object is good or bad, or complex, such as whether the individual is for or against the ideas that the attitude-object represents. In the simple case,
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the good/bad emotional evaluation may be considered similar to Damasios (1995, 1998) somatic markers. In these instances, the evaluation would be an emotional memory of a prior encounter with the attitude-object, although the individual would not need to remember the encounter consciously. Attitudes that are associated with simple evaluations can be considered primitive components of SECs and, therefore, will be represented developmentally earlier than SECs. As the SECs develop, these provide an alternative but slower route from object to behavior. However, the behavior accessed by the SEC route might differ from that rapidly accessed via an attitude; for example, the SEC route is likely to lead to reflective, socially appropriate behavior, whereas the attitude route may not. SEC and attitude representations may be activated by the same stimulus. If the behaviors associated with each representation differ, then there will be competition between them for the behavioral response to the situation (see Figure 1). For example, if you dislike a coworker, then you may be polite (socially appropriate, SEC route) or rude (socially inappropriate, attitude route) in your interactions with that person. Similarly, SECs that occur during a relatively long time period to achieve a long-term goal may conflict with attitude-based behaviors to achieve a short-term, but different, goal. These conflicts must somehow be resolved. It seems plausible that this competition is resolved by lateral inhibition of the competing representations. In addition to conflicting behaviors arising from competing attitudes, there is the possibility of conflict between implicit and explicit attitudesthe research reviewed above shows that implicitly assessed stereotypes often differ from those that are explicitly assessed. When considering this, one must take into account the potential strategy of a subject in reporting politically correct attitudes while holding very different, explicitly available, attitudes that are not expressed to an experimenter. If this is the case, then consciously accessible attitudes are unlikely to be a good predictor of real-world behavior, as this will be determined by the individuals unreported attitudes that are more accurately assessed using implicit measures. This issue aside, it may the case that several conflicting attitudes to the same attitudeobject exist. As in the case for competing knowledge representations (e.g., SECs and attitudes), such conflicts are likely to be resolved by inhibition of competing attitude representationsthe winner of the competition will be determined by factors such as attitude strength and associative priming resulting from current behavior and goals. Based on the literature discussed earlier, I propose that attitude representations implicate distributed networks that represent the attitude-object, its evaluations,
STIMULUS Attitude-object Person
Evaluation
Semantic Knowledge Activation
SEC Activation
Attitude-Based Response
SEC-Based Response
Observed Response
Figure 1: Cognitive Structure of Attitude Representations NOTE: Presentation of an attitude-object (attitude) or person (stereotype) leads to activation of stored evaluations (attitude-based route), semantic knowledge, and structured event complex (SEC) knowledge (SEC-based route). The evaluations and SECs activate their associated responses and the semantic knowledge influences activation of the components of both routes. In addition, the attitude- and SEC-based responses compete with each other. The observed response or behavior is the winner of this competition.
and behavioral responses. The amygdala is likely to be implicated in emotional evaluations of the attitudeobject (as discussed earlier). More complex evaluations, such as those based on the individuals beliefs or value system, are likely to require anterior prefrontal cortex regions that have been implicated in evaluative judgment (Zysset, Huber, Ferstl, & von Cramon, 2002). The representation of the attitude-object itself is likely to implicate the left inferior prefrontal cortex (Demb et al., 1995; Gabrieli, Poldrack, & Desmond, 1998; Martin & Chao, 2001) and temporoparietal regions associated with semantic processing (Castillo et al., 2001; Pinel, Dehaene, Riviere, & LeBihan, 2001; Vandenburghe, Price, Wise, Josephs, & Frackowiak, 1996). The role of the orbitofrontal or ventromedial prefrontal cortex is likely to reflect integration of the different knowledge and evaluative information to prime a behavioral response (or set of behavioral responses) to the attitudeobject. The behavioral responses associated with attitudes may implicate networks of regions in the dorsolateral prefrontal and premotor cortices. The strength of activation of the regions within the network is likely to vary depending on the type of attitude; for example, simple attitudes associated with approach or withdrawal behaviors will not activate the anterior prefrontal cortex, because a complex evaluation is unlikely to be necessary. SECS AND AGGRESSION Much social cognitive neuroscientific research has addressed the relationship between aggression/violence and the brain. There is also extensive research into
Wood / SOCIAL COGNITION aggression in the social psychology literature and social psychology researchers have formulated theories to explain the development and maintenance of aggressive behavior. Several of these theories describe a central role for aggressive scripts or schemas (Anderson & Bushman, 2002; Crick & Dodge, 1994; Guerra, Nucci, & Huesmann, 1994; Huesmann & Guerra, 1997). Such scripts have been suggested to control social behavior in general, not simply aggression (Eron, 1994). According to Guerra and colleagues (1994), scripts are cognitive representations of sequences of events which occur in well-known situations (p. 18). These frameworks are highly compatible with the SEC framework and, as such, I would consider these aggressive scripts to be frequently performed SECs. In their General Aggression model, Anderson and Bushman (2002) propose three knowledge types that are implicated in aggressive behavior perceptual schemata (e.g., knowledge about social events), person schemata (e.g., beliefs about a group of people), and behavioral scripts. Within such a framework, I would consider the perceptual schemata to comprise semantic knowledge, person schemata to comprise attitudes and stereotypes, and behavioral scripts to comprise SECs. Taking these models as a general framework, therefore, I propose that there may be a subset of SECs that store event sequences that are specifically related to aggressive behavior. These may develop as a result of an individuals experience and their activation will be influenced by other knowledge representations, such as cultural rules constraining appropriate social behavior. The presence of an individual or situation that elicits an aggressive response will activate the aggression-related SEC and consequently the aggressive behavior (see Figure 2). This aggressive response may, however, be modulated by social rules or other contextual information. If similar situations frequently result in aggressive behavior, the associated behaviors may become activated relatively automatically in particular situations or in interactions with particular people. This may lead to aggressive behavior being elicited without necessarily accessing the SEC and hence without modulation by context or social rules (see Figure 2). The literature reviewed earlier points to a role for orbitofrontal and medial prefrontal cortex regions in aggressive behavior. Therefore, I propose that these regions may be particularly important in the access to SEC representations of aggression-related events and behavior. Given the role of the orbitofrontal cortex in integrating information from emotion, memory, and the environment, damage to this region is likely to result in impaired integration of this information. This might limit the degree of modulation based on, for example, social rules and result in an increase in aggressive behav-
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SECSEC- BASED ROUTE
Stimulus Person Situation
AUTOMATIC ROUTE
Stimulus Person Situation
Social RuleBased SECs
Social RuleBased SECs
AggressionRelated SEC
AggressionRelated SEC
(Aggressive)
Response
Aggressive Response
Figure 2: Routes to Aggressive Behavior NOTE: In the route based on the structured event complex (SEC), an encounter with a person or situation leads to activation of social rule based and aggression-related SECs, which in turn may lead to an aggressive behavior. In the automatic route, an encounter that has frequently resulted in aggression leads to aggressive behavior without mediation by SEC representations.
ior. Alternatively, aggressive individuals might have similar access to aggression-related SECs as nonaggressive people, but have impaired access to the social rules themselves. Nonaggressive resolutions to conflict may require the successful competition of behavioral alternatives to aggression. An impairment in this ability of nonaggressive SECs to inhibit the aggressive SECs effectively would also lead to aggression. This viewpoint is consistent with the observed disinhibitory effects of orbitofrontal cortex damage (Fuster, 1997; Masterman & Cummings, 1997). SECS AND MENTAL STATE REPRESENTATION An important component of social understanding is mental state representation. Despite the ongoing debate about whether a theory of mind module really exists, the ability to represent the mental states of others must be considered in any theoretical framework of social cognition. As discussed above, theory of mind is likely to involve recognition of an individuals emotional state, integration of information from memory and other environmental stimuli, inferential reasoning, representation of the other persons behavior, and formulation of an appropriate response to the person. Understanding of the neural instantiation of theory of mind is likely to require consideration of these cognitive processes in contributing to a distributed network. Activation of a behavioral sequence by observation of an individuals behavior would lead to activation of associated knowledge representations (see Figure 3). These may include stored knowledge about behavioral responses that are associated with that individual as well as your own past experiences and emotional states. This may lead to priming of other representations of behavior or emotional states, and would enable the future behavior of the observed individual to be predicted.
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BEHAVIORAL AND COGNITIVE NEUROSCIENCE REVIEWS sentation (Williams et al., 2001). If the abnormal development was such that the system was unable to represent others actions but was able to represent the actions of self, then the individuals ability to carry out activitybased behaviors would be intact but their ability to understand the behavior of others would be impaired. Similarly, impairment of other aspects of the network described above might also result in deficits on mental state tasks. SECS AND RELATIONSHIP DEVELOPMENT
SECs Related to Observed Behavior Memories of Emotional States
Observed Behavior
Observed Emotional State
Activation of SEC for the Observed Behavior
Knowledge of the Observed Person
Episodic Memories
Mental State Representation understanding of observed behavior prediction of future behavior understanding of observed emotional states
Figure 3: Cognitive Structure of Mental State Representation NOTE: The observation of a behavior or emotional state activates the appropriate structured event complex (SEC), which in turn activates other knowledge structuresthese knowledge structures will also include attitudinal and stereotypic knowledge. Activation of these knowledge representations constitutes the mental state representation and enables inferences to be made about the observed persons present and future behavior as well as their motivation. The observation of an individuals emotional state also directly activates emotional knowledge structures and enables inferences to be made about the mental state that underlies the persons current emotional response.
Under such a viewpoint, a network of regions would underlie theory of mind, with inferential reasoning based on integrated information from memory (hippocampus; see Fortin, Agster, & Eichenbaum, 2002; Nestor, Graham, Bozeat, Simons, & Hodges, 2002; Packard & Cahill, 2001), emotional evaluation of the person and situation (amygdala; see Buchanan, Denburg, Tranel, & Adolphs, 2001; Ghashghaei & Barbas, 2002; Zald, 2003), and social and nonsocial SECs (dorsolateral and ventromedial prefrontal cortex; see Wood & Grafman, 2003). The distributed network is not unique to theory of mind; rather, theory of mind is a result of the contemporaneous activation of multiple overlapping networks providing access to all of the necessary information. The ability of the primate prefrontal cortex to represent the actions of others has been demonstrated in mirror neurons (Gallese et al., 1996), and it is possible that these representations have evolved to be more complex in humans, such that similar neurons or networks of neurons are capable of representing relatively complex sequences of behavior. Like primate mirror neurons, these networks of neurons in humans would respond to performance and observation of behavioral sequences. Abnormal development of the mirror neuron system in humans may lead to impairment in mental state repre-
Finally, a fundamental component of social behavior is interpersonal relationships. The development of relationships has been proposed to be a function of memory and, in particular, of procedural learning. It has been proposed that knowledge about an individual prior to meeting them is semantic (Grigsby & Stevens, 2002). Therefore, the initial representation you have on meeting someone for the first time is a function of the general context, representations that you already hold of other people, and stereotypes. Grigsby and Stevens (2002) have proposed that these initial representations are modified by experience to incorporate new information about the person. The resulting experience-based representations include automatically activated behaviors that are shared between the people forming the relationshipsuch behaviors will be routine and will generally occur outside of awareness. Effectively, we develop relationship-specific repertoires of behaviors. These ideas are consistent with the SEC framework, such that the behaviors are stored in SECs and presentation of the person will prime the SECs and consequently lead to performance of the appropriate behaviors. It is possible that we may develop repertoires of behavior that are situation- and group-specific, that is, that a particular set of behaviors will be activated when in certain contexts or with certain types of people (e.g., work colleagues vs. family). Impairment in the ability to access or retrieve the SEC knowledge may then lead to behavior that is inappropriate either to the situation or the person with whom the individual is interacting; the affected person would appear to be different or to have undergone a change in personality. I propose that these relationshipspecific behaviors are a subset of SECs. Given that normal social interactions are disrupted following damage to the orbitofrontal rather than dorsolateral prefrontal cortex (Anderson et al., 1999; Blumer & Benson, 1975; Eslinger et al., 1992; Masterman & Cummings, 1997), those social SECs that represent relationship-specific behaviors are likely to involve the orbitofrontal and ventromedial prefrontal cortex, whereas more generic, activity-based SECs will implicate the dorsolateral prefrontal cortex (Wood & Grafman, 2003).
Wood / SOCIAL COGNITION CONCLUSIONS I have reviewed the extant published literature that explores the relationship between social cognitive neuroscience and the brain. I have also introduced the SEC framework in the context of social cognition. I have argued that the prefrontal cortex is important in the representation of social knowledge and, consequently, in the control of social behavior. However, I acknowledge that other brain regions, such as amygdala and temporal cortex, are also important in social cognition. In considering the role of the prefrontal cortex in social cognition, I have emphasized the importance of common networks of regions that subserve social knowledge and the processing of social information. With the rapidly increasing interest in the relationship between social cognition and the brain, researchers should be careful to ensure that each social concept is not considered a new type of process or representationthis can be achieved by evaluating its similarity to established cognitive processes and representations. Although there is likely to be more than one route from a stimulus to a behavior, I believe that the SEC framework provides a useful approach to understanding and exploring social cognition as well as a degree of cohesion between the different areas of research. Finally, the SEC approach provides a useful framework for the systematic study of how the brain, particularly the prefrontal cortex, controls social behavior.
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10.1177/1534582303253625 BEHAVIORAL AND COGNITIVE NEUROSCIENCE REVIEWS Wood / SOCIAL COGNITION