the role of the human prefrontal cortex in social …...the role of implicit and explicit processes...

NE33CH14-Grafman ARI 14 May 2010 18:17

The Role of the HumanPrefrontal Cortexin Social Cognitionand Moral Judgment∗

Chad E. Forbes1 and Jordan Grafman2

1Imaging Sciences Training Program, Radiology and Imaging Sciences, Clinical Center andNational Institute of Biomedical Imaging and Bioengineering; Cognitive NeuroscienceSection, National Institute of Neurological Disorders and Stroke, National Institutes ofHealth, Bethesda, Maryland 20892; email: [email protected] Neuroscience Section, National Institute of Neurological Disorders and Stroke,National Institutes of Health, Bethesda, Maryland 20892; email: [email protected]

Annu. Rev. Neurosci. 2010. 33:299–324

First published online as a Review in Advance onMarch 29, 2010

The Annual Review of Neuroscience is online atneuro.annualreviews.org

This article’s doi:10.1146/annurev-neuro-060909-153230

Copyright c© 2010 by Annual Reviews.All rights reserved

0147-006X/10/0721-0299$20.00

∗The U.S. Government has the right to retain anonexclusive, royalty-free license in and to anycopyright covering this paper.

Key Words

implicit and explicit social cognitive and moral judgment processing,frontal lobes, neural function, social cognitive neuroscience,structured event complex theory

Abstract

Results from functional magnetic resonance imaging and lesion studiesindicate that the prefrontal cortex (PFC) is essential for successful nav-igation through a complex social world inundated with intricate normsand moral values. This review examines regions of the PFC that arecritical for implicit and explicit social cognitive and moral judgmentprocessing. Considerable overlap between regions active when indi-viduals engage in social cognition or assess moral appropriateness ofbehaviors is evident, underscoring the similarity between social cogni-tive and moral judgment processes in general. Findings are interpretedwithin the framework of structured event complex theory, providing abroad organizing perspective for how activity in PFC neural networksfacilitates social cognition and moral judgment. We emphasize the dy-namic flexibility in neural circuits involved in both implicit and explicitprocessing and discuss the likelihood that neural regions thought touniquely underlie both processes heavily interact in response to differ-ent contextual primes.

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PFC: prefrontalcortex

Contents

INTRODUCTION . . . . . . . . . . . . . . . . . . 300A BRIEF PRIMER ON

SOCIAL COGNITION . . . . . . . . . . . 301Social Perceptual Processes . . . . . . . . . 301Attributional Processes . . . . . . . . . . . . . 301Social Categorization Processes . . . . . 302

THE ROLE OF IMPLICITAND EXPLICIT PROCESSESIN SOCIAL COGNITION. . . . . . . . 302

A BRIEF PRIMER ONMORAL JUDGMENT . . . . . . . . . . . . 304Dual Process and Interactionist

Models of Moral Judgment . . . . . . 304STRUCTURE AND FUNCTION

OF THE PFC . . . . . . . . . . . . . . . . . . . . . 306PFC REGIONS CRITICAL

FOR SOCIAL COGNITIONAND MORAL JUDGMENTS. . . . . 307The Role of the PFC in Social

Perceptual Processes . . . . . . . . . . . . 308The Role of the PFC in

Attributional Processes . . . . . . . . . . 308The Role of the PFC in Social

Categorization Processes . . . . . . . . 309The PFC’s Role in Moral Judgment

Processes . . . . . . . . . . . . . . . . . . . . . . . 310STRUCTURED EVENT COMPLEX

THEORY DESCRIBES THEPFC’S ROLE IN SOCIALCOGNITION AND MORALJUDGMENT . . . . . . . . . . . . . . . . . . . . . 311SECs Are Composed of

Multiple Dimensions . . . . . . . . . . . . 312SUMMARY AND

CONCLUSIONS . . . . . . . . . . . . . . . . . 314

INTRODUCTION

Take a second to recall a recent interactionyou had with someone you met for the firsttime at a social event. Hopefully the conver-sation went swimmingly and you devoted mostof your attention to the verbal interaction. Ifprobed, however, you could probably recall, in

addition to the information learned verbally,the person’s ethnicity, whether he/she was sim-ilar to you, and your impressions of which typeof person you thought they were in general (andsubsequently whether you liked them). Youprobably even processed all of this informationwithin a few seconds. Thus within a matter ofseconds, you encoded identifiable informationabout the person, predicted what would be bestto say to facilitate a pleasant interaction, andformed an impression of him/her, all while yourprefrontal cortex (PFC) simultaneously moni-tored and evaluated neural information fromyour five modalities, coordinated movementsand actions, and kept you focused on adher-ing to social or personally relevant norms. Yetyou likely processed such information with narya thought, largely because your PFC can en-gage in most of the aforementioned functionsoutside of your conscious awareness. With thisscenario in mind, you can begin to appreciatethe complexity of interactions between multi-ple cognitive and sensory processes originatingfrom neural regions both within and outside thePFC that provide the foundation for complexsocial behavior and moral judgment.

The PFC is anatomically organized in away that allows for information from all fivesenses to be integrated [see the discussion ofBanyas (1999), Fuster (1997) below]. The PFCis also critical for higher order functions suchas focusing attention on goal-relevant stimuliand inhibiting distractions (Badre & Wagner2004, Botvinick et al. 2004, Dolcos et al. 2007,MacDonald et al. 2000, Milham et al. 2001,Miller & D’Esposito 2005), while evaluatingand interpreting information within the contextof past experiences (Adolphs 1999, Damasio1994, Rolls & Grabenhorst 2008), storing se-mantic information about the self and others( Johnson et al. 2002, Kelley et al. 2002, Schmitzet al. 2004), and temporally organizing actionsor planned behaviors (A. Barbey, M. Koenigs,and J. Grafman, under review; Fuster 1997,Wager & Smith 2003). Given all the cognitivefunctions for which the PFC is necessary, it isnot surprising that the PFC makes higher-ordercognitive functions such as social cognition and

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moral judgment possible. As we describe here,the PFC processes all these functions at varyingprocessing speeds, e.g., impressions and judg-ments of others and one’s surroundings can bereached within milliseconds (termed implicit,fast, or automatic processing) or derived overlonger periods of time (termed explicit, slow,or controlled processing).

Below, we review literature linking PFCfunctions to those of social cognition and moraljudgment. We begin with a general overviewof social cognition and moral judgment andhighlight how the PFC is organized to enablesuch higher-order cognitive processes and theregions they require most. The existing litera-ture is then interpreted within the framework ofthe structured event complex theory (Grafman2002, Wood & Grafman 2003), which offers abroad organizing perspective for how activityin the PFC neural network provides the impe-tus for social cognition and moral judgment.We highlight how PFC activity underlying theimplicit and explicit processes necessary for so-cial cognition and moral judgment varies in dif-ferent situational contexts, i.e., how situationalcues change the way stimuli are processed psy-chologically and neurologically.

A BRIEF PRIMER ONSOCIAL COGNITION

Social cognition refers to the processes bywhich we make sense of ourselves, the socialenvironment or culture in which we live, andthe people around us (Fiske 1993, Macrae &Bodenhausen 2000). Although the term socialcognition can encompass any cognitive pro-cess engaged to understand and interpret theself, others, and the self-in-relation-to-otherswithin the social environment, it can be bro-ken down into several primary categories thathave both implicit and explicit components.These categories include social perceptual pro-cesses, attributional processes, and social cate-gorization processes that use schemas or stereo-types. Research highlighting each category isdiscussed in turn.

Social Perceptual Processes

Research on social perception includes howone processes and identifies faces and categor-ical information such as gender and ethnicity,mimics others on a basic level, and interpretsothers’ movements and intentions. Giventhat humans can process social markers onthe order of milliseconds (Cunningham et al.2004a), engage different neural systems in theprocessing of inanimate objects compared withpeople (Mitchell et al. 2002), and appear tobe uniquely sensitive to human faces (Kouideret al. 2009), one can presume that humansare innately sensitive to social information(Adolphs 1999, Van Overwalle 2009). Usingelectroencephalographic (EEG) methodology,research has documented that faces can be con-sciously distinguished from non-face stimuliby 170 ms, and ethnic in-group and out-groupfaces are differentiated by 250 ms (Ito et al.2004). Distinctions between ethnicity andfacial recognition can occur as quickly as 30–50 ms postpresentation in neural regions suchas the amygdala and middle fusiform gyrus aswell (Cunningham et al. 2004a, Kouider et al.2009). The ability to process social informationrapidly and with little other information pro-vides individuals with a perceptual blueprint orschema that allows them to identify and seek outgoal-relevant stimuli and avoid potentially dan-gerous stimuli in a remarkably efficient manner.

Attributional Processes

Attributional processes refer to an innate driveto explain and understand others’ actions andbehaviors as well as our own (Gilbert &Malone 1995). Attributional processes arehighly contingent on the perspective of the per-ceiver, i.e., whether one is interpreting others’actions from their own perspective or from thatof another (Storms 1973). The default mode isfor individuals to evaluate others’ actions fromtheir own perspective, which typically leads toa fundamental attribution error, i.e., the ten-dency for people to attribute others’ behav-iors to trait characteristics and attribute their

www.annualreviews.org • PFC, Social Cognition, and Moral Judgment 301

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TOM: theory of mind

own behavior to situational factors (Gilbert &Malone 1995, Ross 1977). Individuals are capa-ble of taking the perspective of others, however(e.g., “walk a mile in another’s shoes”), whichhas formed the basis for the perspective-takingliterature in social psychology and a widely in-vestigated theory in the cognitive neuroscienceliterature termed theory of mind (TOM). TOMrefers to the general ability to infer the thoughtsand beliefs of one’s self and others (Carrington& Bailey 2009). Although the mechanisms in-volved in TOM are still unknown, i.e., whetherit occurs via inferring others’ intentions andbeliefs on the basis of observed behaviors (the“theory” theory; Gallese & Goldman 1998) orvia inferring others’ intentions and beliefs bysimulating how the observer might feel in sim-ilar situations (simulation theory; Gallese &Goldman 1998, Ramnani & Miall 2004), gen-eral consensus indicates that TOM is the funda-mental basis for social interactions (for a review,see Carrington & Bailey 2009). As a whole, at-tributional processes serve as the foundationfor developing self-knowledge (e.g., via self-perceptual processes; Bem 1967) in relation toothers in our world and rely heavily on executiveresources, and subsequently PFC resources, ingeneral (Saxe et al. 2006).

Social Categorization Processes

Another line of social cognitive research ex-amines how categorization processes such asschema and stereotype activation affect indi-viduals’ perception and information processing.In regard to social cognition, schemas repre-sent a cognitive framework for social categoriesand the associations among them (Fiske &Taylor 1991). Stereotypes, defined as a generalbelief one has toward different groups or cogni-tive objects (Allport 1954, Fiske 1998, Macraeet al. 1994), can be considered a specific typeof schema. Although schemas and stereotypesmake information processing dramaticallymore efficient (Macrae et al. 1994), they comewith a price. For example, research finds thatexposure to racial out-group members makesnegative stereotypes immediately cognitively

accessible (termed automatic stereotype acti-vation; Devine 1989). Once activated, stereo-types can be cognitively taxing to downregu-late or suppress (C. Forbes and T. Schmader,under review; Richeson et al. 2003, Schmaderet al. 2008), can bias nonverbal behaviors(Dovidio et al. 2002), and can negatively bias ex-plicit perceptions toward out-group membersbehaving ambiguously (Rudman & Lee 2002),all seemingly unbeknownst to the perceiver.Thus although stereotypes facilitate the pro-cessing of information that is consistent withexpectations, they also increase the incidence ofjudgment errors when information contradictsexpectations and biases perceptions to a greaterextent than the stereotyping individual assumes.

THE ROLE OF IMPLICITAND EXPLICIT PROCESSESIN SOCIAL COGNITION

The field of social cognition has devoted mucheffort to understand better the differential ef-fects of implicit and explicit processes on theaforementioned cognitive processes. Implicitprocesses unfold rapidly, require little cogni-tive effort, occur outside individuals’ consciousawareness, and involve posterior cortical andsubcortical regions of the brain (Amodio &Devine 2006, Cunningham & Zelazo 2007). Inaddition to face recognition and stereotype ac-tivation, other implicit processes include condi-tioned, evaluative associations between ideas orcategories and stimuli that fit those categories(termed implicit attitudes; Fazio & Olson 2003,Greenwald & Banaji 1995) and self-serving bi-ases. Conversely, explicit processes are deliber-ative, cognitively taxing, consciously accessible,and largely rely on the PFC (Amodio & Devine2006, Cunningham & Zelazo 2007). Examplesof these processes include deliberative eval-uations of objects (termed explicit attitudes;Oskamp & Schultz 2005), introspective percep-tions of self and others, and attributions.

Although these processes have historicallybeen treated as distinct from one another,given ambiguities in behavioral findings andthe nature of neuroanatomical connections


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(e.g., extensive reciprocal connections betweenPFC and subcortical regions in the brain; seeFigure 1), recent perspectives argue that im-plicit and explicit processes may interact at allstages of cognitive processing (Cunningham& Johnson 2007, Devine & Sharp 2009; C.Forbes, C. Cox, T. Schmader, and L. Ryan,under review). Failure to identify a unitary,rapidly unfolding interaction between implicitand explicit processes could be due largely tomethodological constraints and the nature ofthe issue being investigated (Devine & Sharp2009). Pertaining to the nature of issues beingassessed, implicit attitudes can be highly predic-tive of explicit attitudes, but implicit attitudescan also account for variance that is unexplainedby explicit attitudes when researchers assess so-cially sensitive subjects such as race or gender(Cunningham et al. 2004b, Devine 1989,Greenwald et al. 2009, Nosek et al. 2002).

For instance, women often readily expressdislike toward the math domain and can quicklypair negative words with math-related words onan implicit associations test (a common measureused to assess implicit attitudes; Nosek et al.2002), suggesting they have a negative implicitattitude toward math as well (Nosek et al. 2002).When asking white individuals about theirattitudes toward black individuals, however, al-though they explicitly report positive attitudestoward blacks, they often demonstrate a nega-tive implicit attitude toward them on the im-plicit associations test (Greenwald et al. 2009,Greenwald & Banaji 1995). These negative im-plicit associations in turn can predict decreasedmath effort in women and negative nonverbalbehaviors toward blacks during interracial in-teractions among other things (Dovidio et al.2002; C. Forbes & T. Schmader, under review).

In the case of women’s attitudes towardmath, attitudes resulting from implicit and ex-plicit processes appear to represent two endson a continuum (i.e., faster to slower) that canbe generated either rapidly or slowly and re-sult in a unitary attitude. In the example ofwhites’ attitudes toward blacks, attitudes wouldappear to result from two separate systems (i.e.,faster versus slower) that engender two distinct

ExplicitFrontopolar

cortex

Medial PFC

Orbitofrontalcortex

Anteriorcingulate

cortex

Amygdala

Ventrolateral PFC

Dorsolateral PFC

Implicit

Figure 1Diagram of direct neural connectivity between regions critical for implicit andexplicit social cognitive and moral judgment processes. Solid bidirectionalarrows denote direct reciprocal neural connectivity between two regions withina given processing system, i.e., implicit or explicit processing. Dashedbidirectional arrows represent direct reciprocal connectivity between tworegions typically involved in either implicit or explicit processing. Blue circlesdenote neural regions that are typically involved in more implicit cognitiveprocessing. Red circles signify neural regions that are typically involved inmore explicit cognitive processing. These regions are not exclusively involvedin implicit or explicit processing however. This conjecture is represented by thethree shaded boxes and large arrow on the right. The lightest gray boxrepresents neural regions, namely the amygdala here for the sake of simplicity,that are largely involved in implicit processes. Likewise, the darkest gray boxhighlights neural regions largely involved in explicit processes. The mediumshaded box represents regions that are recruited during both implicit andexplicit processing. PFC, prefrontal cortex.

attitudes. However, it is also possible that thelatter scenario is reflective of an individual’sability to produce a rapid, visceral evaluationof a stimulus that can then be assessed within agiven context for appropriateness and be down-regulated, suppressed, or altered accordingly.

This interpretation would suggest that theimplicit attitude and explicit attitude are uni-tary, but situational demands (e.g., the desireto be politically correct in an interaction with anew acquaintance) necessitate alteration of the


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fMRI: functionalmagnetic resonanceimaging

overt expression of the explicit attitude, mak-ing them appear unique accordingly. In thisinstance, implicit and explicit processes likelyinteracted to engender the appearance of twodistinct attitudes; however, given that these in-teractions can reach fruition within 500 ms,one can appreciate the difficulty inherent inexamining them effectively [for detailed the-oretical examinations of the conditions thatmay elicit implicit and explicit attitude overlapor differentiation, see Fazio & Olson (2003),Gawronski & Bodenhausen (2006), Petty et al.(2007), Wilson et al. (2000)]. Advances in EEGand functional magnetic resonance imaging(fMRI) methodologies, e.g., combining the ex-ceptional temporal and spatial advantages ofeach respectively, could soon pave the way forsuccessful assessments of these interactions.

The examination of implicit and explicitprocesses is not unique to social cognition.Given that visceral, emotional responses tostimuli can also be considered an implicit re-sponse, in recent years investigators have de-voted much attention to understanding howemotional reactions can bias otherwise rationalperceptions when people evaluate the appro-priateness of others’ behaviors. As you mightexpect, attributional products of implicit andexplicit processes also play a prominent role inour next topic: the field of moral judgment.

A BRIEF PRIMER ONMORAL JUDGMENT

Moral judgments are broadly defined as evalu-ative judgments of the appropriateness of one’sbehavior within the context of socialized per-ceptions of right and wrong (Moll et al. 2005).Table 1 provides an overview of traditionalphilosophical dilemmas as well as more recent,real-world examples that have been used to as-sess moral judgment processes in the literature.The study of morality and subsequent moraljudgments has a long history in philosophy andmore recently psychology, and as opposed tothe fundamental top-down and bottom-up pro-cesses the field of social cognition usually tack-les, moral judgments have long been thought

to rely solely on controlled, rational, and log-ical thought processes (Kohlberg 1969, Turiel1983). Given the likely evolutionary origins ofmorality and the degree to which it permeatesall facets of society and cognition from earlychildhood on, the idea that moral judgments areonly a product of controlled cognitive process-ing has been convincingly challenged (Haidt2001, Moll et al. 2005, Schulkin 2000).

More recent research on moral judgmentshas begun to incorporate the likelihood thatmoral judgments have an emotional componentto them as well. On one end of the spectrum,some researchers have argued that moral judg-ments are largely direct products of intuitiveor implicit emotional processes (Haidt 2001,Nichols 2002, van den Bos 2003). According toHaidt’s social intuitionist model (Haidt 2001),moral behavior is predicated largely on implicitmoral emotions such as guilt or compassion thatcompete and interact to guide morality outsideof conscious awareness. These moral emotionswere likely essential to our survival and evo-lution as a species and thus influence our per-ceptions and thoughts at all levels of cognitiveprocessing in the form of “moral intuitions”(Moll et al. 2003). Controlled cognitive pro-cesses are likely to play a role in moral judg-ment only when situational demands necessi-tate them, e.g., situations that engender moraldilemmas (Moll et al. 2003). Although theo-ries such as Haidt’s rightfully identify a criti-cal role for implicit emotional processes, theydeemphasize the importance of explicit cogni-tive processing. As such, it is more difficult toexplain findings demonstrating the importanceof explicit processes, and the integral role thatthe PFC appears to play, in moral judgmentsoverall (discussed below).

Dual Process and InteractionistModels of Moral Judgment

To bridge the gap between moral judgmentsand implicit and explicit processes, other re-searchers have incorporated the concept of adual-process theory, positing that moral judg-ments can be derived via implicit, emotional


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Table 1 A sample of traditional philosophically based (numbers 1 and 2; e.g., Greene et al. 2001, Koenigs et al. 2007) andmore pragmatic (numbers 3, 4, and 5; Knutson et al. 2010) vignettes used to assess moral judgment processes

Type of moral judgmentassessed Typical examples Moral judgment1. Impersonal moraldilemmas

The Standard Trolley dilemma: You are at the wheelof a runaway trolley quickly approaching a fork inthe tracks. On the tracks extending to the left is agroup of five railway workmen. On the tracksextending to the right is a single railway workman.If you do nothing the trolley will proceed to the left,causing the deaths of the five workmen. The onlyway to avoid the deaths of these workmen is to hit aswitch on your dashboard that will cause the trolleyto proceed to the right, causing the death of thesingle workman.

Is it appropriate for you to hit the switch toavoid the deaths of the five workmen? Note:The decision to hit the switch is consideredthe utilitarian choice. The decison to not hitthe switch is the non-utilitarian ordeontological choice.

2. Personal moraldilemmas

The Crying Baby dilemma: Enemy soldiers havetaken over your village. They have orders to kill allremaining civilians. You and some of yourtownspeople have sought refuge in the cellar of alarge house. Outside you hear the voices of soldierswho have come to search the house for valuables.Your baby begins to cry loudly. You cover his mouthto block the sound. If you remove your hand fromhis mouth his crying will summon the attention ofthe soldiers who will kill you, your child, and theothers hiding out in the cellar. To save yourself andthe others you must smother your child to death.

Is it appropriate for you to smother your childto save yourself and the other townspeople?

3. Violations of socialnorms

As I was backing out of a parking lot, I bumped aparked car and left a minor dent. I did not even feelthe impact when I hit the car, but it left a little bit ofdamage. I drove away without leaving a message ortrying to contact the person.

Rating the vignette on dimensions of emotionalintensity, emotional aversion, harm,self-benefit, other-benefit, premeditation,illegality, social norm violations, the extent towhich other individuals were involved in thescenario, likelihood of event occurring in reallife, personal familiarity, general familiarity,and moral appropriateness.

4. Social affective/aversive situations

In the late nineties, I got my girlfriend pregnant. Shetold me she was pregnant and that she wanted me tobe there for her. At first, I took her to herappointments and such, until I became nervous andended the relationship.


5. Intent involved insituations thatengender self-benefit

I was taking a statistics class and the professor’sinstructions were very unclear. So, all the studentsin the class helped each other on homeworkassignments and tests. When it came time to takethe test we would just give each other the answers.



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EFECs: event–feature–emotioncomplexes

DLPFC: dorsolateralprefrontal cortex

VLPFC: ventrolateralprefrontal cortex

VMPFC:ventromedialprefrontal cortex

OFC: orbitofrontalcortex

routes and explicit, controlled routes (Greeneet al. 2001, 2004). Specific to moral dilemmas,Greene and colleagues have argued that emo-tional and controlled cognitive processes arekey components of moral decisions involvingutilitarian (e.g., choosing to sacrifice one to savemany) and nonutilitarian choices (e.g., choos-ing to risk detection by enemy soldiers in lieuof smothering one’s crying baby to death; seeTable 1), and at times can play competitiveroles (Greene et al. 2008). Whereas utilitar-ian judgments require controlled cognitive pro-cessing and are thus cognitively demanding,nonutilitarian or deontological judgments areimplicit and predicated on emotional responses.

As opposed to implicit and explicit processescompeting against each other, other researchersargue that the answer may lie somewhere in be-tween (Moll & de Oliveira-Souza 2007). Mollet al. (2005) suggest that moral processes areproducts of the integration of social contextualknowledge, social semantic knowledge, and ba-sic motivational and emotional drives. Thesethree component representations interact toproduce what Moll et al. term event–feature–emotion complexes (EFECs), which bind to-gether via sequential, temporal, and third-partybinding mechanisms and are influenced byone’s situational and cultural context. Throughthese interactions, the EFEC framework makesspecific hypotheses for moral judgments andmoral emotions in different contexts. As dis-cussed below, the model proposed by Moll et al.(2005) also makes specific predictions regardingpatterns of neural activity in the PFC and sub-cortical regions engendered by situations thatrequire moral judgments.

In sum, there is much debate regarding howmoral judgments are cognitively derived andhow they influence overt perceptions of oth-ers. Regardless of which theoretical conjec-ture is most plausible, moral judgments likelyarise out of complex interactions between im-plicit and explicit processes. The field of cogni-tive neuroscience and the fundamental role thePFC plays in cognition can help shed light onthe nature of social cognitive and moral judg-ment processes. Next we briefly describe the

structure and functions of the PFC that enablesocial cognition and moral judgments.

STRUCTURE AND FUNCTIONOF THE PFC

The PFC can be parsed into dorsolateral(DLPFC), ventrolateral (VLPFC), dorsome-dial (DMPFC), ventromedial (VMPFC), andorbitofrontal (OFC) regions. Whereas theVMPFC and OFC regions evolved from sub-cortical regions in the limbic system, theDLPFC likely evolved much later from motorregions such as the basal ganglia, the premo-tor cortex, and the supplementary motor area(Banyas 1999, Fuster 1997). Given that the mo-tor areas of the cortex are thought to storemotor programs, i.e., representations of well-learned mechanistic procedures, regions of thePFC that evolved more recently may be relatedto these evolutionarily older regions becausethey provide a representational basis for goal-directed action (Barbey et al. 2009, Wood &Grafman 2003). By examining the axonal pro-jections distributed by and received by each ma-jor region of the PFC, we can learn more aboutthe basic functions in which PFC regions areinvolved.

The medial and orbitofrontal regions ofthe PFC are hubs for integrating emotional,viscerally arousing information and relayingthat information to the DLPFC (Fuster 1997).Specifically, medial and orbitofrontal regionsof the PFC receive direct afferents from theamygdala, from most other limbic structures,from the striatum, and from temporal visualassociation areas. Medial and orbitofrontalregions also receive indirect afferents from themesencephalic reticular formation and from theinferior temporal cortex [e.g., the fusiform facearea (FFA)] via the magnocellular portion ofthe mediodorsal nucleus in the thalamus (Fuster1997). Studies in a variety of animal species,including the monkey, indicate that the medialand orbitofrontal regions of the PFC, in turn,send a multitude of efferents to the DLPFC(Amaral & Price 1984, Ghashghaei &Barbas 2002, Ghashghaei et al. 2007), which


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ACC: anteriorcingulate cortex

FPC: frontopolarcortex

suggests that the medial PFC regions(DMPFC, VMPFC, and OFC) are inte-gral for monitoring indviduals’ internal statesand motivations and for relaying that informa-tion to the DLPFC (Elliott & Deakin 2005,Wood & Grafman 2003).

The DLPFC is thought to be involved inthe execution of movement and planned behav-iors as well as the integration of sensory infor-mation (Barbey et al. 2009, Beauregard et al.2001, MacDonald et al. 2000, Miller & Cohen2001, Wood & Grafman 2003). This is particu-larly likely given that the DLPFC is reciprocallyconnected with the basal ganglia, the premo-tor cortex, the supplementary motor area, thecingulate cortex, and association areas and re-ceives indirect afferents from the substantia ni-gra, the cerebellum, and the globus pallidus viamediodorsal and ventrolateral thalamic nuclei(Fuster 1997). Highlighting a fundamental yetpervasive role for the DLPFC in goal-directedbehavior, the neural circuit that embodies thereciprocal connections between the DLPFCand anterior cingulate cortex (ACC) has beenheavily implicated in the detection of and sub-sequent correction for behaviors that engenderoutcomes that differ from expectations (e.g.,Cavanagh et al. 2009). Pyramidal cells in theDLPFC also exhibit the potential to fire overextended periods of time (Levy & Goldman-Rakic 2000) and across events (Bodner et al.1996, Fuster & Alexander 1971), which sug-gests that the PFC is well suited for represent-ing action and engaging in behaviors that al-low humans to execute long-term goals (Barbeyet al. 2009).

Overall, the PFC receives direct afferentsfrom most brain regions, including the hy-pothalamus and hippocampus (at least in therat, cat, and monkey), and is extensively in-terconnected with systems within the occipi-tal, parietal, and temporal lobes that are in-volved in sensory processing for each modality(Fuster 1997). Often considered the “top” of atop-down hierarchically determined architec-ture, the PFC is critical for setting and achiev-ing long-term goals (Koechlin et al. 2003) andfor setting activation thresholds in nonfrontal

brain regions to detect goal-relevant stimuli. Assuch, in conjunction with subcortical regions,the PFC likely provides the key representationsfor implicit and explicit social cognitive andmoral judgment processing. We next discussthe specific regions involved in said processesand findings supporting these conjectures.

PFC REGIONS CRITICALFOR SOCIAL COGNITIONAND MORAL JUDGMENTS

Many social cognitive processes are uniquelyhuman and, as such, utilize distinct neural pro-cesses over and above those involved in mem-ory, executive function, perception, and lan-guage in general (Adolphs 1999, Mitchell et al.2006b, Van Overwalle 2009). Overall, implicitsocial cognitive and moral judgment process-ing typically involves the amygdala, insula,hypothalamus, ACC, OFC, and sensory cor-tex (Cunningham & Zelazo 2007, Moll et al.2005). Conversely, slower explicit processingtypically involves the VMPFC, the DLPFC,the VLPFC, and the anterior most portion ofthe PFC, termed the frontopolar cortex (FPC)(Cunningham & Zelazo 2007, Moll et al. 2005).Although these regions may be typically in-volved in implicit or explicit processing, theymay not be exclusively involved in one form ofprocessing or the other and, as noted above,likely interact at all levels of processing (seeFigure 1). For instance, whereas regions suchas the amygdala, ACC, and OFC may be typ-ically recruited for implicit social cognitiveprocesses, in the presence of contextual cuesthat prime different motivational or affectivestates, these regions may be recruited for, or re-main particularly active during, explicit cogni-tive processing as well and exert influence overPFC regions accordingly (see the discussion ofC. Forbes, C. Cox, T. Schmader, & L. Ryan,under review).

Activity in PFC regions associated with so-cial cognition and moral judgment varies onthe basis of the situational context and howstimuli are presented. For instance, studieshave shown differential neural activity when


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individuals engage in self compared with otherprocessing ( Jenkins et al. 2008, Mitchell et al.2006a, Ochsner et al. 2005), when they are pre-sented with predictable or random patterns ofstimuli (Dreher et al. 2002), and whether stim-uli are presented for short or long durations(Cunningham et al. 2004a; C. Forbes, C. Cox,T. Schmader, & L. Ryan, under review). Us-ing the primers on social cognition and moraljudgments as guides, we review the literaturelinking brain regions with the social processesoutlined in these sections.

The Role of the PFC inSocial Perceptual Processes

The social neuroscience literature reveals thatsocial perceptual processes are dynamic andsensitive to basic, even arbitrary distinctionsamong identifying features of others. Present-ing individuals with subliminal faces of out-group members elicits amygdala activation thatcan be regulated by the ACC, OFC, andDLPFC (Cunningham et al. 2004a; C. Forbes,C. Cox, T. Schmader, & L. Ryan, under re-view). Van Bavel and colleagues (2008) demon-strated that this typical neural response can besituationally manipulated on the basis of arbi-trary social distinctions as well.

Utilizing the minimal group paradigm, aprocess known to establish novel in-groups andout-groups effectively using arbitrary informa-tion (e.g., tossing a coin or selecting a certainpainting over another; Tajfel 1982), Van Bavelet al. (2008) randomly assigned white subjectsto different arbitrary, mixed-race teams underthe assumption that their team would be com-peting against another team later in the exper-iment. Subjects were first presented with thesupposed faces of their team and the other team(which consisted of equal numbers of white andblack faces), were asked to encode them, andthen were presented with the faces later dur-ing a task that asked them to categorize facesby ethnicity or team membership. After theexperiment, subjects provided likeability rat-ings for the different faces they were presentedwith throughout the task. Behavioral findings

replicated the basic minimal-group effect: Sub-jects reported liking members of their team, re-gardless of ethnicity, more than members of theother team. The neuroimaging results indicatedthat compared with out-group faces, exposureto in-group faces engendered greater activity inthe amygdala, FFA, OFC, and dorsal striatum.Furthermore, activity in the OFC mediated thebiased, in-group liking ratings. These findingssuggest that the neural networks underlying so-cial perceptual processes are quite sensitive tothe malleability of social group membershipand self-categorization. A situational shift inself-categorization can alter the way neural net-works process and attend to social stimuli, suchas an out-group face compared with a team-mate’s, in spite of otherwise well-learned nega-tive associations linked to out-group members.

The Role of the PFC inAttributional Processes

An abundance of findings in the TOM litera-ture suggests that specific social cognitive neu-ral networks are involved when individuals en-gage in attributional processes in general (for arecent meta-analysis, see Van Overwalle 2009).Indeed, TOM would not be possible withoutlarge contributions from adequately function-ing PFC regions and the consistent finding thatindividuals with autism have particular difficul-ties with TOM tasks is particularly persuasive.For instance, Castelli and colleagues (2002)asked adults with autism or Asperger syndromeand normal controls to watch animated se-quences of triangles engaging in various move-ments, some of which imply intent. Subjectswere asked to describe what was happening ineach animation, and sequences that depictedsome kind of intent among the triangles led nor-mal controls to “mentalize,” or make inferencesthat implied the triangles had mental states.During this task, autistic subjects demonstrateda lack of mentalizing compared with controlsduring animated sequences that implied intent;autistic subjects also demonstrated less activ-ity in the medial PFC, the tempoparietal junc-tion, and the temporal poles than did controls.


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In addition to findings demonstrating abnor-mal functioning in autistic individuals’ medialPFC during self-related and mentalizing tasksin general (Gilbert et al. 2009), these findingssuggest the medial PFC plays a critical role inallowing individuals to identify themselves asunique agents in a social world that, in turn, al-lows them to infer intent in their behavior andin others’.

The VMPFC seems to be particularly im-portant for perspective taking, TOM, andself and other processing. Research frompatient studies supports this conjecture. Inaddition to the tamping-iron-through-the-medial-PFC-induced curmudgeonry incurredby Phineas Gage, individuals with VMPFC le-sions and frontotemporal dementia are knownto have particular difficulties with mental taskssuch as inferring a person’s psychological stateby interpreting the directionality and expres-sion of their eyes (i.e., the reading the mind inthe eyes test; Baron-Cohen et al. 2001) and fauxpaus detection (Gregory et al. 2002). Patientswith VMPFC as well as OFC lesions are alsonotorious for inappropriate or irrational socialbehaviors (Barrash et al. 2000, Beer et al. 2006,Grafman et al. 1996, Koenigs & Tranel 2007).Investigators have also found increased activityin the medial PFC when individuals engage intasks that are introspective in nature, which sug-gests that the medial PFC may be a hub for self,other, and self-in-relation-to-other processingin general (Amodio & Frith 2006; Gusnard et al.2001; Johnson et al. 2002, 2006).

The Role of the PFC inSocial Categorization Processes

The medial PFC also plays a critical role in so-cial categorization processes. Individuals withVMPFC lesions have exhibited reduced im-plicit stereotyping compared with normal con-trols and those with lesions in the DLPFC(Milne & Grafman 2001), which suggests thatthis region is important for the representationof social schemas and stereotypes. In light of thefunctional connectivity between the VMPFCand the DLPFC, stereotype primes likely

engender increased activity in the VMPFC,which then relays information to the DLPFC.Not surprisingly then, many studies suggest theDLPFC is critical for regulating or suppress-ing stereotype activation in general (Knutsonet al. 2007, Payne 2005, Richeson et al. 2003),and studies of patients with primarily VLPFCor VMPFC lesions (Gozzi et al. 2009) supportthis idea. The latter study also demonstratedthat another important component in implicitstereotyping is conceptual social knowledge andthat anterior temporal lobe lesions, particularlyin the right hemisphere, can compromise thisform of social representation.

Highlighting the dynamic flexibility of theneural substrates that underlie these social phe-nomena, including those involved in implicitand explicit processing, C. Forbes, C. Cox, T.Schmader, & L. Ryan (under review) investi-gated the effects of priming negative in-groupand out-group stereotypes on individuals’ moti-vation to regulate stereotype activation. In thisstudy, white subjects who reported being ex-plicitly nonprejudiced and motivated to remainso were presented with subliminal (30 ms) andsupraliminal (525 ms) black and white faces. Toprime negative in-group and out-group stereo-types, either a violent death metal or violent rapsong, i.e., stimuli that prime negative stereo-types for whites or blacks respectively, wasplayed in the background while subjects wereexposed to the novel faces. Results revealed thatwhen negative white stereotypes were primed,the typical amygdala response to subliminalblack faces was not evident. When negativestereotypes of blacks were primed, however,amygdala activity was elicited in response toblack faces at implicit processing speeds thatpersisted into explicit processing speeds, i.e. theamygdala response was evident in response toblack faces presented at both 30 ms and 525 ms.

Furthermore, functional connectivity anal-yses revealed that the increased amygdalaresponse to subliminal black faces covariedwith increases in OFC and DLPFC activityamong other regions. The amygdala responseto supraliminal black faces covaried with de-creases in ACC activity and again with increases


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in DLPFC activity, which suggested that thenegative stereotype activation engendered in-creased processing demands in the DLPFCspecifically at implicit and explicit processingspeeds. These findings indicate that neural re-gions involved in implicit and explicit process-ing may interact at fast and slow cognitive pro-cessing speeds and that situational primes canalter how neural networks involved in socialcognition perceive and react to social stimuli.

The PFC’s Role inMoral Judgment Processes

The basic components of social cognitive andmoral judgment processing appear similar, andneural regions involved in these types of pro-cesses reflect this. Many key neural regions in-volved in social cognition overlap with those in-volved in moral judgment, including the medialPFC and DLPFC. For instance, Greene andcolleagues (Greene et al. 2001, Greene & Haidt2002) suggest that when individuals considerpersonal moral dilemmas and/or make non-utilitarian judgments, areas involved in emotionprocessing are likely to exhibit increased activ-ity, and this effect would be mediated by the me-dial PFC. Conversely, considering impersonalmoral dilemmas and/or making utilitarian judg-ments are more likely to elicit increased activa-tion in regions associated with cognitive controlprocesses and the DLPFC specifically. Again,according to Greene and colleagues, these dualroutes to decision making may often competeor create tension.

To test this hypothesis, Greene et al. (2004)asked subjects to read a series of moral dilem-mas, ranging from impersonal (e.g., flipping atrolley track switch to save the lives of manycompared to one) to personal (e.g., smotheringyour crying baby to death to avoid being de-tected by oppositional soldiers who will kill youand others) and indicate which alternative theywould choose. Results revealed that personalmoral judgments elicited activity in the medialPFC among other regions, replicating previousfindings (Greene et al. 2001). In contrast, im-personal moral judgments elicited activity in the

DLPFC, which suggested that individuals en-gaged in more effortful cognitive, as opposed toemotional, processing in analyzing these moraldilemmas. Increased activity in the DLPFC wasalso evident when individuals made utilitarianchoices on personal moral dilemmas (e.g., indi-cating they would smother their baby to deathto save the lives of many).

One set of findings inconsistent withGreene’s dual process theory is that individu-als with VMPFC lesions make more emotionalchoices in an ultimatum game and more util-itarian moral judgments in general comparedwith normal controls (Koenigs et al. 2007,Koenigs & Tranel 2007, Moll & de Oliveira-Souza 2007). Other important factors to con-sider when contrasting personal versus imper-sonal moral decisions include the frequency ofexposure to the described scenario. Personalmoral decision making as well as more real-world or pragmatic scenarios would be morelikely to recruit familiar analogous personalmemories, whereas impersonal moral decisionmaking and those dilemmas grounded in tradi-tional philosophy would be less likely to do soon the basis of frequency of experience alone.Controlling for these and other factors thatcould affect scenario processing is critical, andKnutson and colleagues have now establisheda normative database of brief, real-world moralscenarios for this purpose (Knutson et al. 2010).

Thus, Moll and colleagues argue for theEFEC framework described above and positthat a network of closely interconnected neu-ral regions is responsible for integrating thediverse functions involved in moral appraisalsand judgments. In addition to the VMPFC andDLPFC, other critical regions are the FPC, theanterior temporal cortex, the superior temporalsulcus region, and the limbic structures includ-ing the amygdala, the angular gyrus, and theposterior cingulate (Moll et al. 2005, Moll &de Oliveira-Souza 2007, Raine & Yang 2006).Moll and colleagues’ EFEC framework (Mollet al. 2005, Moll & de Oliveira-Souza 2007)makes specific hypotheses regarding the neuralregions involved in moral judgment, emotions,and values.


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Specific to the PFC, the EFEC frameworkpredicts that whereas the anterior PFC is inte-gral for enabling humans to assess the possiblelong-term consequences of their behavior withrespect to others, the DLPFC is integral forpredicting outcomes of one’s behavior in novelcontexts. Consistent with the hypothesized roleof the VMPFC in the representation of so-cial knowledge, Moll et al. (2005) argue thatthe VMPFC plays an important role in allow-ing one to adhere to social norms and culturalvalues that individuals derive through the so-cialization process. Finally, the OFC is likelynecessary for comparing social cues in a givencontext with one’s preexisting representationsof social knowledge to help one determineappropriate behaviors within a given context.Consistent with one theme of this review, thenature of the presenting stimuli and/or thatwhich individuals are asked to deliberate candifferentially activate regions involved in moreimplicit emotional processing (i.e., the limbicsystem) or slow explicit processing (e.g., theDLPFC) depending on the context. Although ahost of evidence from lesion and experimentalstudies supports these conjectures, to date noinvestigators have directly compared the vari-ous models of moral judgment and processingin social neuroscience experiments.

Overall, the medial and lateral PFC as wellas the ACC and OFC are clearly necessary forsocial cognitive and moral judgment process-ing (Figure 2). How these regions interact tofacilitate everything from basic social cognitiveprocesses to more complex processes such asmoral judgment and in what capacity are stillquestions that are much debated in the litera-ture. Next, we outline a theory that attempts toanswer these questions by providing a frame-work for the types of information stored in thedifferent regions of the PFC and how they mayinteract to enable social cognitive and moraljudgment processing in general.

STRUCTURED EVENT COMPLEXTHEORY DESCRIBES THE PFC’SROLE IN SOCIAL COGNITIONAND MORAL JUDGMENT

As mentioned above, on the basis of the func-tional connectivity between different PFC andsubcortical regions and evolutionary and neu-rophysiological evidence, the primary role ofthe PFC is in the representation of action andguidance of behavior (Barbey et al. 2009). Anygiven behavior can be broken down into a se-ries of recognizable events, which are seman-tic in nature and of a fixed temporal duration

APFCAPFCVMPFC/MOFCMOFC

ATLATL

APFCAPFC

MOFCMOFC

ATLATL

LOFCLOFCLOFC

STSSTS

DLPFCDLPFC

APFCAPFC

ATLATL

LOFCLOFCLOFC

APFCVMPFC/MOFC

ATL

APFC

MOFC

ATLSTS

DLPFC

APFC

ATL

AmyAmyAmy VVVV

ACCACC

Figure 2Neural regions identified as critical for social cognitive and moral judgment processing. Neural regions include the anterior prefrontalcortex (APFC), dorsolateral prefrontal cortex (DLPFC), medial and lateral orbitofrontal cortex (MOFC and LOFC), ventromedialregions of the prefrontal cortex (VMPFC), anterior cingulate cortex (ACC), anterior temporal lobes (ATL), amygdala (Amy), and thesuperior temporal sulcus (STS) region. Modified, with permission, from Moll et al. (2005), figure 1.


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SEC: structured eventcomplex

(Barbey et al. 2009, Zacks & Tversky 2001). In agiven situation, a series of events can be primedand linked together to form a script that guidesbehavior and allows one to predict how the sit-uation will unfold. The linking of events can,in turn, represent a set of goal-oriented events,one that is sequentially ordered and composedof social norms that guide behavior and per-ceptions. We refer to this goal-oriented set ofevents as a structured event complex (SEC)(Barbey et al. 2009, Grafman 2002, Wood &Grafman 2003).

Components of SECs can be semanticallyindependent, but they are encoded and re-trieved as an episode using simulation mech-anisms or feature maps (Barsalou et al. 2003a,b;Damasio 1989). SECs provide goal-directedactions with semantic and temporal structureand are activated or primed by environmen-tal cues, arming the organism with ammuni-tion to predict how different social scenarioswill unfurl. SECs ultimately represent myriadbits of knowledge that can be organized in pre-dictable or unique manners to allow for increas-ingly complex behaviors and predictions. Thetype of knowledge a given SEC contains andthe format of the behaviors they facilitate canbe localized to specific neural regions.

SECs Are Composed ofMultiple Dimensions

According to the SEC framework, SECs havemultiple dimensions to them, including pre-dictability, complexity, and category specificity,and the nature of the binding process is pred-icated on the hemisphere in which bindingoccurs (for a review, see Barbey et al. 2009).Overall, whereas the left PFC is hypothesized tointegrate meaning and features between singleadjacent events, the right PFC integrates mean-ing and information across events. In terms ofdegree of predictability, the medial PFC storespredictable SECs, or those SECs that are en-grained in individuals and have structured, fa-miliar goals and behaviors associated with them.Predictable SECs can be thought of as a schemaor stereotype in general; e.g., they represent

how different events such as going to a party or alecture typically unfold, but they are tailored to-ward the individual’s goals. For instance, whengoing to a party, an introvert is likely to have dif-ferent goals than an extrovert, and subsequentlytheir SEC for attending a party, while similar,will uniquely vary on the basis of their individ-ual goals for the evening (e.g., stand in a cornerlike a wall flower versus meet as many new peo-ple as possible).

Conversely, the lateral PFC has evolved tostore adaptive SECs, which are more flexiblein nature and allow for adaptations to uniqueor ambiguous situations. For instance, whenmeeting someone new, an individual is likely toactivate SECs on the basis of the person’s ap-pearance, which allow an individual to predictwhich behaviors are required for a successfulinteraction; however, unexpected feedbackwill stimulate different SECs that, in turn,will update predictions, goals, and ultimatelybehavior. This conjecture is supported by pastresearch indicating that the VLPFC is particu-larly active when individuals experience attitudeambivalence, i.e., a situational cue primes bothpositive and negative information, thus requir-ing the individual to resolve the ambiguity ina novel manner (Cunningham et al. 2004b).

SECs vary substantially in complexity aswell. Given its proximity to phylogeneticallyolder regions of the brain, the posterior PFCstores simple, well-learned SECs that consistof minimal information about event sequences(e.g., see Kruger et al. 2009a,b). This is likelywhere basic social cognitive SECs, such as neu-ral networks sensitive to different facial expres-sions or body movements, are stored, which,when activated by a situational cue, in turn ac-tivate more complex SECs in the anterior PFC.The most anterior portions of the PFC store themost complex SECs, including long-term goalsand integration of multistage event complexes,which is likely why the FPC region is so heavilyinvolved in complex moral judgments (Berthozet al. 2002; Moll et al. 2001, 2002, 2005).

The VMPFC and DLPFC regions enablecategorical specificity in SECs. Specifically, theVMPFC stores SECs specific to social norms


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and scripts. In addition to Milne & Grafman’s(2001) study demonstrating less stereotype ac-tivation by individuals with ventral PFC lesions(Milne & Grafman 2001), fMRI studies havedemonstrated that stereotype activation is likelyto engender increased activity in the VMPFCspecifically (Knutson et al. 2007, Quadflieget al. 2009). Violations of social norms also elicitactivity in the VMPFC (Berthoz et al. 2002),which suggests that this region is upregulatedfor the purpose of retrieving stored social normswhen contextual cues necessitate comparisonsbetween others’ behaviors and known norms.Together these findings support the notion thatthe VMPFC stores SECs specific to generalbeliefs about various social groups and socialnorms, which are necessary for one to navi-gate the social world in an efficient yet moralmanner.

Not unlike other theories, the SEC frame-work posits that the DLPFC is involved in plan-ning and action. The SEC framework specifi-cally hypothesizes that the DLPFC stores eventsequences that represent the planning and ac-tion necessary to achieve a primed goal state.Based on situational cues, overarching goalsdictate how components from SECs activatedin other brain regions are integrated and orga-nized to formulate an action plan with a desir-able outcome.

One way to assess the mechanisms under-lying these assertions would be to examineindividual differences between biased andnonbiased individuals interacting with an out-group member. For instance, we might expectinteractions with an out-group member to elicitactivation in the medial PFC in general, repre-senting stereotypic activation associated withthe out-group. We would also expect, however,for DLPFC activity to vary on the basis ofan individual’s goal to be nonbiased towardthe out-group member, by which increasedDLPFC activity could represent the manip-ulation and integration of SECs to allow theindividual to actualize an egalitarian goal. Onestudy by Rilling and colleagues (Rilling et al.2008) provides a format to investigate thesequestions.

In one study, Rilling et al. (2008) randomlyassigned subjects to a red or black team (pur-portedly based on results from a personalitytest) and asked them to complete a prisoner’sdilemma task with a supposed in-group andout-group partner while brain activity wasassessed via fMRI. Participants were classi-fied as discriminators or nondiscriminatorspost-hoc on the basis of whether they reportedfeeling different when interacting with thein-group partner compared with the out-grouppartner. Results indicated that when playingwith arbitrarily defined out-group members,both nondiscriminators and discriminatorsdemonstrated increased activity in the medialPFC, suggesting they were activating SECsassociated with social norms and perhaps repre-sentations of other known out-group membersin hopes of predicting their partner’s behaviors.

Activity in the DLPFC, however, was mod-ulated by feelings toward the out-group part-ner. Nondiscriminators elicited greater activityin the DLPFC compared with discriminators.Given that typical minimal group paradigmssuch as these engender immediate in-group biasand disliking for out-group members (particu-larly during competitions), increased DLPFCactivity in reported nondiscriminators couldrepresent their attempts to organize activatedSECs from the medial PFC in a manner consis-tent with an overarching egalitarian goal. Thesefindings support the conjecture that a given sit-uational cue activates stereotype-related SECsin the medial PFC, but the DLPFC monitorsand temporally organizes these SECs within thecontext of meta-goal states, such as the desireto behave in a morally just way toward othersto regulate behavior accordingly.

The SEC framework also provides a meansfor understanding how different PFC regionscontribute to implicit and explicit processes andhow these processes differentially affect PFCneural networks. Consistent with the role neu-ral regions along the midline play in implicitprocessing in general (e.g., the amygdala andthe ACC), the medial PFC likely contributesto implicit processes because this region storespredictable SECs associated with habituated


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sequences, schemas, and stereotypes (e.g., onecannot have stereotype activation without thestereotype). Likewise, posterior regions of thePFC are likely involved in implicit processingto the extent they store basic features associatedwith others and others’ intentions, which areautomatically activated upon encounter. Con-versely, the lateral and anterior portions of thePFC are more involved with explicit process-ing, given that these regions store adaptive andcomplex SECs involved in explicit planning, ac-tion, and detailed sequences.

Any given behavior enacted in a specific con-text would necessarily involve an interactionbetween the various SECs that contribute toimplicit and explicit processing (see Table 2).For example, let’s say you run into a friend of afriend at a bar whom you had met a few timesbefore and this second-degree friend is behav-ing strangely. This behavior prompts you toengage in attributional processing to try andexplain your acquaintance’s behavior. To dothis, simple SECs associated with the individ-ual’s features and context, predictable SECs as-sociated with how the individual behaved in thepast, and adaptive and complex SECs account-ing for the unique situation would all be acti-vated. Your motivation to understand or explainyour acquaintance’s behavior would in turn dic-tate whether conclusions would be based moreon implicit or on explicit processes. If you donot necessarily like the person, your explicit at-tributions for their behavior are likely to bemore influenced by predictable SECs that re-flect your lack of motivation to understand theirbehavior and your disliking of them in general(e.g., “this person is weird just like I thought”).If the person is someone you want to like, adap-tive and complex SECs will dictate explicit at-tributions as you are motivated to find specificcontextual factors that may be influencing theirbehavior (e.g., “maybe they had a rough day andone drink too many”).

Thus the lateral PFC can regulate the me-dial PFC, i.e. adaptive SECs will be utilized andpredictable SECs will be inhibited or restruc-tured within the overarching SEC accordingly,when habituated sequences are not appropri-

ate or desired in light of contextual cues. Whenmotivation is lacking, contributions of the me-dial PFC to implicit processing will have agreater influence on explicit perceptions, andpredictable SECs will be utilized in lieu of adap-tive SECs. In both instances, however, the con-struction of the overarching SEC would bethe product of the interaction between multi-ple SECs varying in complexity associated withcontextual primes, norms, values, and currentgoal states or plans of action.

Overall, the SEC framework provides a ra-tionale for the myriad cognitive processes in-volved in social cognition and moral judgment,from the heuristic and efficient to the dynami-cally flexible and cognitively demanding. It alsohighlights the pivotal role that different neuralregions of the PFC play in those processes andthe necessity for these neural regions to interactat multiple speeds of cognitive processing (seeTable 2 for a mapping of social processes on tobrain regions and SEC components). Together,utilizing knowledge of the phylogenetically hi-erarchical structure of the PFC in conjunctionwith physiological properties of the PFC, theSEC framework provides a comprehensive viewof how a given social context can activate andintegrate SECs throughout the PFC that enableindividuals to assess their situations and makepredictions that satisfy personal goals in sociallyand morally appropriate ways either extremelyquickly or more deliberately.

SUMMARY AND CONCLUSIONS

The PFC is vital for human social cognitive andmoral judgment processing. Because more an-terior regions of the PFC serve as the last, inte-grative stop for all facets of perceptual and emo-tional processing, regions such as the OFC, theVMPFC, and the DLPFC are likely critical forevaluating current motivational and emotionalstates and situational cues and for integratingthis information within the context of currentgoal states and past experience. Through inter-actions among these regions, possibly at bothimplicit and explicit levels, humans can buildimmediate impressions of others, infer what


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Table 2 A summary of different SECs involved in social cognitive and moral judgment processes, key PFC regions involved,and the tendency for a given process to occur implicitly (fast) or explicitly (deliberative). BA, Brodmann’s area;PT, perspective taking; SEC, structured event complex; TOM, theory of mind; labels following a given BA region denotewhether fMRI studies (F), lesion studies (L), or transcranial magnetic stimulation (T) provided evidence for that brainregion’s involvement in the respective social process

Underlying information processingcomponents Key PFC regions involved

Implicit or explicitprocess?

Social perceptual processesOther individual

identificationSingle-event processing: identify basicsocial features of individual

BA 9 (F), BA 10 (F), BA 11 (F),BA 47 (F)

Implicit

Social mimicry Single-event processing: sequentialdependencies based on partnerbehaviors that vary by single adjacentevent

BA 6 (F), BA 44 (F) Implicit

Movement intentions Single-event processing: identify intentand meaning of basic biologicalmovements

BA 9 (F), BA 11 (F) Implicit

Attributional processesSelf-related processing Predictable SECs associated with

self-concept; occasional use of adaptiveSECs when behaviors contradictperceived self-concept

BA 9 (F), BA 11 (F, L), BA 12(F, L), BA 32 (F)

Both

Other processing/PT/TOM

Predictable SECs associated withknowledge of others; adaptive SECs toaccount for ambiguous behaviors; socialcategory–specific SECs bias perceptionsbased on learned associations of others’group memberships

BA 6 (F), BA 9 (F, L), BA 11(F, L), BA 12 (F, L), BA 32 (F),BA 46 (T)

Both

Moral judgments Predictable SECs associated withself-perceived appropriate behaviors;adaptive SECs are applied to morallyambigous situations; social andnonsocial category–specific SECsconsisting of socially and personallyacceptable beliefs and norms

BA 9 (F), BA 10 (F), BA 11(F, L), BA 12 (F, L), BA 32 (F),BA 46 (F), BA 47 (F)

Both

Social categorization processesStereotypes/schemas/

scriptsPredictable SECs representingwell-learned beliefs toward others andnormal courses of behavior in general;social category–specific SECsrepresenting well-learned beliefs,attitudes, and social norms

BA 9 (F), BA 11 (F, L), BA 12(F, L), BA 46 (F, L), BA 47 (F)

Implicit

Impression formation Predictable SECs involved withestimating others’ intentions based onlimited identifying information; socialcategory–specific SECs associated withothers’ perceived social categoricalinformation

BA 9 (F), BA 11 (F), BA 12 (F) Implicit

(Continued )


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Table 2 (Continued )

Underlying information processingcomponents Key PFC regions involved

Implicit or explicitprocess?

Predictive processesFuture planning Long duration SECs involved in

planning and action; predictable SECsassociated with self-concept

BA 9 (F), BA 10 (F), BA 11 (F),BA 12 (F), BA 46 (F, L)

Explicit

Strategies in novel contexts Nonsocial category–specific SECsinvolved in predicting behavior in novelcontext and planning and action

BA 46 (F), BA 47 (F) Explicit

Strategies in learnedcontexts

Social category–specific SECs involved inwell-learned social rules and scripts

BA 9 (F), BA 11 (F), BA 12 (F),BA 47 (F)

Implicit

others are thinking, and plan actions that arelikely to facilitate a successful interaction withothers, all within the context of social norms.These basic behaviors and impressions, in turn,form the foundation for more complex cogni-tive processes such as evaluating another’s be-havior in relation to culturally ascribed rulesor to function successfully within large socialgroups.

The SEC framework provides a means tounderstand how regions within the PFC inter-act to enable social cognitive and moral judg-ment processing. Although outside the realm ofthis article, in light of our understanding of thefunctional connectivity between the PFC andmost other subcortical neural regions, SECsunderlying social cognitive and moral judg-ment processing likely integrate emotional andreward-related responses to contextual stim-uli and basic perceptual processes (Wood &Grafman 2003). These SECs, in turn, are in-fluenced by the socialization process and in-dividual differences. The complex interactionbetween these processes can occur at multipleprocessing speeds to facilitate sophisticated im-plicit and explicit social cognition and moraljudgment. Moll et al. (2005) posit in theirEFEC framework that complex behaviors suchas moral judgment likely involve the integrationof SECs that represent social norms, basic per-ceptual features in one’s environment such asfacial expressions, visceral emotional responsesto stimuli, and references to past experience

via autobiographical memory reconstruction, aswell as SECs that represent meta or long-termgoal states among other things. Such integra-tion would require interplay among neural re-gions such as the anterior PFC, the DLPFC,the VMPFC, the OFC, the superior tempo-ral sulcus, the anterior temporal lobe, and thelimbic system, including the hypothalamus, theseptal area, and the amygdala in a matter ofmilliseconds (Figure 2). In line with evolution-ary perspectives, the order in which the afore-mentioned list of critical neural regions arelisted may also represent a hierarchical struc-ture that allows for increasingly complex socialand moral behaviors.

In attempts to assess such complex neuraland social interactions in a scientifically validmanner, social neuroscience experiments havebegun to include an increasing array of tasksand problems reflecting the varied social ex-periences of real life. Social processes are notsimply another brain activity worthy of atten-tion but are key brain processes determiningsuch things as outcomes after brain injury, thetrajectory of human evolution, and the mod-ulation of human impulses. This review hasemphasized the PFC’s important role in thesebehaviors. Whereas some brain regions, suchas the ventral axis structures from the brainstem to cortex concerned with reward or limbicstructures concerned with emotion and attach-ment, have been understandably linked to so-cial behaviors, other brain areas, such as regions


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within the parietal cortex, which have beenimplicated (primarily via functional neuroimag-ing) in social behavior, have not been firmly es-tablished yet as being crucial to the examinedsocial process. Although it has become commonto attribute social processes to certain regionswithin the PFC, there is less certainty abouthow to conceptualize the spatial topography tounderstand better why certain social processeslie near each other in these brain areas and whatmight the underlying computational processesbe that support these social (and presumablyother kinds of cognitive) processes.

The PFC has evolved to represent the mostcomplex aspects of knowledge and informa-tion processing. Recent research has shown thatsome areas within the PFC are part of an in-creasingly hierarchical system for processinginformation from single events to the linkage ofsets of events. More dorsal regions of the PFCare more likely to process information pertain-ing to an agent’s actions toward external stim-uli (e.g., agents acting upon objects), whereasmore ventral regions appear more likely to as-sess the relevance of information to the socialagent (e.g., reward value attributed to exter-nal stimuli). Hemispheric asymmetries in in-formation processing are also apparent; the lefthemisphere codes a dominant meaning or char-acterization of stimuli, whereas the right hemi-sphere codes multiple concepts in parallel with-out committing to one concept or meaning.Although less efficient than left hemisphereprocessing, particularly when a single solutionis optimal, such processing would be superiorwhen more than one solution to a social prob-lem is possible.

This very brief speculative characteriza-tion of the PFC’s functional roles applies toall kinds of functional domains including themoral and social processes reviewed above. Thefact that some of the most prominent deficitsthat occur following damage to the PFC aresocial-cognitive suggests that at least certain as-pects of social behavior are tightly coupled tothe processing constraints of the PFC. In re-cent reviews, our colleagues offer some exam-ples of how the schema we sketched above is

related to specific social and cognitive process-ing deficits in patients with lesions to specificareas of the PFC as well as which prefrontal cor-tical regions might be activated depending onspecific processing demands (e.g., Barbey et al.2009, Krueger et al. 2009a, Moll et al. 2005,Wood & Grafman 2003).

Computational forces within the PFC ap-pear to allow for at least two hierarchical mech-anisms to operate. One mechanism involvesrepresentational complexity, which links a deepsearch tree with parallel searches occurring si-multaneously. The other mechanism involvestemporal coding across events that merges ap-parently separable events into a single engram,allowing for streamlined forecasting and mem-ory retrieval. These two mechanisms enablemore detailed and elaborated conceptions ofsocial behavior to be represented and utilizedthan would be available from a single event em-bedded in a stream of events. Although humansmay benefit from the development of such elab-orated conceptions in our behavior, constraintson resource utilization may bias us to rely moreon attitudes, heuristics, and simplified personalvignettes when making decisions about beliefs.

If important aspects of social beliefs are rep-resented in memory in the PFC, how similar isthat representation to that which is seen in otherforms of representational memory such as se-mantic memory concerned with the meaning ofwords and objects? Simpler forms of social rep-resentation, such as attitudes, may obey princi-ples similar to that of semantic representations,including being sensitive to frequency of expo-sure, influenced by context, etc. Little evidenceindicates whether the same constraints wouldapply to more complex beliefs such as religiousor political beliefs (e.g., see Kapogiannis et al.2009, Zamboni et al. 2009). Frequency of eventexposure affects the activation site within themedial PFC as does complexity of event infor-mation (Krueger et al. 2009a,b). Less frequentlyexposed information is associated with the com-plexity of representation and activation of theFPC. This association suggests that more fre-quently exposed information can lead to sparsercue representation because the behavioral


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action sequence would be more predictableand procedurally rigid (also predicting storagesites more posterior within the frontal lobesthan FPC), whereas less frequent informationwould require more complex cuing and deeperrepresentational search and deliberation be-cause outcomes would be less predictable, givenless direct personal experience with the eventsequence.

This level of complex representation shouldbe slower to process and enact than other formsof representation such as object naming or evensocial concepts. What kind of advantage doesit offer? This form of complex representationwould offer an advantage because it could in-hibit more impulsive behavior and have a su-pervening role in decision making. In particu-lar, it would automatically activate potential orcertain consequences in the future of an imme-diate action. Such foresight allows the individ-ual to implement strategic action that is poten-tially costly in the present but advantageous inthe long run and can overcome potential liabil-ities in physical capabilities or other attributes.In a brain that is built with inherent inhibitorypathways between competitive brain regions,a brain region that was composed of SECswould have the mechanisms to inhibit simpleassociative behaviors using temporal informa-tion encapsulated within engrams stored in thePFC. Compared with other recent evolutionarychanges, this particular change would offer sub-stantial advantages in many situations—bothsocial and nonsocial—and could stimulate theevolution or development of other functionalbrain properties. For example, if our repre-sentational memories captured and integratedsocial information over long time durations,that evolutionary change may have stimulatedthe development of language content that con-veyed the social consequences (e.g., allowingthe verbal expression of foresight) associatedwith one’s current actions and motives, therebyfacilitating the expansion of language beyondits use for simple object identity and naming.

To make these ideas more concrete, letus take an example of one social event. Youare with politically informed friends and are

discussing whom you are going to vote forin the next presidential election. How mightyour cognitive and neural processes supportthat social interaction? Because the discussionis within a known social group and it is likelythat at least one other person in the group willchoose the same candidate as you will, yourbrain would activate regions within the PFCthat are concerned with reading others’ inten-tions, bonding, the heuristics of voting for aparty’s candidate (if favored, your reward sys-tem would also be active), narrative discussionof the candidates’ qualifications versus his or heropponent, as well as the overall context of theelection. Equal emphasis in information pro-cessing is not paid to all aspects of this scenarioat any one time, so regions concerned with eachof the above social processes are likely to be dif-ferentially activated at any one point in time.

Most of the social processes described aboveare explicit, but other implicit social processesmay also be engaged. If you are much more fa-miliar with your own candidate’s background,you may be likely to activate stereotypes and bi-ases about his opponent (who may be classifiedas being a candidate from an out-group, fromyour perspective). Expectation of how the con-versation will go allows priming of future narra-tives to occur and also taxes cognitive structuresconcerned with foresight and action planning.Similar conversations with less informed peoplecould wind up taxing more primitive and im-plicit cognitive and social representations andtypically evoke more emotional, and less ratio-nale, discourse. The dynamics of such discus-sions cause many regions and social processesto be simultaneously primed in preparation forretrieval of information (relevant or irrelevant).

It is difficult to capture the above scenariowithin a laboratory setting, and even compart-mentalizing such a dynamic situation is chal-lenging. Investigators have tended to isolate themajor social process contributors to simple re-sponses with various kinds of probes. What dif-ferentiates us from other species that have theirown social structures is the human ability touse solutions and ideas that do not depend onthe surface features of the subjects (e.g., size,


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attractiveness, progeny) nor their physical ca-pabilities (e.g., strength, aggressive tendency).Despite these differences, under certain cir-cumstances with unknown individuals, the se-lection of the person who is judged to be themost popular or whom you might vote for of-ten corresponds with the physical features ofthe face, and a significant association exists be-tween those attractive features and the candi-date’s likelihood to win an election (Spezio et al.2008, Todorov et al. 2005). So although humansocial complexity has distanced us from relatedspecies, e.g., chimpanzees or gorillas, they arenot out of view.

In this article, we have emphasized func-tional neuroanatomy and have not discussed thechemical and genetic features of human socialbehavior. Quantifying the anatomic, chemical,genetic, and behavioral components of socialbehavior in combination will allow researchersto account for as much variance in behavior as ispossible in open societies. Social neurosciencewill play a key role in this effort.

The social interactions and judgmentsof humans have been based on evolution-ary pressures and environmental and socialcontingencies. They will continue to evolvein parallel with technological changes. Thewidespread use of devices that can providealmost instant information (e.g., face recog-nition and identification) and feedback (e.g.,eliciting pleasurable sensations via individuallytailored visual stimuli on Web sites) as well asthe emergence of social networks based simplyon user-provided input will change the waywe interact with others and the way the brainevolves or devolves in the future. In addition,introducing such sophisticated technology at ayoung age may affect development and enhancebrain systems concerned with more immediateresults and gratification. Public discussion ofthese issues will become more important aswe judiciously manage the benefits of newtechnology in balance with its effects on socialbehavior and on the development of the socialbrain.

DISCLOSURE STATEMENT

The authors are not aware of any affiliations, memberships, funding, or financial holdings thatmight be perceived as affecting the objectivity of this review.

ACKNOWLEDGMENTS

This work was supported by the Imaging Sciences Training Program, Radiology and ImagingSciences, Clinical Center, and the National Institute of Biomedical Imaging and Bioengineeringand the Intramural Research Program of the National Institute of Neurological Disorders andStroke, National Institutes of Health. The authors thank Joshua Poore and an anonymous reviewerfor helpful comments on earlier versions of this manuscript.

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NE33-FM ARI 14 May 2010 19:47

Annual Review ofNeuroscience

Volume 33, 2010Contents

Attention, Intention, and Priority in the Parietal LobeJames W. Bisley and Michael E. Goldberg � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � 1

The Subplate and Early Cortical CircuitsPatrick O. Kanold and Heiko J. Luhmann � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � �23

Fly Motion VisionAlexander Borst, Juergen Haag, and Dierk F. Reiff � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � �49

Molecular Pathways of Frontotemporal Lobar DegenerationKristel Sleegers, Marc Cruts, and Christine Van Broeckhoven � � � � � � � � � � � � � � � � � � � � � � � � � � � � �71

Error Correction, Sensory Prediction, and Adaptationin Motor ControlReza Shadmehr, Maurice A. Smith, and John W. Krakauer � � � � � � � � � � � � � � � � � � � � � � � � � � � � � �89

How Does Neuroscience Affect Our Conception of Volition?Adina L. Roskies � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � 109

Watching Synaptogenesis in the Adult BrainWolfgang Kelsch, Shuyin Sim, and Carlos Lois � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � 131

Neurological ChannelopathiesDimitri M. Kullmann � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � 151

Emotion, Cognition, and Mental State Representation in Amygdalaand Prefrontal CortexC. Daniel Salzman and Stefano Fusi � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � 173

Category Learning in the BrainCarol A. Seger and Earl K. Miller � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � 203

Molecular and Cellular Mechanisms of Learning Disabilities:A Focus on NF1C. Shilyansky, Y.S. Lee, and A.J. Silva � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � 221

Wallerian Degeneration, WldS, and NmnatMichael P. Coleman and Marc R. Freeman � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � 245

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NE33-FM ARI 14 May 2010 19:47

Neural Mechanisms for Interacting with a World Fullof Action ChoicesPaul Cisek and John F. Kalaska � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � 269

The Role of the Human Prefrontal Cortex in Social Cognitionand Moral JudgmentChad E. Forbes and Jordan Grafman � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � 299

Sodium Channels in Normal and Pathological PainSulayman D. Dib-Hajj, Theodore R. Cummins, Joel A. Black,and Stephen G. Waxman � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � 325

Mechanisms of Synapse and Dendrite Maintenance and TheirDisruption in Psychiatric and Neurodegenerative DisordersYu-Chih Lin and Anthony J. Koleske � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � 349

Connecting Vascular and Nervous System Development: Angiogenesisand the Blood-Brain BarrierStephen J. Tam and Ryan J. Watts � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � 379

Motor Neuron Diversity in Development and DiseaseKevin C. Kanning, Artem Kaplan, and Christopher E. Henderson � � � � � � � � � � � � � � � � � � � � � � 409

The Genomic, Biochemical, and Cellular Responses of the Retina inInherited Photoreceptor Degenerations and Prospects for theTreatment of These DisordersAlexa N. Bramall, Alan F. Wright, Samuel G. Jacobson, and Roderick R. McInnes � � � 441

Genetics and Cell Biology of Building Specific Synaptic ConnectivityKang Shen and Peter Scheiffele � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � 473

Indexes

Cumulative Index of Contributing Authors, Volumes 24–33 � � � � � � � � � � � � � � � � � � � � � � � � � � � 509

Cumulative Index of Chapter Titles, Volumes 24–33 � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � 513

Errata

An online log of corrections to Annual Review of Neuroscience articles may be found athttp://neuro.annualreviews.org/

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the role of the human prefrontal cortex in social …...the role of implicit and explicit processes...

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