Social Cognitive Neuroscience: Where Are We Heading?

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ReviewTRENDS in Cognitive SciencesVol.8 No.5 May 2004Social cognitive neuroscience:where are we heading?Sarah-Jayne Blakemore1, Joel Winston2 and Uta Frith112Institute of Cognitive Neuroscience, 17 Queen Square, London, WC1N 3AR, UKWellcome Department of Imaging Neuroscience, 12 Queen Square, London, WC1N 3BG, UKHumans crave the company of others and suffer profoundly if temporarily isolated from society. Much ofthe brain must have evolved to deal with social communication and we are increasingly learning moreabout the neurophysiological basis of social cognition.Here, we explore some of the reasons why social cognitive neuroscience is captivating the interest of manyresearchers. We focus on its future, and what webelieve are priority areas for further research.The field of social cognitive neuroscience is still relativelynew but builds on a variety of well established disciplinesincluding social, developmental and cognitive psychology,evolutionary biology, neuropsychology and computerscience, each providing a solid basis of relevant research.In the past few years, interest in the neurological underpinnings of social cognition has burgeoned, as demonstrated by at least four special issues of major journalsin this field [1– 4]. What drives this interest in socialcognitive neuroscience? And what is the future of thisflourishing discipline? In this article, we pick out severalareas of social cognitive neuroscience and focus onwhere we believe each area might head in terms offuture research.What is social cognitive neuroscience?Most generally, social cognition encompasses any cognitiveprocess that involves conspecifics, either at a group levelor on a one-to-one basis. Social cognitive neuroscienceencompasses the empirical study of the neural mechanisms underlying social cognitive processes. One keyquestion is whether general cognitive processes involvedin perception, language, memory and attention, aresufficient to explain social competence, or whether overand above these general processes there are specificprocesses that are special to social interaction. Thispossibility is exciting because it can explain socialimpairment in otherwise very able individuals, in particular in autism.It may once have seemed foolhardy to work outconnections between fundamental neurophysiologicalmechanisms and highly complex social behaviour,let alone to decide whether the mechanisms are specificto social processes. However, as we shall see, neuroimaging studies have provided some encouraging examples.The next step of linking brain mechanisms to genesthat contribute to social competence is already in sight(see Box 1).However, we need to be cautious when interpreting theresults of neuroimaging studies reporting brain activations during high level cognitive processes such asmoral reasoning, deception and fairness. These kinds ofprocesses are challenging to emulate and control withinthe scanning environment, and in some cases, what islabelled deception or morality in an experiment is farfrom those concepts in everyday life. Furthermore, in thecontext of social cognition there have as yet been relativelyfew attempts to replicate findings. On the other hand, itBox 1. Social genesIt is unknown just how biological factors interact with environmentalvariables to produce individual differences and pathology. In thefuture, we anticipate that the genetic basis for different aspects ofsocial cognition will be illuminated. This is feasible by studyingindividuals who are born without the ability to develop normal socialcommunication, for example people with autism and people withpsychopathy.Congenital abnormalities in the neural substrates of social cognition can serve to identify endophenotypes that relate to disordersof social cognition. The term endophenotype refers to the ‘insidephenotype’ rather than overt behaviours, which are likely to be theproduct of many different endophenotypes. These then can lead thesearch for the genetic basis of specific social functions. Examples ofallelic variation combining with environmental conditions contributing to social phenomena, such as the development of antisocialbehaviour, are also being characterized [62]. The gene in this case(MOA-A) is implicated in central neurotransmitter pathways, whichsupports the contention that aspects of individual differences mightbe characterized by such pathways [63].Social cognitive processes can be genetically selected. A primeexample of this is in dogs, which are able to glean information aboutthe location of an object from a human’s eye gaze and pointing [64].This appears to be specific to domesticated dogs; neither chimpanzees nor wolves are able to use a person’s eye gaze to search for anobject, demonstrating that this ability is neither specific to primatesor canine species in general. By contrast, young puppies can use eyegaze information, implying that the ability is not learned from yearsof experience with people. Instead it is suggested that this ability hasbeen bred into the dogs’ gene pool over centuries of domestication.What do we know about social interaction in other species? A primeexample of social species are insects. Ants are known to be able tochange their social roles, say from worker to warrior, as the situationdemands. Insect societies could serve as analogies to human societies, and in particular, insects could provide genetic models forhuman social adaptation.Corresponding author: Sarah-Jayne Blakemore (s.blakemore@ucl.ac.uk).www.sciencedirect.com 1364-6613/ - see front matter q 2004 Elsevier Ltd. All rights reserved. doi:10.1016/j.tics.2004.03.012

TRENDS in Cognitive Sciencesis reassuring that in certain areas, for example in thestudy of mentalising (see section: Understanding others’minds), there are now at least ten studies using differentstimuli and performed in different laboratories, whichhave yielded strikingly similar results.Even when a neuroimaging study is highly controlledand the results have been replicated many times over,what does it mean to know that a brain region is activatedby a certain task? Why does it matter and what does it add?In isolation, brain imaging data has been criticized asbeing of little importance for understanding the workingsof the mind. But we would argue that brain imaging datacomplement and extend the results from behavioural,singe cell and lesion studies. The next section provides anexample of a field where all of these methods have beenused to great effect. Scanning people’s brains while they donothing but observe another person do something hasopened a new door to research on the neuroscience ofsocial cognition.Understanding others’ actionsIn the past decade, neurophysiological research hasprovided evidence of a brain system that decodes conspecifics’ actions and may contribute to the understandingof other people’s intentions, goals and desires. Mirrorneurons, found in ventral premotor cortex of macaquemonkeys, are activated both when the monkey executesgrasping actions and when it observes someone else(or another monkey) making grasping actions [5]. Mirrorneurons appear to distinguish between biological and nonbiological actions, responding only to the observation ofhand-object interactions and not to the same action ifperformed by a mechanical tool, such as a pair of pliers [6].Following the discovery of mirror neurons in monkeys,there is increasing evidence that a large proportion of thehuman motor system is activated by the mere observationof action [7]. Brain imaging studies have revealed that themotor activation to observed action is functionally specific:premotor cortex and parietal cortex are activated in asomatotopic manner according to the modality of theaction being observed [8]. In addition, observing an actionaffects the peripheral motor system in the specific musclesthat are used in the action being observed [9].The study of the mirror system provides an example ofan attempt to identify the neurophysiological activity thatunderlies the ability to understand the meaning of one’sown and another person’s actions. This class of mechanismmay be fundamental to several higher level social processes, where the actions of other agents are interpreted insuch a way that they directly influence one’s own actions.This is the case in the attribution of intentions to othersand oneself, and the ability to imitate as well as to teachothers. Although it seems obvious that another person’sactions can influence one’s own actions, insight into theprecise nature of this influence at the behavioural andphysiological level was provided only recently in an experiment by Sebanz et al. [10]. When a subject performed aspatial compatibility task, the presence of a partneraltered the timing of the subject’s responses in the sameway as when two simultaneous tasks were performed by asingle subject.www.sciencedirect.com217Vol.8 No.5 May 2004(a)Right superior temporal sulcus(b)Implicit task(age 5MedHighExplicit task(trust judgment)TRENDS in Cognitive SciencesFigure 1. (a) Experimental design of a study of interference effects of observingbiological movements on actions [13]. The subject (S) made sinusoidalmovements with their right arm at the same time as observing movements thatwere either congruent or incongruent with their own movements. The observedmovements were made either by another human (experimenter, E) or by a roboticarm (R). There was also a baseline condition in which the subject moved their armwithout watching anything. Subject arm movements were recorded using anOptotrak system. (b) Interference effects. For each arm movement, the variance inthe movement orthogonal to the dominant dimension of movement and in thedominant dimension of the incongruent movement was calculated. Meanvariances (and standard error bars) are shown for the five conditions. The onlycondition in which movement variance differed significantly from the baselinemovement condition was that in which subjects watched the human experimentermaking incongruent arm movements. Thus, the interference effect seems to bespecific for observed human actions. Reproduced with permission from [13].Observing another person’s actions also influences one’sown ongoing movements. Recent evidence suggests thatobserving an action interferes with one’s own actions whenthese are different from those being observed [11 – 13]. Thisinterference effect seems to be specific for observed humanactions; observing a robot making a movement does notinterfere with ongoing actions [13] (Figure 1).Understanding actions: future researchWhy is it that mirror neurons require biological actionsto be activated [6]? What is special about biological actionsin this case? Why is it that the observation of biologicalmovements performed by a human interferes with action,whereas robotic movements do not [13]? What is it aboutthe presence of another person that is the influentialfactor? Does a human have to be present, or would a robotprogrammed to show the characteristic kinematics ofbiological motion have the same influence?Does eye gaze, our own and that observed in people withwhom we communicate, play a crucial role in theseinteractions [14,15]? Gaze bias can influence the perceivedattractiveness of faces, not merely reflecting a prioripreference [16]. Mere signals of an impending communication, either being looked at intently, or being called byone’s name, activates significant portions of the brainregions known to be involved in understanding others [17].

Review218TRENDS in Cognitive SciencesVol.8 No.5 May 2004Can the mirror system be trained? In a recent studymonkeys were trained to rip paper [18]. When this waslearned, specific mirror neurons started to fire in responseto the action sound. Are mirror neurons sufficientlyflexible and dynamic that they can start to representany type of action in all modalities?Does the mirror system enable us to understandingother people’s minds? Is the mirror system functioningnormally in people with autism whose understanding ofother minds is impaired?brain imaging studies using a wide variety of verbal andnon-verbal stimuli to investigate mentalising (see [23]).The subcomponents of this mentalising process andthe precise nature of the triggering stimuli still remainto be revealed.Meanwhile, work on mentalising is rapidly evolving tothe investigation of the neurophysiological basis of thecomplex behaviour shown by people when playing economic games [24], during deception and when showingempathy and moral sensitivity.Understanding others’ mindsAutism research has led to the hypothesis that sociallearning requires the detection of intentions and innermental states of other agents [19]. Specifically, it isproposed that there is a brain mechanism that enablesus automatically to attribute mental states to self andothers, and this mechanism is faulty in autism. The searchfor the genetic basis of this ability has begun (see Box 1).So automatic and pervasive is this mind-readingmechanism that ordinary adults feel compelled to attribute intentions and other psychological motives toanimated abstract shapes, simply on the basis of theirmovement patterns [20]. This has been exploited inneuroimaging studies in which participants view animations of moving shapes [21,22] and has provided information on the underlying brain system. In the study byCastelli et al. [21], a comparison between animations thatevoked mental state attributions (e.g. one triangle mocking another) and animations in which triangles movedrandomly demonstrated activation of the medial frontallobe, the superior temporal sulcus (STS) and the temporalpoles. These regions have consistently been activated inCheating and bargainingThe ingenuity of people to outwit each other and to usebluff and double bluff is an instance of advanced socialskills that rely on an intuitive mentalising ability. Severalneuroimaging studies have attempted to investigatedeception, but this is a challenging task because of theconfined and artificial context of the brain scanner. Taskshave been devised in which subjects are instructed towithhold truthful responses and answer with their opposites to questions concerning recent autobiographicalevents [25], or to lie about a card’s identity [26] or pastevents [27]. These studies have found activations incomponents of the mentalising system when subjects arelying. Whether this artificially engineered deception usesthe same mechanisms as spontaneous deception remainsto be seen.It has been argued that being equipped with mechanisms for detection of cheaters would carry high evolutionary advantages [28]. An imaging study in which subjectsviewed faces that varied on trustworthiness found automatic activation of the amygdala with magnitude proportional to the perceived untrustworthiness of the face(a)(b) 600CongruentIncongruentRobotSRSRVariance on0TRENDS in Cognitive SciencesFigure 2. Superior temporal sulcus (STS) is activated when making explicit trustworthiness judgements. STS has been activated in many imaging studies of socialcognition, for example mentalising, biological motion perception and even simple face perception. Here, greater STS activation was observed when subjects made explicitjudgments of trustworthiness about faces compared with when they made age judgments (implicit task) about the same faces. (a) The STS activation in the explicit task.(b) The size of the response in the STS for the two tasks (age and trustworthiness judgment) and as a function of trustworthiness (low, medium or high) of the face. There isa clear difference between activation in the two tasks, the STS being activated for the explicit trustworthiness judgment task only, but no relationship with the perceivedtrustworthiness of the faces. Adapted from reference [29].www.sciencedirect.com

ReviewTRENDS in Cognitive Sciencesand activation of the STS during explicit trustworthinessjudgements only [29]; (see Figure 2). What makes a faceappear trustworthy, and whether these characteristicsare universal or culturally specific, is still unknown. Thereis some evidence that untrustworthy people might havemore memorable faces than trustworthy faces. This evidence comes from a study in which many different faceswere presented to subjects whose memory for the faces wassubsequently tested. The faces of people who had previously chosen to defect in prisoner’s dilemma games werebetter remembered than those who cooperated, eventhough the subjects in the memory experiment saw onlythe faces and had no information about the performance inthe prisoner’s dilemma game [30].Fairness and justiceMoral judgements activate brain regions that are involvedin mentalising, including the medial frontal cortex, according to a recent study in which subjects were scanned whileevaluating moral dilemmas [31]. Medial frontal cortexappears to be critical to moral development according to astudy that compared patients who suffered lesions in thisregion at a young age and those whose cortex was damagedin adulthood [32]. Patients with childhood lesions showeddefective social and moral reasoning, whereas this was notevident in those with later damage.Mentalising: future researchMany aspects of social communication involve mentalising: understanding beliefs, intentions, desires of others;knowing that these can differ from one’s own mentalstates; understanding that to see is to know; attributingintentions to actions, eye gaze and facial expressions, andso on. Does the brain’s intuitive mentalising system playan equally important role in each of these? Can mentalising be reduced to subcomponents, such as a representationof intentional and contingent actions? What are thedifferent roles of the brain regions involved in mentalising? What is the role of top-down control when reflectingon one’s own and others’ mental states?How is mentalising related to competition and deception, cooperation and teaching, fairness and moral judgement? What can we learn about the brain basis ofmentalising from individual differences in mentalisingskills? What social skills do not involve mentalising?Understanding others’ emotionsThe brain reads facial expressions extremely rapidly[33 – 35]. Several brain imaging studies have shown thatthe amygdala is activated by emotional expressions infaces (e.g. [36,37]), even independent of attention orawareness [38,39]. There is some suggestion that amygdala responses to other emotions might depend uponindividual differences, such as extraversion [40]. Morerecently, there has been interest in the perception ofdynamic displays of emotion in faces [41] and of emotionfrom bodily posture [42].Complex emotions, such as jealousy, pride, embarrassment and guilt, are different from the simple emotions thatwww.sciencedirect.comVol.8 No.5 May 2004219we might recognize in another person’s face. They oftenimply awareness of another person’s attitude to oneself,and an awareness of the self in relation to other people. Ifso, they are likely to involve the mentalising system. Thereis imaging evidence that this is the case for emotions suchas embarrassment [43] and forgiveness [44].The study of empathy has recently been advanced byscanning couples, where under highly controlled conditions, one partner suffered an electric shock, and theother’s brain was scanned as they anticipated thepartner’s pain [45]. In this study, brain regions activatedby the expectation of another’s pain overlapped with thoseactivated by the experience of one’s own pain. The anteriorcingulate and insula were the most critical regions activated in this study. These areas are not activated bymentalising tasks, and this raises the possibility thatfeeling another’s pain is independent of seeing the worldfrom another person’s point of view.Complex emotions: future researchIs there a difference in the brain between emp

Social cognitive neuroscience: where are we heading? Sarah-Jayne Blakemore1, Joel Winston2 and Uta Frith1 1Institute of Cognitive Neuroscience, 17 Queen Square, London, WC1N 3AR, UK 2Wellcome Department of Imaging Neuroscience, 12 Queen Square, London, WC1N 3BG, UK Humans crave the company of others and suffer pro-foundly if temporarily isolated from society.

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