facial expressions, their communicatory functions

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Facial Expressions, Their Communicatory Functions and Neuro-Cognitive SubstratesAuthor(s): R. J. R. BlairSource: Philosophical Transactions: Biological Sciences, Vol. 358, No. 1431, Decoding, Imitatingand Influencing the Actions of Others: The Mechanisms of Social Interaction (Mar. 29, 2003),pp. 561-572Published by: The Royal SocietyStable URL: http://www.jstor.org/stable/3558134 .

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c-m HE ROYALRJP SOCIETY Publishedonline5 February 2003

Facial expressions, theircommunicatoryunctionsand neuro-cognitiveubstratesR. J.R. Blair

Unit onAffectiveognitiveNeuroscience, ood and AnxietyDisorders rogram,National Institute fMental Health,National InstitutefHealth,DepartmentfHealth and Human Services,Room206, MSC 2670, 15K NorthDrive,Bethesda,MD 20892-2670, USA ([email protected])Human emotional expressions ervea crucial communicatory ole allowingthe rapid transmission fval-ence information rom one individual to another. This paper will review the literatureon the neuralmechanisms necessary for this communication: both the mechanisms involved in the production ofemotional expressions and those involved in the interpretation f the emotional expressions of others.Finally,reference o theneuro-psychiatric isorders of autism,psychopathy nd acquired sociopathywillbe made. In these conditions,the appropriateprocessingof emotional expressions s impaired. In autism,it is argued that the basic response to emotional expressionsremains intact but that there is impairedability o represent he referent f the individualdisplaying he emotion. In psychopathy, he responsetofearful nd sad expressions s attenuated and this interfereswith socialization resulting n an individualwho fails to learn to avoid actions that result n harm to others. n acquired sociopathy,the response toangryexpressions n particular s attenuatedresulting n reduced regulationof social behaviour.

Keywords: facialexpressions; amygdala; communication;psychopath;autism1. INTRODUCTION

Facial expressions are a crucial component of humanemotional and social behaviour and are believed to rep-resent innate and automatic behaviour patterns Darwin1872). The purpose of this paper is to consider facialexpressions: the stimulithat elicittheirpresentation, heneuro-cognitivesystemsnecessary for their production,theneuro-cognitive ystems hat nterpret he expressionsproduced by others and the conditions under which theinterpretermay respond to the emoter thus closing thecommunicatory oop. To do this, will make one funda-mental assumption: that facial expressionsof emotion doindeed have a communicatoryfunction,and that theyimpart specific information o the observer. Thus, thesuggestionwill be thatexpressionsoffearfulness,adnessand happiness are reinforcers hat modulate the prob-ability hat a particularbehaviourwillbe performedn thefuture. ndeed, fearfulfaces have been seen as aversiveunconditioned stimuli thatrapidly convey information oothersthat a novel stimulus s aversive nd should be avo-ided (Mineka & Cook 1993). Similarly, t has been sug-gested that sad facial expressions also act as aversiveunconditioned stimuli discouraging actions that causedthedisplayof sadness in another ndividualand motivatingreparatory ehaviours Blair 1995). Happy expressions, ncontrast, are appetitive unconditioned stimuli whichincrease the probabilityof actions to which they appearcausally related (Matthews & Wells 1999). Disgustedexpressions are also reinforcers ut are used most fre-

quentlyto provide information bout foods (Rozin et al.1993). Displays of anger or embarrassment, t is argued,do not act as unconditionedstimulifor versive ondition-ing or instrumentalearning. nstead, theyare importantsignalsto modulate current ehaviouralresponding,parti-cularly in situations involving hierarchy interactions(Blair & Cipolotti 2000; Keltner & Anderson 2000).In contrast o thecommunicatory unction ssumption,therehave been suggestions hat emotionalexpressions reautomatic displays that occur as a function of theemotional experience of the individual (Darwin 1872;Buck 1984; Izard & Malatesta 1987; Ekman 1997).According to these authors,althoughthe expression mayimpart nformationo observers, hetransmission f nfor-mation is not theirfunction. nstead, the expression s anautomatic consequence of the individual's experience(Ekman 1997). However, theempirical iterature oes notindicate that individuals display emotional expressionsautomaticallyas a functionof the degree to which theyfeel a particularemotion (Fridlund 1991; Camras 1994).Instead social context predicts probabilityof emotionalexpression n humans as it does probability f non-verbaldisplays n non-humanspecies (Cheney & Seyfarth 980;Hinde 1985). Thus, participants mile more at a humour-ous video or show greaterdistress o the sound of an indi-vidual in distress ftheyare togetherwithanother ratherthanif hey re alone (Chovil 1991; Fridlund 1991). Simi-larly, nfant milingfromthe age of 10 monthsis almostentirelydependent on visual contact with the caregiver:withoutsuch contact the infant s veryunlikelyto smile(Jones & Raag 1989; Jones etal. 1991).Importantly,heargumenthere is notthatthedisplayofan emotionalexpression mplies ntent o conveya specificmessage to the observer. The argument is simply thatOne contribution of 15 to a Theme Issue 'Decoding, imitating andinfluencing he actions of others: the mechanisms of social interaction'.

Phil. Trans.R. Soc. Lond.B (2003) 358, 561-572DOI 10.1098/rstb.2002.1220 561 ? 2003 The RoyalSociety

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562 R. J.R. Blair Facial expressions,ommunicationnd neural ubstratesemotional xpressions erve a communicatoryunctionthat hey ave evolved o that nformationn thevalenceof objects/situationsan be transmittedapidly etweenconspecifics. hus, important riggersoran emotionaldisplaynclude oth n emotional vent ndalso a poten-tialobserver.f theres no observer,he motional isplaywilleither ot occur or be considerably uted.A particularlylear llustrationf thecommunicatoryfunctionf emotional xpressions an be seen after ninfant's iscoveryf a novelobject.The infant ill ooktowardsheprimaryaregivernd their ehaviour illbedetermined y the caregiver'smotionaldisplay. f thecaregiver isplays n expression f fear or disgust, hechildwillavoidthe novelobject. f thecaregiverisplaysa happyexpression, he child will approachthe novelobject.Thisprocess s known s socialreferencingnd isseen in children rom he age of eightto ten months(Klinnertt l. 1983,1987;Walker-Andrews998). Inter-estingly,omparableocialreferencings seen nchimpan-zees (Russelletal. 1997) and a very imilar rocesshasbeen shown n othermonkeysnd labelled bservationalfear Mineka& Cook 1993).Minekacharacterizesheprocessof observationalearwithin n aversive onditioning rameworkMineka &Cook 1993). The US is themothermacaque's expressionoffear,which heshows o theCS, thenovel bject.Thismaternal earful xpression, he US, elicitsan uncon-ditioned esponse, fearfuleaction,nthe nfantmonkey.Pairing f the US with heCS, the novelobject, llowstheCS toelicit conditionedesponse; he nfantmonkeycomes to show a fearfuleaction o the novelobject.A simple onditioningpproachs,however,nlikelyobe appropriatenhumans. n humans, herepresentationof the emoter's ntenthas been shownto be crucial.Indeed,the earning f valencesfornovelobjects an bethought f similarlyo the learning fnamesfornovelobjects.Whenhearing newword, hildren o not auto-maticallyssociate hisword withwhatever ovelobjectis in their mmediate ield of view. Instead,they urntowards he speaker, alculate the objectthatthey reattendingo,and associate henewwordwith hisnovelobject Baldwin t l. 1996;Bloom2002). Similarly,ur-ing social referencing,f the child is attendingo oneobjectwhen hecaregiverisplaysn emotional esponsetoanother,he hildwill ook tthe aregivero determinethe directionf their ttention. he childwillthenformthe ppropriatessociation etween he nformationom-municated ythecaregiver'sxpressionnd theobject owhich the caregiver ad been attending Moses et al.2001). Thus, thecommunicationfvalenceto objects,like the communication f names to objects, nvolvesassociationf he ffectivenformationith CS that or-responds o the communicator'seferent.

2. THE PRODUCTION OF EMOTIONALEXPRESSIONSThe suggestiondeveloped above is that emotional

expressions re communicatoryignals hatfunctionoconvey valence information apidly to conspecifics.Specifically,hey reparticularlyikelyobe elicited nderconditionswhen there s an emotional timulus n theenvironmentnd there s an audienceto perceive he

expression. But emotional expressionsare not automati-cally elicitedunder these conditions. ndividuals are cap-able of intentionally manipulating their emotionaldisplays,theymayfollow displayrules', societalproscrip-tions as to what emotion should be displayed n givencir-cumstances and how intensely it should be displayed(Ekman & Friesen 1969). Indeed, one major task facedby the child in middle childhood is to learn the culture'sdisplayrulesgoverning he conditions thatare appropriateforthe displayof specificemotions. In a classic studyofthe development of display rules and control overemotional expressions, age-relatedchanges were demon-strated n theabilityof childrento cover theirdisappoint-ment at the discoverythat theirgiftfor helping out anadultwas much less interestinghanthegift heyhad beenexpecting; hedisappointment f theyounger hildrenwasfar easier to detect (Saarni 1984).There is thus a suggestion of spontaneous or over-learned emotional expressionsto emotional stimuli n thepresence of observers as well as controlled or posedemotionalexpressionsas a function fdisplayrules. t hasbeen argued that the neuropsychologicaldata about theproduction of emotional expressionsecho thisdichotomy(Rinn 1984; Hopf etal. 1992). Thus, it has been claimedthat sub-cortical regions are necessary for spontaneousemotional displays but not controlled ones, whereascorticalregions re necessaryfor ontrolledemotional dis-plays but not automatic emotionaldisplays (Rinn 1984).However, this strictdichotomyoverstates the empiricalpicture. Thus, investigations fpatientswith Parkinson'sdisease and otherpatientswithdamage to the basal gang-lia reportmarked reductions in the production of spon-taneous emotional expressions; such patients showreduced displaysofemotional expressionswhenwatchingemotionally arousingvideos relativeto comparison indi-viduals (Borod et al. 1990; Pitcairn et al. 1990; Weddell1994; Smith et al. 1996). However, such patients alsoshow some impairment in the production of posedemotionaldisplays, houghto a lesserdegree (Borod etal.1990; Weddell 1994; Smith et al. 1996). Similarly, herehave been reports hat esions offrontal ortex mpairtheabilityof the patient to pose emotional expressionsbutspare the production of spontaneous emotionalexpressions (Hopf et al. 1992). However, other studiesfind significant mpairment in the production of bothposed and spontaneous emotionalexpressions n patientswith frontalcortex lesions (Weddell et al. 1988, 1990;Weddell 1994).The data thereforeuggestthatsub-corticalregions, nparticularbasal ganglia, and corticalregions,particularlyfrontalcortex, are involved in both the production ofspontaneous and controlled emotional displays.A sche-matic ofregionsknownto be involved s presented n fig-ure 1. Basal ganglia and frontal ortexare represented sreciprocally nterconnected such that damage to eitherstructurempairs heproductionofemotionalexpressions.The greateroutputfromthe frontal ortexrepresents hefact that while frontalcortical lesions cause significantimpairmentto both the production of spontaneous andcontrolledexpressions Weddell et al. 1988, 1990; Wed-dell 1994), lesions to the basal ganglia disproportionatelyaffect he productionof spontaneous expressions Borodet al. 1990; Weddell 1994; Smith et al. 1996). Frontal

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Facial expressions,ommunicationnd neural ubstratesR. J.R. Blair 563frontalortex

amygdalandother motorrogrammessystemsrocessing - basalganglia for xpressionsemotionaltimuliFigure1. A schematic fregionsknown o be involvedntheproduction femotional xpressions.

cortex s likely o be crucialfor epresenting oals to eithershow or suppressan emotionalexpression.The basal gan-glia receives inputs from both the amygdala and otherstructuresprocessing emotional information.Althoughamygdala lesions do reduce the display of spontaneousfearful isplaysto novel objects (Pratheret al. 2001), theydo not affect heproductionof controlled fearful r otheremotional displays (Anderson& Phelps 2000).3. RESPONDING TO THE EMOTIONALEXPRESSIONS OF OTHERS

Two dissociable routeshave been shown to be involvedin processing fear conditioning (Armony et al. 1997;LeDoux 2000). Thus, information n conditioned stimuliduring uditory earconditioning an be mediatedby pro-jectionsto theamygdalafrom ither heauditory halamusor auditory cortex (LeDoux et al. 1984; Romanski &LeDoux 1992a,b; Campeau & Davis 1995). Analogously,there have been suggestions that information on theemotionalexpressionsof otherscan be conveyedeitherbya sub-cortical athwayretinocollicular-pulvinar-amygdalar)or by a corticalpathway retinogeniculostriate-extrastriate-fusiform) de Gelder et al. 1999; Morris et al. 1999;Adolphs 2002).The suggestion s that the sub-corticalpathwayis fastand allows immediateautomaticaccess of information nemotional expressions to the amygdala that can thenmodulate the processing of information through thecorticalpathway Pizzagalli et al. 1999; Adolphs 2002). Insupportofa sub-corticalpathway,positivecovariations ofcerebral blood flow (as measured by positron emissiontomography maging)have been demonstrated n thepul-vinar, superior colliculus and amygdala in response tomasked facial expressions of anger that had been pre-viouslyassociated with an aversive stimulus Morris et al.1999). Visual masking s assumed to be a result of inter-ference between the induction of neural activityby thestimulusand themask,which occurs within herelativelyslow response time of primaryvisual cortex neurons(Macknik & Livingstone 1998). Neurons in the superiorcolliculus are capable of respondingto much more rapidchanges in visual input and hence produce quite distinctresponsesto the facialexpressionand neutral mask. How-ever, such responses fail to elicit conscious experience.Additional support for the suggestion of a sub-corticalpathwayhas been provided bywork withG.Y., a patientwith a long-standing ight-sided emianopia after ccipital

lobe damage at the age of8 years (de Gelder et al. 1999).This 'blindsight'patientshowed some abilityto discrimi-nate (by guessing) between different acial expressionsinhis blind hemifield.Later neuro-imagingwork with G.Y.demonstrated differentialmygdala responses to fearfulversus happy expressions when these were presented toboth the blind and seeinghemifields.However, striate ndfusiformactivityonly occurred in response to stimulipresentedto the seeing hemifield. n addition, amygdalaresponses to fear conditioned faces exhibit condition-specificcovariations with neural activity n the posteriorthalamus and superiorcolliculus (Morris et al. 2001).The cortical route nvolvesregionsofoccipital and pos-teriortemporalvisual cortex (Haxby et al. 2000, 2002).In particular,neuro-imagingstudies have indicated thatthreespecific reas are involved n faceprocessing:thelat-eral occipital gyri,bilateralregionsin the lateral fusiformgyrus and the posterior superior temporal sulcus(Kanwisher etal. 1997, 2000; Haxby etal. 1999). More-over,there are strong uggestionsof a dissociationinfunc-tion between the fusiform yrus and superior temporalsulcus (Hasselmo et al. 1989; Hoffman& Haxby 2000).The suggestion s that the fusiform yrus s more involvedin the processing of facial identitywhereas the superiortemporal sulcus is more involved in the processing ofsocial communication (Haxby etal. 2002).Recent event-related otentialand magnetoencephalog-raphy studies have allowed considerable specificationofthe time-course for the processing of emotionalexpressions Pizzagalli et al. 1999, 2002; Streit t al. 1999;Halgren et al. 2000). The earliest activity hat discrimi-nates between emotional facial expressions s seen in mid-line occipital cortex frombetween 80 to 110 ms post-stimulus Pizzagalli et al. 1999; Halgren etal. 2000). Fromca. 160 ms, activity s seen in the fusiformgyrus andsuperior temporalsulcus (Streitetal. 1999; Halgren etal.2000; Pizzagalli etal. 2002). This literature as yetto findevidence of early amygdala activity hat the sub-corticalroute should predict. Indeed, the earliest activity een isat ca. 220 ms in the right amygdala (Streit et al. 1999).However, therehas been a report of neuronal discrimi-nation, as singleunit responses,between the emotions offear and happiness after nly 120 ms in the orbital frontalcortex ofa patient Kawasaki etal. 2001). This would sug-gest a sub-corticalroute to orbital frontal ortex.There appear to be further ctivationsof superiortem-poral cortex after the amygdala activation (Streit et al.1999), perhaps as a consequence ofthe amygdala activity.Indeed, a recent tudyexamining ingleunitactivitynthetemporalvisual cortex nmonkeysfound that nformationsufficient o distinguishdifferent motional expressionsoccurred ca. 50 ms after information sufficient o dis-tinguishfaces from otherobjects was available (Sugase etal. 1999). This again suggeststhepossibility hatresponseto emotional stimuli n the temporal cortex is modulatedby feedback from structures such as the amygdala(Adolphs 2002). Moreover, many imaging studiesinvestigatingheneuralresponseto emotional expressionshave reported greater uperiortemporal sulcus and fusi-formgyrus activity o emotional expressions relative toneutral expressions (Phillips et al. 1998; Critchleyet al.2000; Iidaka etal. 2001). In addition,taskconditions thatincrease attention to emotional expressions result in




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564 R. J.R. Blair Facial expressions,ommunicationnd neural ubstratesincreased superior temporal sulcus and fusiformgyrusactivity Narumoto et al. 2001; Vuilleumier et al. 2001;Pessoa et al. 2002).Two additional cortical areas that have been linked tothe processing of emotional expressions are bilateralregionsof inferior rontal ortex and inferior arietalcor-tex. Three neuro-imagingstudies have observed inferiorfrontal ortexactivity o emotional expressions George etal. 1993; Nakamura et al. 1999; Gorno-Tempini et al.2001) although, it should be noted, many other studieshave not. Activityn theinferior arietalcortex,or at leastthe proximal region of superior temporal sulcus, is fre-quently implicated in the processing of face stimuli(Haxby etal. 2000) and expressionprocessing Phillips etal. 1997; Streit et al. 1999; Halgren et al. 2000; Kesler-West et al. 2001; Pizzagalli et al. 2002). Moreover, twostudies investigatingwhich cortical regions,when dam-aged, most effectedexpression recognition stressed theimportance of the inferior arietal cortex (Adolphs et al.1996, 2000). These areas are ofpotential nterest s proxi-mal areas are activated when either n individual s initiat-ing a movement or when they are observing anotherinitiate the same movement (Iacoboni et al. 1999). Thishas promptedsuggestions hatrespondingto another ndi-vidual's expressionrelies on the activation of motorpro-grammes that the individual uses for the production ofexpressions (Preston& de Waal 2003).As stated in thebeginningof thispaper, a fundamentalassumptionof thispaper is that emotional expressions recommunicatory ignals that serve specificpurposes. Theclaim is that thisperspective llows an understandingntospecific patternsof activation seen forspecificemotions.Importantly, earful, ad and happy expressionscan all beviewed as reinforcers hat modulate the probability hat aparticularbehaviour will be performed n the future.Theamygdala has been implicated in aversive and appetitiveconditioning ncluding nstrumentalearning Killcross etal. 1997; Everitt et al. 2000; LeDoux 2000). It is thusunsurprising, iventhe suggestedrole of fearful, ad andhappy expressions s reinforcers,hatneuro-imaging tud-ies, with a fewexceptions (Kesler-Westet al. 2001), havegenerally ound thatfearful,ad and happy expressions llmodulate amygdala activitySchneideret al. 1994; Breiteret al. 1996; Morris etal. 1996; Phillipsetal. 1997, 1998;Baird et al. 1999; Blair et al. 1999; Drevets et al. 2000),though it should be noted that happy expressionshavebeen reported to both increase and decrease amygdalaactivity Breiter et al. 1996; Morris et al. 1996). Theneuropsychological iterature upportsthe neuro-imagingliterature about the importance of the amygdala in theprocessing of fearful expressions. There have beenoccasional suggestions that amygdala damage leads togeneral expression recognition impairment but thesereportsare typicallyfrompatientswhose lesions extendconsiderably beyond the amygdala (Rapcsak et al. 2000).Instead, amygdala lesions have been consistently ssocia-ted with impairment in the recognition of fearfulexpressions Adolphs etal. 1994, 1999; Calder etal. 1996;Schmolck & Squire 2001). Impairment n the processingof sad expressionsis not uncommonlyfound in patientswith amygdala lesions (Adolphs et al. 1999; Schmolck &Squire 2001). Indeed, a recent reviewofpatient perform-ance across studies,reported hat ca. 50% ofpatientswith

amygdaladamage presentwith mpairment or the recog-nition of sad expressions (Fine & Blair 2000). Amygdalalesions rarelyresult in impairment n the recognitionofhappy expressions (Adolphs et al. 1999; Fine & Blair2000). However, this may reflect the ease with whichhappy expressions are recognized (Ekman & Friesen1976).Disgusted expressionsare also reinforcers ut are usedmost frequentlyto provide information about foods(Rozin et al. 1993). In particular, they allow the rapidtransmission f tasteaversions;theobserver s warned notto approach the food that the emoter s displaying hedis-gustreaction to. Functional imagingstudieshave consist-ently hown that disgusted expressionsengage the insulaand putamen (Phillips et al. 1997, 1998; Sprengelmeyeret al. 1998) and patientswithdamage to the nsula presentwith selective mpairment orthe recognition fdisgustedexpressions (Sprengelmeyer et al. 1996; Calder et al.2000). Experimental investigations in macaques haveshown that there s a primary aste corticalregion n theanterior nsula (Rolls 1997) and neuro-imaging tudies nhumans have also shown the insula to be involved in therepresentation f taste (O'Doherty et al. 2001b; Small etal. 2001). Crucially, insula lesions have been found toblock the acquisition and expression of taste aversionlearning Cubero etal. 1999). Thus, thesuggestion s thatthe disgusted expressionsof others activate in particularthe insula allowingtaste aversion (disgust expressionUS-novel food CS associations) to occur.In contrast o the expressionsconsideredabove, it is farless clear that the angryexpression s a basic reinforcer.Angryexpressionsare known to curtailthe behaviour ofothers n situationswhere social rulesor expectationshavebeen violated (Averill 1982). They appear to serve toinform he observer o stop the current ehavioural actionrather han to convey any informations to whether hataction should be initiated n the future. n otherwords,angry xpressions an be seen as triggersor esponserever-sal (Blairet al. 1999; Blair & Cipolotti 2000). Orbitalfron-tal cortex s crucially mplicated n responsereversal Diaset al. 1996; O'Doherty et al. 2001a; Cools et al. 2002).Interestingly,imilarareas of lateral orbital frontal ortexare activatedby angry xpressions nd responsereversal sa functionof contingency hange (Sprengelmeyer t al.1998; Blair et al. 1999; Kesler-West et al. 2001). Inaddition,mostneuro-imagingtudiesdo notobserve myg-dala activationto angry xpressions Sprengelmeyer t al.1998; Blair et al. 1999; Kesler-West et al. 2001). The onlystudy,to my knowledge,that did observe amygdala acti-vationby angry xpressions oundveryweak activation hatwas significantlyess than that seen to fearful xpressions(Whalen et al. 2001).

4. NEUROTRANSMITTER NVOLVEMENT NRESPONDING TO THE EXPRESSIONS OFOTHERSThere is a growingbody of data indicating degreeof

differential neurotransmitter nvolvement in systemsresponsible for the processing of emotional expressions.Thus, pharmacological interventions can alter thecommunicatory salience of emotional expressions. Forexample, serotonergicmanipulationshave been foundtoPhil. Trans.R. Soc. Lond. B (2003)



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Facial expressions,ommunicationnd neural ubstratesR. J.R. Blair 565differentiallyffectthe processing of fearful nd happyexpressions Harmer etal. 2001a), noradrenergicmanipu-lations to differentiallyffect the processing of sadexpressions (Harmer et al. 2001b) whereas dopaminergicand GABAergic manipulations differentiallyffect theprocessingofangry xpressions Borrilletal. 1987; Blair &Curran 1999; Zangara et al. 2002). Given these differen-tial effectsone mightpredict that the serotonergicandnoradrenergicmanipulations are differentiallyffectingthe amygdala's role in responding to fearful, ad andhappy expressions as unconditioned stimulifor aversiveand appetitive conditioning and instrumental earning,whereas GABAergic manipulations impact the role oforbital frontal ortex n modulatingthe response to inter-personal signals of conflict uch as anger. Certainly, t isknown thatthere s considerable serotonergic nd norad-renergic nnervation f the amygdala (Amaral etal. 1992)and the impact of noradrenergicmanipulations of theamygdala's role in the augmentationof episodic memoryis well known (Cahill & McGaugh 1998; Cahill 2000).There are highconcentrations fbenzodiazepine receptorsites in both amygdala and the frontal ortex (Dennis etal. 1988; Bremner et al. 2000). However, although thecentral nucleus of the amygdala which projects to auto-nomic centres n the brain stem is denselyinnervatedbyGABA neurons,the basolateral nucleus of the amygdala,projecting to cortical regions, contains only scatteredGABA neurons (Swanson & Petrovich1998). It is plaus-ible that the basolateral nucleus, as a functionof ts inter-connections with cortical regions, is more involved inrespondingto fearful xpressions nd thusrelatively naf-fectedby GABAergic manipulations.At presentonlyone study, o my knowledge,has exam-ined the neuralunderpinnings ftheeffects f thesephar-macological agents (Blair et al. 2003). This investigatedthe impact of diazepam on the neural response tomorphed angry and fearful expressions. Interestingly,while diazepam abolished the increase in lateral orbitalfrontal cortex activityas a functionof increased angryexpressionintensity, he increase in amygdala activity sa function f ncreasedfearfulxpression ntensity as notaffected y diazepam. This study hus adds supportto thesuggestion hatGABAergic manipulations mpacttheroleof orbital frontal cortex in modulating the response tointerpersonal ignals of conflict uch as anger.

5. ACKNOWLEDGINGOTHER INDIVIDUALS'EXPRESSIONS: CLOSING THECOMMUNICATORY OOPIn thispaper the communicatory unctionof emotionalexpressionshas been stressed. Reference was made to acrucial determinant f whether n expressionwill be elic-ited: the presence of others Jones & Raag 1989; Chovil1991; Fridlund 1991; Joneset al. 1991). Individuals typi-cally display expressionswhen there s an audience to wit-ness theseexpressions.This might uggestthat ndividualsshould stop displayingemotional expressionswhen the

audience has demonstrated thattheyhave registered hedisplay of the emoter. Thus, for example, in the socialreferencing xample providedabove, the caregiver houldstopto displayfearwhen the nfant emonstrates hattheywill now not approach theaversivenovel object. However,

although this would intuitively ppear to be the case, Iknow ofno empirical iterature emonstratingt to be so.One particular case where there are clear indicationsthat the audience demonstratesthat theyhave registeredthe display of the emoter is seen during embarrassmentdisplays.Embarrassment s associated withgaze aversion,shifting ye positions, speech disturbances,face touches,a nervous smile and a rigid,slouched posture (Goffman1967; Asendorpf 1990; Lewis et al. 1991). More recentwork has demonstrated that embarrassment displayunfolds in the followingreliable sequence. This involvesgaze aversion; a smile control, which is a lower facialaction thatpotentiallynhibits he smile; a non-Duchennesmile, which only involves the zygomaticmajor muscleaction thatpulls the cornersof the lips upwards; a secondsmile control; head movements down; and then facetouching,which occurred ca. 25% of the time (Keltner1995).Leary & Meadows (1991), Leary et al. (1996) andothers (Keltner 1995; Miller 1996; Gilbert 1997;Keltner& Buswell 1997) have suggestedthat embarrass-ment serves an importantsocial functionby signallingappeasementto others.When a person's untowardbehav-iour threatens his/herstanding in an important socialgroup, visible signs of embarrassment unctionas a non-verbalacknowledgementofshared social standards.Learyarguesthatembarrassment isplaysdiffusenegativesocialevaluations and the likelihood of retaliation. The basicidea is that embarrassmentserves to aid the restorationofrelationshipsfollowing ocial transgressionsKeltner &Buswell 1997). In otherwords, embarrassmentdisplaysmay be initiatedby an individual followingan emoter'sdisplayofanger: fthe ndividual's behaviourwas uninten-tional or the angryobserver s ofhighstatus.There is a good deal of empirical evidence to supportthis appeasement' or remedialfunction fembarrassmentfrom studies of both humans and non-human primates(Leary & Meadows 1991; Gilbert 1997; Keltner &Buswell 1997; Keltner & Anderson 2000). For example,Semin & Manstead (1982) found that people reactedmore positively o others after social transgressionfthetransgressorswerevisibly mbarrassed. n addition,Learyet al. (1996) presented evidence that people are actuallymotivatedto conveyembarrassment o others as a way ofrepairing heirsocial image.6. PATHOLOGICALEXPRESSION PROCESSING:THE CASES OF AUTISM,DEVELOPMENTALPSYCHOPATHY ANDACQUIRED SOCIOPATHYIf emotional expressions serve a communicatoryfunc-tion,as I have been arguing,we might xpect thatatypicalrespondingto the emotional expressionsof otherswouldadversely ffect evelopment.Three ways in which devel-opmentcan be affectedwillbe discussed below withrefer-ence to the neuro-psychiatric conditions of autism,developmentalpsychopathy nd acquired sociopathy.Autism s a severedevelopmentaldisorder described by

the American Psychiatric Association's diagnostic andstatisticalmanual (DSM-IV) as 'the presence ofmarkedlyabnormal or impaired development in social interactionand communication and a markedlyrestricted epertoireof activities and interests' American PsychiatricAssoci-Phil. Trans. R. Soc. Lond. B (2003)



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566 R. J.R. Blair Facial expressions,ommunicationnd neural ubstratesation 1994, p. 66). The main criteriaforthe diagnosis inDSM-IV can be summarized as qualitative mpairmentnsocial communication and restricted nd repetitivepat-terns of behaviour and interests.These criteriamust beevident before3 yearsof age.As long as autism has been recognized, the idea hasexisted that the main difficultyorpeople with autism isan inabilityto enter into emotional relationships.Thus,Kanner, the psychiatristwho originally escribedthe dis-order in 1943, wrote these children have come into theworld withan innate inability o form the usual, biologi-cally provided affective ontactwith otherpeople, just asother childrencome into the world with innate physicalor intellectualhandicaps' (Kanner 1943, p. 250). Morerecently, t has been suggested that autism is due to aninnate impairment n the abilityto perceive and respondto the affectivexpressionsof others,and that this deficitleads to their profound difficultiesn social interaction(Hobson 1993).Many studieshave investigated he ability f ndividualswith autism to recognize the emotional expressions ofothers.Many have reported hatchildrenwith utism havedifficulty ecognizingthe emotional expressionsof others(Hobson 1986; Bormann-Kischkelet al. 1995; Howard etal. 2000) witha recentclaimsuggesting hat this s specificforfearful xpressions Howard etal. 2000). However,theabove only applies to studieswhere the groups have notbeen matched on mental age. When they are, childrenwith autismhave usuallybeen foundto be unimpaired nfacial affect ecognition Ozonoff et al. 1990; Prior et al.1990; Baron-Cohen etal. 1997b; Adolphs et al. 2001). Inaddition, several studies have found the emotion pro-cessing mpairment o be pronounced onlywhenthe emo-tion is a complex 'cognitive' emotion such as surpriseorembarrassment Capps et al. 1992; Baron-Cohen et al.1993; Bormann-Kischkelet al. 1995).I would therefore rgue thatautism does not representa disorderwherethere s atypicalrecognition femotionalexpressions.However, autism is interesting ecause of thewell-documented mpairmentn theory f mind shownbypatientswiththis disorder (Frith 2001). Theory of mindrefers o theability o represent hemental states ofothers,i.e. theirthoughts,desires,beliefs, ntentions nd knowl-edge (Premack & Woodruff 1978; Leslie 1987; Frith1989). Impairment n theory f mind is interestingor hecommunicatoryrole of emotional expressions. Thus, ahealthy ndividual,whenwitnessing he emotionaldisplayof another individual, will attempt to represent theintended cue that elicitedthe emoter's expression.So, forexample, during ocial referencing,fthe child s attendingto one object when the caregiver displays an emotionalresponse to another,the child will look at the caregiver odeterminethe direction of their attention (Moses et al.2001). Theoryofmindshouldbe involved ntherepresen-tationofthe emoter's intention. f it is, we mightpredictanomalous behaviouralreactionsto the emotionaldisplaysof other individuals in childrenwith autism given theirtheory-of-mindmpairment. n particular,we should seea reduction n theusual orientation esponseto theemoterto calculate the elicitingstimulus. Indeed, this is exactlywhat is seen in childrenwith autism. A series of studieshas examined the behaviouralreactionsof ndividualswithautism when the child has been playingwiththe exper-

imenter and the experimenterhas feignedan emotionalreaction,usuallydistress Sigman et al. 1992; Dissanayakeet al. 1996; Bacon et al. 1998; Corona et al. 1998). Allfourof these studies have reportedreduced orientation othecaregiver ythechildrenwithautismalthoughthiswasonly n the lower ability ample in theBacon et al. (1998)study.However, thisdoes not reflect lack ofresponsive-ness to other individuals' emotion. A child with autismpresented with another individual in distresswill showaversive autonomic arousal to the other's distress Blair1999) and, as has been arguedabove, childrenwithautismpresent with no impairment in expression recognition(Ozonoffet al. 1990; Prioretal. 1990; Baron-Cohen et al.1997b; Adolphs et al. 2001).The above argument generates furtherpredictionsabout emotion in autism. Social referencing,he learningof emotional valence fornovel objects,should be impairedin childrenwith autism. The childwithautismshould failto use the emoter'sgaze directionto calculate the correctobject to associate thevalence elicitedbythe emoter'sdis-play in the same waythattheyfail to use a speaker's gazedirectionduringnovel word use to calculate the speaker'sreferentBaron-Cohen et al. 1997a). This, in turn,pre-dicts that childrenwith autism may present with veryunusual emotional reactions to objects. That is, withoutrepresentinghe emoter's referent heymay associate val-ence to novel objects inappropriately r not at all.Psychopathy s a developmentaldisordercharacterizedin partby callousness, a diminishedcapacityforremorse,impulsivitynd poor behavioural control Hare 1991). Itis identifiedn childrenwiththe antisocialprocess screen-ing device (Frick & Hare 2001) and in adults with therevisedpsychopathy hecklist (Hare 1991). Importantly,this disorder s not equivalentto thepsychiatric iagnosesof conduct disorder or antisocial personalitydisorder(American PsychiatricAssociation 1994). These psychi-atricdiagnoses are relatively oorlyspecifiedand concen-trate lmost entirely n the antisocial behaviour shownbythe individual rather han any form of functional mpair-ment. Because of this lack of specification, ates ofdiag-nosis of conduct disorder reach up to 16% of boys inmainstream education (American PsychiatricAssociation1994) and rates ofdiagnosis of antisocialpersonalitydis-order are over 80% in forensic nstitutionsHart & Hare1996). Because of these high rates of diagnosis, popu-lations dentifiedwith hesediagnostictools arehighly et-erogeneous and also include many individuals with otherdisorders.Psychopathy,n contrast, s shownby less than1% of ndividuals nmainstream ducation (Blair & Coles2000) and less than 30% of individuals incarcerated inforensic nstitutionsHart & Hare 1996).One account ofpsychopathyhas linked the disorder toearly amygdala dysfunction nd consequent impairmentin processing fearful and sad expressions (Blair 1995,2001; Blair et al. 1999). The basic suggestion is thatpsychopathic ndividualsrepresent hedevelopmentalcasewheresad and fearful xpressionsare not aversiveuncon-ditioned stimuli.As a consequence ofthis,the individualdoes not learn to avoid committing ehaviours thatcauseharmto others and will commit themif,by doing them,he receives reward (Blair 1995). In line withthis theory,psychopathic ndividuals have been foundto presentwithreduced amygdaloidvolume relativeto comparison indi-

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Facial expressions,ommunicationnd neural ubstratesR. J.R. Blair 567viduals (Tiihonen et al. 2000) and reduced amygdalaacti-vation, relative to comparison individuals, during anemotional memorytask (Kiehl et al. 2001) and aversiveconditioningtasks (Veit et al. 2002). Moreover, in func-tionsthatrecruit he amygdalasuch as aversive ondition-ing and instrumentalearning, he augmentationof startlereflex yvisual threatprimesor arousal to the anticipationofpunishment re all impaired npsychopathic ndividuals(Blair 2001). Also in line with the theory,psychopathicindividuals show pronounced impairment n processingsad and fearfulexpressions. They show reduced auto-nomic responses to these expressions Aniskiewicz 1979;Blair et al. 1997) and, particularlyn childhood, impairedabilityto recognize these expressions (Blair et al. 2001).Finally, their socialization is markedly mpaired. Thus,although it has been repeatedlyshown that the use ofempathy nducing positiveparenting trategies y caregiv-ers decreases the probabilityof antisocial behaviour inhealthydevelopingchildren, t does not decrease theprob-ability f antisocialbehaviour n childrenwho presentwiththe emotional dysfunctionof psychopathy(Wootton etal. 1997).Acquired sociopathyrepresents n interesting ounter-point to developmental psychopathy. Acquired sociopa-thy' was a term introducedby Damasio et al. (1990) tocharacterize ndividualswho,following cquired lesions ofthe orbitofrontalortex,fulfil heDSM-III diagnosticcri-teria for 'sociopathic disorder' (American PsychiatricAssociation 1980). Previously,Blumer & Benson (1975)had used the term 'pseudo-psychopathy' to refer topatientswith frontal obe lesions presenting n this man-ner. Althoughthere have been suggestionsthat develop-mental psychopathyand acquired sociopathy might bedifferentorms f the same disorder Damasio 1994), thisnow appears unlikely Blair 2001). Indeed, developmentalpsychopathy nd acquired sociopathy presentverydiffer-ently. Psychopathic individualspresentwithpronouncedlevels of goal-directedinstrumental ggressionand anti-social behaviour,reflectingn impairment hat interfereswiththeir bility o be socialized (Cornell et al. 1996). Incontrast,patientswith acquired sociopathy presentwithfrustration- r threat-induced eactiveaggressionwhethertheir cquired lesion ofthe orbitalfrontal ortex occurs inchildhood (Pennington& Bennetto 1993; Anderson et al.1999) or adulthood (Grafmanetal. 1996; Blair & Cipol-otti 2000).I have argued for the communicatory ole of angry ndembarrassment expressions in regulating social hier-archical interactions, in particular, the role of angryexpressions n stoppingthe current ehavioural action andthe role of embarrassmentdisplays in communicatingalack of intent to commit the action that has resulted insocial disapproval.We might xpecttherefore hat an indi-vidual whose response to angry/embarrassmentexpressions s dysfunctionalhould presentwith mpairedmodulation of their social behaviour. The orbital frontalcortexis implicated in the response to angry expressions(Sprengelmeyer tal. 1998; Blair etal. 1999; Kesler-Westet al. 2001). Interestingly,hen, patients with acquiredsociopathy following esions of the orbital frontal ortexpresentwithgenerally mpairedexpressionrecognition utthis impairment is particularly marked for angryexpressions Hornak et al. 1996; Blair & Cipolotti 2000).

The strongsuggestion is therefore hat this impairmentunderliestheirsocially inappropriatebehaviour.7. CONCLUSIONS

In thispaper, I have stressed the communicatoryfunc-tion of emotional expressions. Importantly, he argumentis not that the display of expressions implies that theemoter intended to convey a specific message to theobserver, t is simplythat emotional expressions serve acommunicatory function. Crucially, the emoter'semotional displays are a function of the presence ofobserversand the observer will attemptto determine thereferent f the emoter's display. Assuming the observeraccomplishes this,appropriate nformationwill have beentransferred romthe emoter to the observer.Although emotional expressions are not intentionalcommunications, their display can be intentionallymanipulated.Children learndisplayrules; social rules thatstipulatewhen it is, and when it is not, appropriate todisplayemotionalexpressions.Thus we can learn to inten-tionallymask or alter our expressions s a function f thesedisplayrules. Presumably,the emoter's intent modulatesthe frontal obe-basal gangliacircuitryhat has been impli-cated in the production of emotional expressions.Although ystemsgenerally nvolved n processingfacialstimuli, such as the occipital cortex, fusiform nd thesuperior temporal sulcus process expressions, the com-municatory unctionof emotional expressions s reflectedin thepartlydissociable neural systems hat are addition-ally involved in processing emotional expressions. Thus,expressionsthat serve as positive or negative reinforcerspreferentiallyctivate the amygdala (fearfulness, adnessand happiness). Although disgusted expressions are alsoreinforcers,hey re used mostfrequentlyo provide nfor-mation about foods. As such they engage the insula, aregion involved in taste aversion. Angry expressionsinitiateresponse reversal and activate regions of orbitalfrontal cortex that are involved in the modulation ofbehaviouralresponding.If we assume that emotional expressionsserve a com-municatoryfunction,we must predict that theywill bemore likelyto be displayed when a potential observer ispresent.This is indeed the case. In addition,we mustpre-dict that the display of the expressionwill be terminatedwhen the observer has shown clear indication that theyhave received the communication. This remains to beinvestigated.The consequences of impairment in being able toadequately process the emotional displays of others canbe severe. I have argued that although individuals withautismmaybe able to recognizethe expressionsofothers,it is highly ikelythat theyfail to adequately process theemoter's referent nd thattheytherefore rocess the dis-play incorrectly ecause of their mpairment n theoryofmind. In contrast, ndividualswith thedevelopmentaldis-order ofpsychopathy nd individuals withacquired soci-opathyfollowing esions of the orbital frontalcortex failto respond appropriately to specific expressions. Inpsychopathic ndividuals,the processingof other ndivid-uals' sadness and fear is particularly ffected.This leadsto a failure n socialization. The psychopathic ndividualdoes not learnto avoid actions thatcause harm to others.




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568 R. J.R. Blair Facial expressions,ommunicationnd neural ubstratesIn acquired sociopathy, the processing of others' angerand probablyembarrassment s particularly ffected. hisleads to a failure to adequately modulate behaviouraccording to the social context.In short,emotional expressions allow the rapid com-munication of valence informationbetween individuals.They allow the observer o rapidly earnwhichbehavioursand objects (includingfoods) to approach or avoid, as wellas information llowing rapid modification of behaviouraccording to the social environment and hierarchy.Impairment in systems that respond to the emotionalexpressionsof others can have devastating ffects.

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de Gelder,B., Vroomen,J.,Pourtois,G. & Weiskrantz, .1999 Non-conscious ecognitionf affectn theabsenceofstriate ortex.NeuroReport0, 3759-3763.Dennis,T., Dubois, A., Benavides,J.& Scatton,B. 1988 Dis-tribution f central mega 1 (benzodiazepinel)and omega2 (benzodiazepine2)receptor ubtypesn themonkey ndhuman brain.An autoradiographictudywith 3H]flunitra-zepam and theomega 1 selective igand [3H]zolpidem.J.Pharmacol. xp. Theor. 47, 309-322.Dias, R., Robbins,T. W. & Roberts,A. C. 1996 Dissociationinprefrontalortex faffectivend attentionalhifts. ature380, 69-72.Dissanayake,C., Sigman,M. & Kasari,C. 1996 Long-termstabilityf individualdifferencesn the emotionalrespon-siveness f childrenwith utism.J. ChildPsychol. sychiat.37, 461-467.Drevets,W. C., Lowry,T., Gautier, C., Perrett,D. I. &Kupfer, . J.2000 Amygdalar lood flow esponses o faci-ally expressed adness.Biol. Psychiatry7(Suppl. 8), 160S.Ekman,P. 1997 Should we call it expression r communi-cation? nnovationsocialSci. Res. 10, 333-344.

Ekman,P. & Friesen,W. V. 1969 The repertoirefnonverbalbehavior: ategories, rigins, sage,and coding.Semiotica ,49-98.Ekman,P. & Friesen,W. V. 1976 Picturesf acialaffect.aloAlto,CA: Consulting sychologistsress.Everitt, . J.,Cardinal,R. N., Hall,J.,Parkinson, .A. & Rob-bins,T. W. 2000 Differentialnvolvementfamygdala ub-systemsn appetitive onditioningnd drugaddiction. nTheamygdala: functionalnalysised. J.P. Aggleton), p.289-310. OxfordUniversityress.Fine,C. & Blair,R.J.R. 2000 Mini review: hecognitivendemotional ffectsfamygdala amage.Neurocase, 435-450.Frick,P. J.& Hare, R. D. 2001 Theantisocialrocesscreeningdevice. oronto,Ontario:Multi-Health ystems.Fridlund,A. J. 1991 Sociality fsolitary miling: otentiationby an implicit udience.J. Personalityocial Psychol. 0,229-246.Frith, U. 1989 Autism: explainingthe enigma. Oxford:Blackwell.Frith, . 2001 Mindblindnessnd thebrain nautism.Neuron32, 969-979.George,M. S., Ketter, . A., Gill,D. S., Haxby,J.V., Unger-leider,L. G., Herscovitch, . & Post, R. M. 1993 Brainregionsnvolvednrecognizingacial motion r dentity:noxygen-15 ET study. . Neuropsychiatry, 384-393.Gilbert, . 1997 The evolution f socialattractivenessnd itsrole in shame,humiliation, uiltand therapy. r.J. Med.Psychol. 0, 113-147.Goffman,E. 1967 Interaction itual: essayson face-to-facebehavior. ardenCity,NY: Anchor.Gorno-Tempini,M. L., Pradelli, ., Serafini, ., Pagnoni,G.,Baraldi,P., Porro,C., Nicoletti,R., Umita,C. & Nichelli,P. 2001 Explicit nd incidental acial xpression rocessing:an fMRI study.Neuroimage4, 465-473.Grafman,J., Schwab, K., Warden, D., Pridgen,B.S. &Brown,H.R. 1996 Frontal lobe injuries,violence, andaggression: reportof the Vietnam head injurystudy.Neurology 6, 1231-1238.Halgren,E., Raij, T., Marinkovic,K., Jousmaki, . & Hari,R. 2000 Cognitive esponseprofile f the humanfusiformface area as determinedyMEG. Cerebr. ortex 0, 69-81.Hare, R.D. 1991 The Hare psychopathyhecklist: evised.

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GLOSSARYCS: conditionedtimulusUS: unconditionedtimulus


facial expressions, their communicatory functions

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