The neuropsychology of infants' pro-social preferences

(1)

ContentslistsavailableatScienceDirect

Developmental Cognitive Neuroscience

jo u rn al h om ep age : ht t p : / / w w w . e l s e v i e r . c o m / l o c a t e / d c n

The neuropsychology of infants’ pro-social preferences

Gustaf Gredebäck

^a,∗

, Katharina Kaduk

^b

, Marta Bakker

^a

, Janna Gottwald

^a

, Therese Ekberg

^a

, Claudia Elsner

^a

, Vincent Reid

^b

, Ben Kenward

^a

aUppsalaChildandBabylab,UppsalaUniversity,Sweden

bDepartmentofPsychology,LancasterUniversity,UnitedKingdom

a r t i c l e i n f o

Articlehistory:

Received9October2014

Receivedinrevisedform21January2015 Accepted21January2015

Availableonline28January2015

Keywords:

ERP P400 Prosocial Empathy Infant EEG

a b s t r a c t

Thecurrentstudyistheﬁrsttoinvestigateneuralcorrelatesofinfants’detectionofpro-and antisocialagents.DifferencesinERPcomponentP400overposteriortemporalareaswere foundduring6-month-olds’observationofhelpingandhinderingagents(Experiment1), butnotduringobservationofidenticallymovingagentsthatdidnothelporhinder(Exper- iment2).TheresultsdemonstratethattheP400componentindexesactivationofinfants’

memoriesofpreviouslyperceivedinteractionsbetweensocialagents.Thisleadstosuggest thatsimilarprocessesmightbeinvolvedininfants’processingofpro-andantisocialagents andothersocialperceptionprocesses(encodinggazedirection,goaldirectedgraspingand pointing).

1. Introduction

Pioneering work by Premack and Premack (1997) demonstratedthat1-year-oldinfantsattributegoalstoani- matedagentshelpingorhinderingeachother,suggesting thattheseeventsarevaluedaspositiveandnegativeby theinfants. This initialﬁnding hasbeen replicated and extendedinseveralways.Infantsfrom3monthsofage express different preferences for animated agents that eitherhelp(pro-social)orhinder(anti-social)anothergeo- metricshapefromclimbingahill(Hamlinetal.,2010).At thisageinfantslooklongertowardthehelperthanthehin- derer,theeffectbeingdrivenbyatendencytoavoidlooking attheanti-socialagent.At6 months,once infants’own manualcapabilitieshavedeveloped,infantssystematically

∗ Correspondingauthorat:vanKraemersalle1,SE-75142Uppsala, Sweden.Tel.:+460701679414.

E-mailaddress:gustaf.gredeback@psyk.uu.se(G.Gredebäck).

reachforpro-socialagentswhengivenachoicebetweena helperandahinderer(Hamlinetal.,2007).

Theseinitialpro-socialpreferencesaremorecomplex duringthesecondhalfoftheﬁrstyear,beinginﬂuenced by the social context in which an interaction occurs.

Eight-month-oldspreferagentsthatactpositivelytoward pro-socialothersandnegativelytowardanti-socialothers (Hamlinetal.,2011)whereas9-month-oldspreferagents thattreatsimilarotherswellanddissimilarotherspoorly (Hamlinetal.,2013a).At1yearofage,infantsnotonly attributedispositionalstatestotheseinteractinggeomet- ricshapes(Kuhlmeieret al.,2003)but alsopredictthat agents willseekoutothers thathave previouslyhelped them(FawcettandLiszkowski,2012).

Scarf et al. (2012) have criticized the interpretation made by Hamlin et al. (2007). Instead of focusing on helping and hindering actions,Scarf etal. (2012) argue that infantspreferagents thatareassociatedwithposi- tiveevents. Althoughthis wasa reasonable criticismof the originalstudy this alternative interpretationcannot accountfortheconceptualreplicationsofthismethodthat

http://dx.doi.org/10.1016/j.dcn.2015.01.006

by-nc-nd/4.0/).

(2)

havebeenperformedusingdifferentstimuli(Hamlinetal., 2013b;HamlinandWynn,2011),norcanitaccountforthe subsequentmorecomplexﬁndingsthatinfants’prosocial preferencesarenotrigidbutdependoncontext(Hamlin etal.,2011,2013a,b).Insum,thereiscurrentlysubstan- tialsupportforthenotionthatinfantsareabletointerpret theinteractionofanimateagentsaspro-oranti-socialand thattheyusethisinformationtoguidetheirattentionand reachingactions(forareviewseeHamlin,2013,2014).

Severaldifferentinterpretationshavebeenproposedto accountforinfants’evaluation ofactions’social valence.

One possibility is that early-emerging mentalistic processes such as theory of mind and perspective taking (Kovacs et al., 2010; Onishi and Baillargeon, 2005;

Southgate et al., 2007) mediate infants’ pro-social preferences (Hamlin et al., 2013b). In fact, Hamlin et al.

(2013b) suggest, based on modeling of empirical data, that10-month-olds’pro-socialpreferencesmightinvolve second-order mental-state representations. That is, the goalofoneagentrelatestotheintentionofanother(here referredtoasthementalisticaccount).

In adults and children the temporal parietal junc- tion(TPJ),andwithincreasedagethepre-frontalcortex (Kobayashietal.,2007),areoftenimplicatedinmentalistic processes(VanOverwalleandBaetens,2009),alongwith activationin thesuperiortemporal sulcus(STS; Decety, 2011;DecetyandHoward,2013;Molletal.,2002).Basedon neuropsychologicalinvestigationsofempathyconducted withadults andolder children,alternative accountsare alsopossible.It isconceivablethatsomepro-socialpreferences are governedby lower level social perception processes,whichrelateactionstogoalswithouttheneed formentalizing(herereferredtoasthesocialperception account).Severalindicationssuggestthattheseprocesses areorganizedbytheSTSwithoutnecessaryinvolvementof highercognitivefunctions.Adultsshowedmoreactivation oftheSTSforanimatedgeometricalshapesthatappeared tointeractinanintentionalmannerwhencomparedtoran- dommovements,theactivitybeingrelatedtoparticipant’s ratingsofintentionality(Castellietal.,2000).Inchildren, arecentfMRIstudydemonstratedthattheSTS(asoneof severalareas)issensitivetoperceivedintentionalharmin others(Decetyetal.,2012).OnalargerscaletheSTSissen- sitivetobody movementandgoaldirectedactionssuch asreachingandlooking,inadditiontobeingsensitiveto facesandemotionalexpressionsingeneral(Allisonetal., 2000).

Thecommondenominatorofthementalisticandsocial perception accounts of processing of socially valenced actionsisthereforetheinvolvementoftheSTS.Ininfants it hasbeen arguedthat theP400ERPcomponent is an indexofSTSactivity(Gredebäcketal.,2010).Therearesev- erallinesofenquirythatsupportthisassumption.Firstof all,theP400isoftendescribedasaninfantversionofthe adultN170–N200(alongwiththeinfantN290;deHaan et al.,2002;Nelsonetal., 2006).Thisis basedonstud- iesthatdemonstrateinfantP400andadultN170–N200in responsetoidenticalstimuli(Gredebäcketal.,2010;Senju etal.,2006)andtheobservationthatsimilarmanipulations altertheamplitudeofinfantP400andadultN170–N200 components(Csibraetal.,2008).TheN170–N200inturn

hasbeendirectlyrelatedtotheSTSviasourcelocaliza- tion and joint EEG, fMRI measures (Puce et al., 1998;

Itier and Taylor, 2004; Dalrymple et al., 2011).On the basisofthesearguments,and theobservationthatboth accountsinvolveSTSactivity,wehypothesizethataninfant P400ERPcomponentindexesprocessingofactions’social valence.

Nostudyhasinvestigatedtheneuralcorrelatesofpro- socialpreferencesinyounginfants.However,afewstudies havedemonstratedthattheinfantERPcomponentP400is relatedtoprocessingofgoaldirectedactionssuchasgrasp- ing(Bakkeretal.,inpress)andpointing(Gredebäcketal., 2010;Melinderetal.,inpress), toemotionalprocessing (Leppanenetal.,2007),biologicalmotion(Reidetal.,2006) andgazedirection(Senjuetal.,2006).Inthiscontextitis importanttonotethatP400amplitudesarelargerforfunc- tionalandgoaldirectedactions(reachingfor,orpointing towardobjects,lookingatinterestingsights)thancontrol stimulithatlacktheseobjectdirectedproperties.

Inthisstudyweexaminetheneuralcorrelatesofinfants’

pro-socialpreferencesbymeasuringEEGandtargetERP componentshypothesizedtobesensitivetopro-andanti- socialagentsinthehill-climberparadigm(Hamlinetal., 2007).More speciﬁcally,6-month-oldinfantswerepre- sentedwithtwoscenarios.InExperiment1oneagenthelps anotheragent(ballwitheyes)toreachthetopofahill, whereasadifferentagenthindersthecircularagentfrom reachingthetopofahill.InExperiment2oneagentpushes upaninanimateball(withouteyes)tothetopofthehill andanotheragentpushedtheballdownthehill.Follow- ingthesescenariosinfantswerepresentedwithrepeated imagesofthetwoagentsthathelpedorhinderedinExper- iment1andmovedupvsdowninExperiment2(onlyone imagewaspresentedoneachtrial)andERPcomponentsfor theseimageswereanalyzed(forsimilardesignsseeKaduk etal.,2013;Pariseetal.,2008).

We hypothesize that P400 amplitudes will differ betweenpro-andanti-socialagents(Experiment1).Fur- thermore, given that prior studies have demonstrated largeramplitudesof P400forcongruentthanincongru- entpointing (Gredebäcketal.,2010)andgazedirection (Senjuetal.,2006),aswellasforuprightoverinvertedbio- logicalmotionpoint-lightdisplays(Reidetal.,2006),we predictalargerP400inresponsetoagentsthatpreviously havehelpedoveragentsthatpreviouslyhinderedothers.

Thehypothesizedcommondenominatorofpreviouslyand currentlyinvestigatedsocialstimuliisalargerP400ampli- tudeforfunctionalandtypicalsocialbehavior(pointingto objects,lookingatinterestingsights,andagentsthathelp others).NodifferenceinP400amplitudesisexpectedin Experiment2wheretheagentthatisbeinghelpedand/or hinderedisreplacedbyaninanimateball.

WealsoanalyzedtheNccomponent.Thismid-latency componentoccursapproximately300–700msafterstim- ulus onset and is most prominent at fronto-central electrodes.Itreﬂectsattentionalorientingtosalientstimuli (Courchesne et al., 1981) and/or a general attentional arousal(Richards,2003),asitislargertoinfrequentthan frequentstimuli(e.g.Courchesneetal.,1981)andislarger duringperiodsofsustainedattention(Richards,2003).We examinedtheNcinordertoprecludeattentionandother

(3)

lowerlevelaccountsthatmayprovideanalternativeexpla- nation for differences found betweenconditions in the P400.

2. Experiment1 2.1. Methods

2.1.1. Participants

Fourteen6-month-oldinfants(eightfemale;meanage 6months,3days,range5months,27daysto6months, 12days)wereincludedinthefinalanalysis.Anadditional 11infants(fivefemale)wereexcludedsincetheydidnot passtheinclusioncriteriaofatleast10artifactfreetrials perstimulusset(helper/hinderer).Noneoftheseinfants participatedinExperiment2.Parentssignedaconsentform priortoparticipationandreceivedagiftcertificate(100 SEK).Thelocalethicalcommittee,inaccordancewiththe declarationofHelsinki,approvedthestudy.

2.1.2. Stimuliandprocedure

Eachparticipatinginfantwaspresentedwithtwosets of stimuli, one training set and one test set, created in Blender, an open source 3D animation environment (www.blender.org).Thetrainingsetincludedsixmovies (threehelperandthreehinderer)inwhichaprotagonist(a redballwitheyes)attemptedandfailedtoclimbahill.In eachmovietheprotagonistmadethreefailedattemptsto climbthehillafterwhichtheprotagonistwaseitherhelped orhinderedbyanothergeometricshape(abluesquareora yellowtrianglewitheyes,seeFig.1).Themovieswerepre- sentedinacounterbalancedorder(helperorhindererﬁrst), withsquareandtrianglerandomlyassignedtobehelperor hinderer.Eachmoviewas14slongandwasprecededby ablackscreen(duration3spriortoﬁrstmovie,2sprior toallremainingmovies).Thetotaldurationoftheentire trainingsessionwas97s(judgedbytheauthorstobethe maximumamountoftimethatinfantswouldattendtothe trainingstimuliandthesubsequentteststimuli).

Thehinderer moviesstartedwithastillimageofthe hill(1000ms).The protagonistemerged from theright, climbedtheﬁrsthalfofthehillandthenbouncedupand downthreetimes(afterwhich4000mswereelapsedsince moviestart).Theprotagonistthentriedunsuccessfullyto climbthesteeper secondhalfofthehill.Thesemotions wereintendedtoestablishtheprotagonistasanagentin needofassistancebecauseitwasunabletoreachitsgoal.

Movementsoftheprotagonistduringtheseeventswere accompaniedbyasoundhighlightingthemovementsof theball.Followingtheseinitialeventsthehindererentered fromthetopofthehill(7700mselapsed)andpushedthe protagonistallthewaydownthehillbeforereturningto itsinitialpositionanddisappearing(13100ms).Themovie endedwithastationarypicturedepictingtheprotagonist atthebottomofthehill.Intotalthemovielasted14s.The helpermovieshadanidenticaltimingandoverallstructure, exceptthatthehelperappeared frombelowandhelped theprotagonistby pushingit upthehill.Asthe helper movedbackdownthehill,theprotagonistbouncedthree timesonthehilltop.Thismovementendedjustbeforethe helperdisappearedfromthescreenatthebottomofthe

hill.Thehelperandhindererhadmovingeyesandgazedat theprotagonistastheyinteractedwithit.Theprotagonist’s eyesalwaysﬁxateditsgoalatthetopofthehill.Ineach moviethehelperandhindererwereaccompaniedbydif- ferentsoundshighlightingtheirmovements,withaslightly lowerpitchedsoundalwaysaccompanyingthetriangleand aslightlyhigherpitchedsoundaccompanyingthesquare.

Thetestsetof40trialsrandomlyalternatedstillimages ofthehelperandhinderer(20trialseach),positionedat themiddleofthehill.Eachtrialconsistedofablackpicture withaﬁxation-cross(duration1200–1400ms)followedby animageofthehelperorhinderertogetherwithitscor- respondingsound(imageduration400ms,soundduration 250ms).Thistargetstimuluswasthenfollowedbythenext ﬁxationcrossandthenextstimulusimage.

In ordertoincreaseparticipants’opportunitytopro- cessthetrainingmaterial,participatingfamiliesweresent internet links tothe training setand asked towatch it together with their child on the two consecutive days immediatelyprior to theexperiment day.Parentswere instructedtowatchthemoviesinfullscreenmodein a quietenvironmentwithoutdistractions.Parentswerealso informed thatpresenting themovies moretimes might reducetheirinfant’sattentiontothestimulionceinthelab.

Allparentsreportedthattheyhadfollowedtheseinstruc- tionswhenaskedonarrivaltothelab.

Duringthelabsessionparticipantsoncemoreviewed thetraining setand directlythereafterthetest set.The studywasawithinsubjectdesign,assucheachinfantwas presentedwithbothhelperandthehinderertrials.Once thetestsetwascompleted,orifinfantslostattentiontothe screen,thetrainingsetwaspresentedoncemorefollowed bythetestset.Thestimuliwererepeateduntilparticipants stoppedattending.Onaverageinfantsattendedto48trials (range24–59)oftheteststimulidepictingthehelperand 48 trials(range24–58)ofthetest stimulidepictingthe hinderer.

2.1.3. EEGrecordingandanalysis

Age appropriate 128-channel Geodesic Sensor Nets (HCGSN130;EGI,Eugene,OR)wereusedtorecordEEGsig- nals.Thesignal(vertexreferenced)wassampledat250Hz, amplifiedbyEGINetamplifier(GES300Amp;EGI,Eugene, OR)andstoredforoff-lineanalysis.ContinuousEEGdata were digitally filtered (0.3–30Hz) and segmented from 200mspriortotheappearanceoftheagentto1000ms aftertheagent’sappearance.Theelectrodesfromthemost anteriorandposteriorareawerenotincludedinthefinal analysisduetohighnoisecausedbypoorcontactwiththe scalp.Intotal,38electrodeswereexcludedfromtheanaly- ses(seeFig.2).Onremaining90electrodesartifactswithin trials wereinitially definedaschannelswithmorethan 200␮Vchangeinamplitude.Thedatawerethenmanu- allycheckedforartifacts.Onaverage21helpertrialsper infant(range13–34)and20hinderertrials(range10–30) wereincludedinthefinalanalysis.Thisdatawerebaseline corrected(averageamplitudeof200mspriortoappear- anceofagent)individuallyforeachtrial.Segmentswere thenre-referenced(averagereference)andaggregatedto individualaveragesforeachtrialtype(helper/hinderer).

Individual averages and the grand average ERPs were

(4)

Fig.1. StimuliusedintrainingandtestsetofExperiment1.Notethattheidentityofthehelper(hereatriangle)andthehinderer(hereasquare)was randomizedacrossparticipants.(Forinterpretationofthereferencestocolorinthissentence,thereaderisreferredtothewebversionofthearticle.)

Fig.2. DenoteschannelsusedtoanalyzeP400(blackcircles),channelsincludedintheanalysis(graycircles)andexcludedchannels(whitecircles).Grand averageERPdataareshownforselectedchannelsfortheﬁrst600msaftertheonsetoftheteststimulus(imageofhelper/hindererinExperiment1 agentmovingupordowninExperiment2).Blacktrianglesmarksigniﬁcantdifferencesbetweenhelperandhindertrials.Solidlinesrepresenthelperin Experiment1andagentmovingupinExperiment2,dashedlinesrepresenthindererinExperiment1andagentmovingdowninExperiment2.

(5)

visuallyinspected andelectrodes inlocationsrelated to posteriortemporalcortex(P400)werefurtherexamined (seeFig.2).

Channelspreviouslyusedtoassess theP400compo- nentoverposteriortemporalareasininfancy(Gredebäck etal.,2010)werealsoinvestigatedinthepresentstudy(left channelnumbers;59,60,61,65,66,67,andrightchannel numbers;77,78,84,85,90,91).InadditionERPcompo- nentNc(channelnumbers5,6,7,12,13,20,29,104,105, 106,111,112,118)wasanalyzed.Analyseswerebasedon theaverageamplitudeofthesechannelsandatimeinter- valrangingfrom250to400msaftertheappearanceofthe helperorhindereronthescreen(inthetestset)forP400.

TheNcwasinvestigatedusingtheaverageamplitudeofthe above-mentionedchannelsduringatimerangefrom400 to600msaftertheappearanceofthehelperorhinderer.

AmplitudedataforP400wasaggregatedoverelectrodes andenteredasthedependentvariableinaGeneralLinear Model (GLM) with agent (helper, hinderer) and hemi- sphere(left,right)aspredictorsandcomplementedwith non-parametricWilcoxonMatchedPairsTest(aggregated overhemisphere).AmplitudedataforNcwereaggregated overchannelsandenteredasthedependentvariableina repeatedmeasuret-testwithagentasindependentvari- ableand complemented with non-parametricWilcoxon MatchedPairsTest.Alldatasetswerecheckedforoutliers (±3z-score),however,nooutlierchannelsweredetected.

2.2. Results

TheamplitudeofP400differedsigniﬁcantlybetween the helper (2.36␮V, SE=1.35) and hinderer (−0.96␮V, SE=1.4),F(1,13)=5.27,p=.039,²_p=.29(seeFigs.2and3).

Nosigniﬁcantmaineffectofhemisphere(leftandright), F(1,13)=1.09,p=.31,orinteractioneffectbetweenhemi- sphereand agent, F(1,13)=0.002, p=.96, wasobserved.

A WilcoxonMatched Pairs Testdemonstrated a signifi- canteffectoftrialtype,W(14)=20,p=.04fortheP400.At thesametimenodifferencesbetweenhelper(−3.82␮V, SE=1.05) and hinderer (−1.98␮V, SE=1.12) trials were observed for the Nc, t(13)=1.33, p=.21. A Wilcoxon MatchedPairsTestconfirmednosignificanteffectoftrial type,W(14)=34,p=.24fortheNccomponent.

2.3. Discussion

Experiment1demonstratesdifferentialprocessingof pro-andanti-socialagents,expressedaslargerP400ampli- tudesforagentsthatpreviouslyhelpedthanagentsthat previouslyhinderedanotheragent. Nodifferences were observedinERPcomponentNc.Oneimportantcaveatisthe possibilitythatreportedeffectsreﬂectssuperﬁcialproper- tiesofthestimuli(e.g.upwardanddownwardmotion)and notofsocialvalence.InordertocontrolforthisExperiment 2presentedinfantswithhighlysimilareventsinwhichthe agentbeinghelpedorhinderedisreplacedwithaball.Thus, thehelpingagentinExperiment1isnowmovingaball (withnoeyes)upahillandthepriorhinderingagentfrom Experiment1nowmovesaballdownthehill.

ERPcomponentsreﬂectingevaluationsofsocialvalence shouldnolongerdifferentiatebetweenthetwotrialtypes

inExperiment2,becausetheredballisnolongerestab- lishedasanagentwithgoalsandcanthereforenolonger behelpedorhindered.AtthesametimeERPcomponents resultingfromotherpropertiesofthestimulisuchassuper- ﬁcialperceptualorattentionaldifferencesshouldremainor beenhanced.Alongtheselineswehypothesizethatdiffer- encesinamplitudeofP400betweenhelperandhinderer shoulddisappearwhencomparingupwardanddownward motioninExperiment2.

3. Experiment2 3.1. Methods

3.1.1. Participants

Fourteen6-month-oldinfants(sixfemale;meanage6 months,3days,range5months,21daysto6months,12 days)wereincludedintheﬁnalanalysis.Anadditional10 infants(ﬁvefemales)wereexcludedsincetheydidnotpass theinclusioncriterionofatleast10artifactfreetrialsper trialtype.GeneralprocedureswereconductedasinExper- iment1.

3.1.2. Stimuliandprocedure

Thegeneralpropertiesofthestimuliremainedthesame asdescribedinExperiment1above.Theteststimuliand procedurewereidentical.Themaindifferencebetweenthe twotrainingstimulisetswastheball’sabsenceofeyesand self-propulsion.Thustheballwasinanimateandmoved onlywhenbeingpushedup(moveupmovies)ordown (movedownmovies)thehill.Themovementsofthetwo agentsastheypushedtheballupanddownthehillwere identicaltoinExperiment1.Thedurationofeachmovie was7s–movieswereshorterbecausetheylackedtheini- tialphaseestablishingtheball’sattempttoclimbthehill.

Beforetheﬁrstmoviea 3sblack screenwaspresented.

Fortheremainingmoviesthedurationoftheblackscreen was2s. The total presentationtimeof theentiretrain- ingsessionwas55slong.Themovieswerepresentedin acounterbalancedorder,withthetwoagents(squareand triangle)randomlyassignedtomovietypes(moveupor movedown).

Themovedownmoviesstartedwithastillimageofthe hillwiththeballlocatedatthemiddleofthehill(1000ms).

Theagentmovingdownthenappearedfromabove,pushed theballdownthehill,andmovedupthehillandleftthe screenusingidenticalmotionsandtimingstothehinderer inExperiment1.Themovieendedwithastillpicturecon- tainingtheballstationaryatthebottomofthehill(600ms).

Themoveupmovieshadanidenticaltimingandoverall structure,butheretheagentmovingupappearedfromthe bottom,pushedtheballupthehill,usingidenticalmotions andtimingstothehelperinExperiment1.Allotheraspects ofthetrainingset,thetestset,andtheexperimentaldesign wereidenticaltoExperiment1,includingsoundsassoci- atedwiththedifferentagents.Onaverageinfantsattended to 49 trials (range 30–87) of the test stimuli depicting themove-upagentand50trials(range30–70)ofthetest stimulidepictingthemove-downagent.

(6)

Fig.3.AverageamplitudeoftheP400component,separateforthetwotrialtypes(helper,hinderer)inExperiments1and(moving-up,moving-downagent) 2withasterisksindicatingdifferencesbetweenhelpingandhinderingtrialsatp<.05anderrorbarsrepresentingSE(A).Individualamplitudedifference scores(helper–hinderer;movingup–movingdownagent)separateforeachexperiment(B).

3.1.3. EEGrecordingandanalysis

The data reduction procedure was identical to that described underExperiment 1.On average20 move-up agenttrialsperinfant(range11–47)and21move-down agenttrials(range10–45)wereincludedintheﬁnalanal- ysis.

3.2. Results

TheamplitudeofP400didnotdifferbetweenthetwo trialtypes;move-upagent(−2.98␮V,SE=1.68)andmove- down agent (−1.0␮V, SE=1.56), F(1,13)=2.48, p=.14 (Figs.2and3).Nosignificantmaineffectsofhemisphere (leftandright),F(1,13)=.006,p=.94,orinteractioneffects betweenhemisphereandagent,F(1,13)=1.94,p=.18,were observed.A WilcoxonMatched PairsTestdemonstrated nosignificanteffectoftrialtype,W(14)=31,p=.18forthe P400.InadditiontheresultsdemonstrateasignificantNc component,t(13)=2.74,p=.002,withamorenegativeNc amplitudeforthemovingdownagent(−4.83␮V,SE=1.79) when contrasted to the moving up agent (−2.74␮V, SE=1.38).TheWilcoxonMatchedPairsTestfurthercon- firmedthesignificanteffectoftrialtype,W(14)=15,p=.02.

3.3. Discussion

Experiment2didnotﬁnddifferencesbetweenampli- tudes in ERP component P400 when comparingagents movinganinanimateballupordownahill.Thereisthere- forenoevidenceforaP400effectwhenthesocialvalence dimensionisremoved,suggesting thatP400inthecur- rentcontextismodulatedbydegreeofprosociality.Instead Experiment2demonstratesdifferencesbetweenupward anddownwardmovingagentsintheNccomponentoften assumedtoindexattention(Richards,2003).Asnosuch effectwasdemonstratedinExperiment1,thisislikelynot relatedtothecorequestionathandandmightreﬂectatten- tionaldifferencewithrespecttolow-levelvisualproperties of the stimuli used in Experiment 2. Apparently these aspectsofthestimulibecomemoresalientwhenthesocial interactionandthehelpingorhinderingisremoved.

4. Generaldiscussion

Six-month-oldinfants’neuralactivity,asmeasuredby theERPcomponentP400,differedwhenobservingagents thatpreviouslyhelpedandagentsthatpreviouslyhindered others.TheP400amplitudedifferencesdidnotmanifest themselvesinExperiment2,whereupwardanddownward movingagentshadnopro-orantisocialconnotations.This isthefirststudythatrelatesdetectionofprosocialitytoa specificERPcomponentandthefirsttodemonstratethat infantP400amplitudes aremediatedby anagent’s his- toryofhelpingorhinderingothers(forpriorworkonEEG oscillationsin14-month-oldsinthecontextofprosocial behaviorseePaulusetal.,2013).

Thecurrentﬁndingappearsconsistentwithbehavioral dataat6monthsofage.Priorworkhasdocumentedovert preferencesforhelpingoverhinderingagents,measured bybothlookingtimesandpreferentialreaching(Hamlin etal.,2007,2010)atthesameage.Wedidnotmeasure infants’behavioralresponsestothestimuli,butitshould benotedthatthecurrentstimuliverycloselyresemblethe stimuliusedinpreviousstudiestodemonstratebehavioral preferencesforpro-socialagentsandavoidanceofantiso- cialagentsininfantsofthesameage(Hamlinetal.,2007).

Itisthereforeverylikelythattheneuralcorrelatesofsocial valenceprocessingdemonstratedhererepresenttheﬁrst stagesoftheneuralprocessleadingtoinfants’expression ofpro-socialpreferences.

Theﬁndingsarealsoconsistentwiththefewpriorstud- iesthat have indexed social perception usingthe P400 component.ThesameERPcomponentthathereindexes socialvalencehaspreviouslybeendocumentedtoindex socialperceptionofvariousstimuli,includinggoaldirected grasping (Bakker et al., in press), pointing (Gredebäck et al., 2010; Melinder et al., in press) and gaze direc- tion(Senjuet al.,2006).In thosestudiesfunctionaland goaldirected actionsresultedin largeramplitudesthan non-goaldirectedand/ornon-functionalevents.Wesug- gestthatthecurrentresultsﬁtinwiththisinterpretation undertheassumptionthat6-month-oldsaremorereadily attunedtoprocesspositivecomparedtonegativevalenced socialactions.ThisprocessesisindexedbyERPcomponent

(7)

P400.Thisassumptionreceivessupportfromtheobser- vationthat acrossa variety ofsocial modalities, infants in their first 6 months devote more attention to pos- itive stimuli, with a bias toward negativity developing later(Vaishetal.,2008).Furthermore,specificallyinthe hillclimberparadigmyounginfantsdevotemore visual attentiontothehelperthanthehinderer (Hamlinetal., 2010).However,thislatterstudyalsodemonstratesthat 3-month-oldsdiscriminateahindererfromaneutralactor butnotahelperfromaneutralactor.Together,thesefind- ingsarenotyetfullyinterpretable.Whatisclearhowever isthattheinfantP400responseisgeneraltoabroadrange ofsocialstimuliincludingnotonlythediscriminationof moreorlessfunctionalactionsbutalsothediscrimination ofvalencedsocialactions.TheP400componentnotonly indexessocial perceptualprocesses that relateoneper- son’sactionstoimmediategoals(Bakkeretal.,inpress;

Gredebäcketal.,2010;Senjuetal.,2006)butalsotointer- actionsbetweensocialagents.Thoughthecurrentstimuli belongtoasomewhatdifferentclassofsocialeventsitis possiblethatcurrentP400responsemapsthesameunder- lyingneuralnetworksdedicatedtootherformsofsocial perception.

Onedesigndifferencebetweenthisstudyandprevious studiesoftheinfantP400revealsanewaspectoftheP400.

In previous studies, conditiondifferences weredirectly perceivableintheteststimuli,forexamplebecauseapoint- inggesturewascongruentorincongruentwithanobject locationdisplayedafractionofasecondpreviously.Inthis study,however,therewerenodifferencesinthedirectly perceivablepropertiesoftheteststimuli(theagentsthem- selves).Rather,agentsdifferedinbehaviordisplayeddur- ingthetrainingstimuli,whichwerepresentedseparately.

Mostinfantssawafullsetof40testtrials,whichlasted68s, meaningtesttrialswerepresentedonaverage34saftera trainingstimulus.Differentresponsestodifferentagents basedontheirprevioushistoryofsocialinteractionimply thatinfantsencodeinmemoryattributionsofvalenceto speciﬁcagents(Hamlinetal.,2013a).Thecurrentresults indicatethattheinfantP400canindexnotonlyimmediate evaluationsofsocialstimulibutalsoactivationofmemory ofpropertiesassociatedwithparticularagents.

It is difﬁcult toconnect ERPcomponents tospeciﬁc spatiallocationsonthecortex,intheabsenceofsource localization. However, with respect to P400, there is a strongcandidateareathathaspreviouslybeenassociated withthisneuralmarker.Nelsonetal.(2006)arguethatthe infantP400isfunctionallysimilartotheadultN170com- ponent(seealsoCsibraetal.,2008;deHaanetal.,2003;

Nelsonetal.,2006).Inturn,theadultN170componenthas beenconnectedwiththeSTSusingbothsourcelocalization ofERPdata(ItierandTaylor,2004)andjointrecordings ofERPandfMRI(Dalrympleetal.,2011).Onepossibility, thatrequiresfurtherstudybeforeﬁrmconclusionscanbe made,isthattheP400componentdemonstratedforpro- andantisocialagentsin6-month-oldsoriginatesfrompro- cessessimilartothose underlyingother formsof social perception,namelySTSactivity(Gredebäcketal.,2010).

Theaimofthisstudywasnottodirectlycomparethe mentalisticandnon-mentalisticaccountsforsocialvalence detectiondescribedintheintroduction,astherearemany

aspectsofneuralactivitythatarenotaccessibleviaERP techniques.WehypothesizedaP400componentbecause boththeseaccountsinvolveSTSactivity,whichtheinfant P400hasbeenarguedtoreﬂect.However,wenotethat visualinspectionofERPdatadidnotdemonstrateanyother ERPcomponentsselectively processinghelpingandhin- dering(Experiment1)butnotagentsmovingupordown (Experiment2).Assuch,noclearevidenceofalargernet- workinvolvingthepre-frontalcortexcanbefoundinthe currentstudy.Thecurrentﬁndingsthereforeprovideno supportforthehypothesisthatsecond-ordermentaliza- tionliesbehindprosocialpreferencesat6-monthsofage, although such processes have been implicated in older infants(Hamlinetal.,2013b).Althoughundetectedfrontal correlates cannot beruled out, a parsimonious account of6-month-olds’prosocialpreferencesbasedonthecur- rent data is that they rely on a network restricted to posterior-temporalareasandtheSTS,assuggestedbythe non-mentalisticaccount.OnepossibilityisthatSTSacti- vationissupportedbyanthropomorphizingprocessesin theamygdala(HeberleinandAdolphs,2004)that trans- formmovinggeometricshapesintoperceivedagentswith intentionsandgoals.

5. Conclusions

We demonstratedthattheP400componentnotonly indexes socialperceptual processes thatrelateone per- son’sactionstoimmediategoals(Bakkeretal.,inpress;

Gredebäcketal.,2010;Senjuetal.,2006)butalsoactivation ofthememoryofsocialagents’previouspro-andantiso- cialactions.Similaritiesbetweenthecurrentresultsand priorstudiestargetingsocialperceptionsuggestthatsimi- larmechanismsmightbeinvolvedinprocessingbothgoal directed actions(pointing and gaze), biological motion, andcollaborativeinteractionsbetweennon-humanagents (helping).Whenitcomestosocialvalencetheseprocesses appearfunctionalat6monthsofage.

Conﬂictofinterest

Noconﬂictsofinteresttoreport.

Acknowledgments

The paper was supportedby ERC-StG grant CACTUS (312292)andMarieCurieITNACT(289404).

References

Allison,T.,Puce,A.,McCarthy,G.,2000.Socialperceptionfromvisualcues:

roleoftheSTSregion.TrendsCogn.Sci.4(7),267–278.

Bakker,M.,Daum,M.M.,Handl,A.,Gredebäck,G.,2015.Neuralcorrelate ofactionperceptionattheonsetoffunctionalgrasping.Soc.Cogn.

Affect.Neurosci.(inpress).

Castelli,F.,Happe,F.,Frith,U.,Frith,C.,2000.Movementandmind:a functionalimagingstudyofperceptionandinterpretationofcomplex intentionalmovementpatterns.Neuroimage12(3),314–325.

Courchesne,E.,Ganz,L.,Norcia,A.M.,1981.Event-relatedbrainpotentials tohumanfacesininfants.ChildDev.52,804–811.

Csibra, G.,Kushnerenko, E., Grossman, T., 2008. Electrophysiological methodsinstudyinginfantcognitivedevelopment.In:Nelson,C.A., Luciana, M.(Eds.),HandbookofDevelopmentalCognitive Neuro- science.MITPress,Cambridge,MA,pp.247–262.

(8)

Dalrymple,K.A.,Oruc,I.,Duchaine,B.,Pancaroglu,R.,Fox,C.J.,Iaria,G., etal.,2011.Theanatomicbasisoftherightface-selectiveN170IN acquiredprosopagnosia:acombinedERP/fMRIstudy.Neuropsycholo- gia49(9),2553–2563.

Decety,J.,2011.Dissectingtheneuralmechanismsmediatingempathy.

Emot.Rev.3(1),92–108.

Decety,J.,Howard,L.H.,2013.Theroleofaffectintheneurodevelopment ofmorality.ChildDev.Perspect.7(1),49–54.

Decety,J.,Michalska,K.J.,Kinzler,K.D.,2012.Thecontributionofemo- tionandcognitiontomoralsensitivity:aneurodevelopmentalstudy [Research Support,U.S. Gov’t, Non-P.H.S.]. Cereb.Cortex 22(1), 209–220.

deHaan,M.,Johnson,M.H.,Halit,J.,2003.Developmentofface-sensitive event-relatedpotentialsduringinfancy:areview.Int.J.Psychophys- iol.51,45–58.

deHaan,M.,Pascalis,O.,Johnson,M.H.,2002.Specializationofneural mechanismsunderlyingfacerecognitioninhumaninfants.J.Cogn.

Neurosci.14,199–209.

Fawcett,C.,Liszkowski,U.,2012.Infantsanticipateothers’socialpreferences.InfantChildDev.21(3),239–249.

Gredebäck,G.,Melinder,A.,Daum,M.,2010.Thedevelopmentandneural basisofpointingcomprehension.Soc.Neurosci.5(5–6),441–450.

Hamlin,J.K.,2013.Moraljudgmentandactioninpreverbalinfantsand toddlers:evidenceforaninnatemoralcore.Curr.Dir.Psychol.Sci.22 (3).

Hamlin,J.K.,2014.Thecaseforsocialevaluationinpreverbalinfants:

gazingtowardone’sgoaldrivesinfants’preferencesforhelpersover hinderersinthehillparadigm.Front.Psychol.5,1563.

Hamlin,J.K.,Mahajan,N.,Liberman,Z.,Wynn,K.,2013a.Notlikeme=bad:

infantspreferthosewhoharmdissimilarothers.Psychol.Sci.24(4), 589–594.

Hamlin,J.K.,Ullman,T.,Tenenbaum,J.,Goodman,N.,Baker,C.,2013b.The mentalisticbasisofcoresocialcognition:experimentsinpreverbal infantsandacomputationalmodel.Dev.Sci.16(2),209–226.

Hamlin,J.K.,Wynn,K.,Bloom,P.,2007.Socialevaluationbypreverbal infants.Nature450(22),557–560.

Hamlin,J.K.,Wynn,K.,Bloom,P.,2010.Three-month-oldsshowanega- tivitybiasintheirsocialevaluations.Dev.Sci.13(6),923–929.

Hamlin,J.K.,Wynn,K.,2011.Younginfantspreferpro-socialtoantisocial others.Cogn.Dev.26(1),30–39.

Hamlin,J.K.,Wynn,K.,Bloom,P.,Mahajan,N.,2011.Howinfantsandtod- dlersreacttoantisocialothers.Proc.Natl.Acad.Sci.U.S.A.108(50), 19931–19936.

Heberlein,A.S.,Adolphs,R.,2004.Impairedspontaneousanthropomor- phizingdespiteintactperceptionandsocialknowledge.Proc.Natl.

Acad.Sci.U.S.A.101(19),7487–7491.

Itier,R.J.,Taylor,M.J.,2004.SourceanalysisoftheN170tofacesand objects.Neuroreport15(8),1261–1265.

Kaduk,K.,Elsner,B.,Reid,V.,2013.Discriminationofanimateandinan- imate motion in9-month-old infants:an ERP study.Dev. Cogn.

Neurosci.6,14–22.

Kobayashi,C.,Glover,G.H.,Temple,E.,2007.Children’sandadults’neural basesofverbalandnonverbal‘theoryofmind’.Neuropsychologia45 (7),1522–1532.

Kovacs,A.M.,Teglas,E.,Endress,A.D.,2010.Thesocialsense:susceptibility toothers’beliefsinhumaninfantsandadults.Science330(6012), 1830–1834.

Kuhlmeier,V.,Wynn,K.,Bloom,P.,2003.Attributionofdispositionalstates by12-month-olds.Psychol.Sci.14(5),402–408.

Leppanen,J.M.,Moulson,M.C.,Vogel-Farley,V.K.,Nelson,C.A.,2007.An ERPstudyofemotionalfaceprocessingintheadultandinfantbrain.

ChildDev.78(1),232–245.

Melinder,A.M.,Konijnenberg,C.,Hermansen,T.,Daum,M.,Gredebäck,G., 2015.Thedevelopmentaltrajectoryofpointingperceptionintheﬁrst yearoflife.Exp.BrainRes.(inpress).

Moll,J.,deOliveira-Souza,R.,Bramati,I.E.,Grafman,J.,2002.Functional networksinemotionalmoralandnonmoralsocialjudgments.Neu- roimage16(3),696–703.

Nelson, C.A., Moulson, M.C., Richmond, J., 2006. How does neuro- scienceinformthestudyofcognitivedevelopment?Hum.Dev.49, 260–272.

Onishi,K.H.,Baillargeon,R.,2005.Do15-month-oldinfantsunderstand falsebeliefs?Science308,255–258.

Parise,E.,Reid,V.M.,Stets,M.,Striano,T.,2008.Directeyecontactinﬂu- encestheneuralprocessingofobjectsin5-month-oldinfants.Soc.

Neurosci.3(2),141–150.

Paulus,M.,Kühn-Popp,N.,Licata,M.,Sodian, B.,Meinhardt,J.,2013.

Neuralcorrelatesofpro-socialbehaviorininfancy:differentneu- rophysiologicalmechanismssupporttheemergenceofhelpingand comforting.Neuroimage66,522–530.

Puce,A.,Allison,T.,Bentin,S.,Gore,J.C.,McCarthy,G.,1998.Temporal cortexactivationinhumansviewingeyeandmouthmovements.J.

Neurosci.18(6),2188–2199.

Premack,D.,Premack,A.J.,1997.Infantsattributevalue±tothegoal- directedactionsofself-propelledobjects.J.Cogn.Neurosci.9(6), 848–856.

Reid,V.,Hoehl,S.,Striano,T.,2006.Theperceptionofbiologicalmotion byinfants: anevent-related potentialstudy. Neurosci.Lett.395, 211–214.

Richards,J.E.,2003. Attentionaffects therecognition ofbrieﬂypre- sented visual stimuli in infants: an ERP study. Dev. Sci. 6, 312–328.

Scarf,D.,Imuta,K.,Colombo,M.,Hayne,H.,2012.Socialevaluationor simpleassociation?Simpleassociationsmayexplainmoralreasoning ininfants.PLoSONE7(8).

Senju,A.,Johnson,M.H.,Csibra,G.,2006.Thedevelopmentandneu- ral basis of referential gaze perception. Soc. Neurosci. 1 (3–4), 220–234.

Southgate,V.,Senju,A.,Csibra,G.,2007.Actionanticipationthrough attribution of false belief by 2-year-olds. Psychol. Sci. 18 (7), 587–592.

Vaish,A.,Grossmann,T.,Woodward,A.,2008.Notallemotionsarecreated equal:thenegativitybiasinsocial-emotionaldevelopment.Psychol.

Bull.134(3),383–403.

VanOverwalle,F.,Baetens,K.,2009.Understandingothers’actionsand goalsbymirrorandmentalizingsystems:ameta-analysis.Neuroim- age48(3),564–584.