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How social is the chaser?: Neural correlates of chasing perception in 9-month-old infants

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Developmental Cognitive Neuroscience

j ou rn a l h om ep a ge :h t 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

How social is the chaser? Neural correlates of chasing perception in 9-month-old infants

Martyna Galazka

, Marta Bakker, Gustaf Gredebäck, Pär Nyström

UppsalaChildandBabylab,DepartmentofPsychology,UppsalaUniversity,Uppsala,Sweden

a r t i c l e i n f o

Articlehistory:

Received20October2015

Receivedinrevisedform21March2016 Accepted12May2016

Availableonline24May2016

Keywords:

P400

Animacyperception Chasing

a b s t r a c t

Weinvestigatedtheneuralcorrelatesofchasingperceptionininfancytodeterminewhetheranimated interactionsareprocessedassocialevents.ByusingEEGandanERPdesignwithanimationsofsimple geometricshapes,weexaminedwhetherthepositiveposterior(P400)component,previouslyfound inresponsetosocialstimuli,aswellastheattentionrelatednegativefronto-centralcomponent(Nc), differswheninfantsobservedachaserversusanon-chaser.InStudy1,thechaserwascomparedtoan inanimateobject.InStudy2,thechaserwascomparedtoananimatebutnotchasingagent(randomly movingagent).ResultsdemonstratenodifferenceintheNccomponent,butstatisticallyhigherP400 amplitudewhenthechasingagentwascomparedtoeitheraninanimateobjectorarandomobject.We alsofindadifferenceintheN290componentinbothstudiesandintheP200componentinStudy2,when thechasingagentiscomparedtotherandomlymovingagent.Thepresentstudiesdemonstrateforthe firsttimethatinfants’processcorrelatedmotionsuchaschasingasasocialinteraction.Theperception ofthechasingagentelicitsstrongertime-lockedresponses,denotingalinkbetweenmotionperception andsocialcognition.

©2016TheAuthors.PublishedbyElsevierLtd.ThisisanopenaccessarticleundertheCCBY-NC-ND license(http://creativecommons.org/licenses/by-nc-nd/4.0/).

1. Introduction

Thehumanvisualsystemnotonlydetectsphysicalstructures in the environment but also their causal and social structures derivedfrommotioninformation.Whenobservingdisplayswith simple geometrical shapes engagedin a variety of interactions suchasfighting,dancingandchasing,adultobserversconsistently describeseeinganimate,interactingentitieswithdistinctgoalsand intentions(HeiderandSimmel,1944;forreview,seeScholland Tremoulet,2000).Thisextraordinaryabilityofthevisualsystemto derivesuchsocially-richinformationfromrelativelysimplevisual inputrevealstheprimaryandinterdependentlinkbetweenper- ceptionandsocialcognitioninadulthood(Schultzetal.,2004).The factthatthediscriminationofinteractingandrandomlymoving objectstakesplacealreadyat3-months(Rochatetal.,1997),pro- videsevidencethatsocialcategorizationplaysafundamentalrole inhowhumansperceivetheirenvironment.However,todateno studyhasprovideddirectevidencethatinfants’socialnetworks arebeinginvolvedwhenobservinginteractionssuchaschasing,

∗ Correspondingauthorat:UppsalaChild&BabyLab,Box1225,S-75142Uppsala, Sweden.

E-mailaddress:martyna.galazka@psyk.uu.se(M.Galazka).

andthequestionwhethersocialcategorizationthroughmotionis presentalreadyearlyininfancyremainsunanswered.

Inthelastdecades,neuralcorrelatesinvolvedintheperception ofinteractionshavebeenmuchresearchedinadults.Thesestudies findthatareasusedforperceptionofsocialstimulialsocorrespond whenviewinganimateinteractionssuchaschasing.Muchlikethe detectionofbiologicalmotion,chasingelicitsactivationinthetem- poroparietalcortex,theposteriorsuperiortemporalsulcus(pSTS) andtheangulargyrus(Castellietal.,2000;Leeetal.,2012;Martin andWeisberg,2003;Schultzetal.,2004)oftenlateralizedtothe righthemisphere(Gaoetal.,2012;Schultzetal.,2005;Shultzetal., 2011).

Together,adultresearchonanimacyperceptionsuggeststhat observers,whilewatchinglifelessgeometricalshapesmove,inter- pret them in terms of animacy and intentionality while the neurologicalcorrespondence oftheareasassociated withsocial stimulisupporttheideathatadultsperceivetheseeventsassocial.

Forinfants,muchlikeadults,motioninformsaboutthetypeof observedagentsandevents.Forinstance,studiesexamininginfant visualattentionhavefoundthat3-month-oldsorientandprefer toattendtodisplayswhere twodiscs arechasing comparedto displaysinwhichtheyaremovinghaphazardlybouncingoffthe boundariesof thescreen (Rochat et al.,1997).Recentevidence (Galazkaand Nyström,2016)furthersuggeststhat infantvisual

http://dx.doi.org/10.1016/j.dcn.2016.05.005

1878-9293/©2016TheAuthors.PublishedbyElsevierLtd.ThisisanopenaccessarticleundertheCCBY-NC-NDlicense(http://creativecommons.org/licenses/by-nc-nd/4.

0/).

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attentionwithinchasinginteractionsislargelyaccountedbythe chaser,reflectingthedevelopingsensitivitytokinematicinforma- tionpertainingtointeractionsinlimitedvisualdisplays(Galazka etal.,2014;GalazkaandNyström,2016).Butvisualattentionalone doesnotinformaboutwhetherinfantsattendtoanimatedinter- actionsbecauseof theirsocial narrative, orwhetherperceptual propertiesoftheeventalonecausetheattentionalshifts.Onepos- sibilityisthatareasresponsivetosocialstimuliareelicitedwhen infantsobserve thesetypes of animated displays,much like in adults.Anotherpossibility,however,isthatinfants’visualattention towardanimated displaysisdue tolower levelperceptualpro- cesses.Forinstance,objectsthatsharethesamemotiontrajectory (knownastheclassicalGestaltlawof‘commonfate’)(Wertheimer, 1923/1938),objectsthatcomeclosetogether,orobjectsthatmove contingentlymightcapturevisualattentionmorethanrandomly movingobjectswithoutinterpretingthemassocial.Infact,very young infants attend to the features of chasing, such as goal- directed motionofone object towardanother and acceleration more sothan when these features are configuredin a chasing motion(Frankenhuisetal.,2013).Inthepresentarticle,weaddress thistheoreticaldistinctionbyexaminingneuralactivationofsocial brainprocessesduringchasingperception.

InfantneurologicalstudieshavepreviouslyusedERPcompo- nentmeasurestodeterminethesensitivitytoanimacyandsocial information. One such ERP study found evidence for differen- tialsensitivitytoanimateandinanimatemotionin9-month-olds (Kaduk et al., 2013). The findings suggested that by 9-months infantsallocatemoreattentiontoanobjectmovinginanimately thanananimateobjectasevidencedbytheincreasednegativityin thefronto-centralNccomponent,amid-latencycomponentthat hasbeenfoundtoreflect general attentionalarousal(Richards, 2003)aswellasorientationtosalientstimuli(Courchesneetal., 1981).

Theprocessingof social informationin infants, ontheother hand,hasbeenmeasuredbytheN290andtheP400component, fromnowreferredtoasaN290/P400complex.Thislatentcom- ponentoverthelateralposteriorregionhasbeenarguedtoindex pSTSactivity(Gredebäcketal.,2010;GredebäckandDaum,2015) andininfantsithasalmostexclusivelybeenassociatedwithpro- cessingsocially-valencedinformation(Gredebäcketal.,2015).For instance,inresponsetogesturesthatconveysocialmeaningsuch ashandsturnedrightsideupina‘give-me’gesture(Bakkeretal., 2015),grasping(Bakkeretal.,2014,2016),pointing (Gredebäck etal.,2010;Melinderetal.,2015),gazedirection(Senjuetal.,2006) andwhenobservingbiologicalmotion(Reidetal.,2006).Theinfant N290/P400complex,wasfoundtoparalleltheN170componentin adults(Gredebäcketal.,2010;Senjuetal.,2006)–acomponent associatedinresponsetosocialstimulisuchashumanfaces(Csibra etal.,2008).UnliketheinfantP400component,theP400compo- nentinadultpopulationhasbeenassociatedwithawiderange offactorssuchasvisualambiguity(KornmeierandBach,2009), memoryload(Klaveretal.,1999;Beuzeron-ManginaandMangina, 2000),and attentionalcontrol (Falkenstein et al.,1999).Collec- tively,althoughnostudyhaspreviouslyexploredspecificneural correlatestochasing, thesestudiessuggesta uniquesetofERP componentstoanimatedobjectsandsocialinformationininfancy.

Theprimarygoalofthecurrenttwostudieswastoexaminethe neuralcorrelatesofchasingininfantsbytappingtheN290/P400 complexandtheNccomponent.Indoingso,wegaininsightinto theunderlyingprocessesofsocialperceptionthroughmotion.

Based on the two possible accounts of infant preference to animateddisplays,wehypothesizethat ifchasinginteractionis interpretedasasocialeventtheN290/P400complexwillbelarger whenchasingmotioniscomparedtoinanimatemotion(Study1) andwhenitiscomparedtoanimatebutrandommotion(Study 2).PresenceoftheP400componentinthesecomparisonswould

speakinsupportofthesocialaccountsuggestingthatinfants,like adults,processchasingasmorethanasetofmotioncues.Bycon- trast,presenceoftheattentionalNccomponentalone,wouldspeak foralower-levelperceptualprocessingaccount,inwhichattention tomotionparametersalonedeterminespreferenceforthechasing event.

2. Study1:chasingversusinanimatemotion 2.1. Methods

Toaddressthequestionof neuralcorrelatesunderlyingper- ceptionofachasinginteractionwepresented9-month-oldinfants withdisplaysdepictingtwogeometricalshapesinvolvedinchas- ing,whereoneshape(atriangleorarectangle)consistentlymoved towardanother,whileitspartner(agreycircle)consistentlymoved away.InStudy1,thechasingmotionwascomparedtoinanimate motion.Theinanimatemotiondepictedtwoobjects(arectangle ifatrianglewasshownduringthechasingcondition,ortriangle otherwise, anda grey circle)movingat aconstant speed along lineartrajectories,onlychangingdirectionbybouncingoffthedis- playboundariesortwostationaryobjectsinthedisplay.Usinga paradigmpreviouslyusedfor assessingERPresponsesin young children(Gredebäcketal.,2015;Kaduketal.,2013),wefirstpre- sentedtheanimationsandthenmeasuredtheERPresponsetothe stillimagesofagentsintheanimation(atriangleandarectangle).

2.2. Participants

Eighteen9-month-oldinfants(6female;meanage=270days;8 months29days)wereincludedinthefinalsample.Allparticipants werefull-termwithoutknownneurologicalordevelopmentaldis- abilities.Additional16infantsweretestedbutwerenotincludedin thefinalanalysisduetofailureinmeetingtheinclusionarycriterion ofminimum10artifact-freetrialsforeachcondition(arectangle andatriangle).Althoughtheexclusioncriterionappearstoresult ina highdrop rate,a recentmeta-analysisoninfantERPshave determinedadropoutrateofabout50%tobethestandardinthis typeofparadigmwithsuchyoungpopulation(Stetsetal.,2012).

Participantswererecruitedfroma listofparentswhoindicated interestinparticipatinginresearchwiththeirchild.Themajority ofinfantswereprimarilyfromwhitemiddle-classbackgroundliv- inginamedium-sizedEuropeancity.Studieswereconductedin accordancewith1964DeclarationofHelsinkiandallinfants’par- entsprovidedwritteninformedconsentaccordingtotheguidelines specifiedbythelocalEthicalCommittee.Fortheirparticipation, parentsreceivedagiftvoucherworthapproximately10euro.

2.3. Stimuliandprocedure

Allinfantsbegantheprocedurebyobservingvideoanimations foreachconditionpresentedona17-incomputerscreen(Fig.1).

Thesevideodisplaysweredirectlyfollowedbymultiplestatictest imagesthatwereusedtoextractERPs.Inpreviousresearch,this procedure(videoandtestimage)hasbeenfoundtoreliablyinflu- enceERPsininfantsthisage(Gredebäcketal.,2015;Kaduketal., 2013).

Themovinganimationsconsistedof10-svideopresentations at the start of the procedure: 2 times the Chasing interaction and 2 times the Inanimate motion. The animations were cre- atedusingAnimeStudioDebut10,ananimationsoftware(http://

my.smithmicro.com/anime-studio-debut-10.html).Allanimations depictedagraycircleandeitheranorangetriangleorabluerect- angle,where thetriangleand therectanglealwaysbelongedto oneconditioneach(counterbalancedbetweensubjects).Allshapes werematchedforluminosityandsize,andallgeometricalshapes

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Fig.1. Stimuliusedduringtheinitialvideopresentation(initialandreminder)andtestimages.Theidentityofthechaser(hereabluerectangle)andtheinanimateobject (hereanorangetriangle)inStudy1andrandomobjectinStudy2wascounterbalanceldacrossparticipants.Thetrajectoryrepresentedherereflectsthefirst4softhevideo.

(Forinterpretationofthereferencestocolorinthisfigurelegend,thereaderisreferredtothewebversionofthisarticle.)

movedagainsttexturedgreenbackgroundwithtwobrownrectan- gularshapesplacedoneachsideofthescreentoprovidecontext fortheinteraction(barriersbehindwhichobjectscouldmoveor bounceoff of).Examplesofeach animationareprovided inthe Supplementarymaterials.

2.3.1. Chasinginteraction

Thechasing interactionbegan withthechaser(orangetrian- gleor bluerectangle)moving at constantvelocity of 0.4visual degrees/frame (12 pix/frame) toward the target (gray circle), while the target moved at the baseline velocity of 0.19 visual degrees/frame(6pix/frame).Whenthechasergotwithin2.5visual degrees (80pixels) fromthetarget, thetarget accelerated to4 timesitsinitialvelocityto0.8visualdegrees/frame(24pix/frame) forthedurationof24frames.Afterthisitdeceleratedtoitsini- tialspeed.Theaccelerationandtheeventualdecelerationofthe targetoccurred4 times in10strialduration. Aspecific 4-note high-pitchedsoundaccompaniedthechasinganimationanditcor- respondedtotheincreasingproximityofthechasertoitstarget.

2.3.2. Inanimatemotion

The inanimate motion animation depicted the main shape (orangetriangle/bluerectangle)andthegraycirclemovingatacon- stantspeedof0.4visualdegrees/frame(12pix/frame).Eachshape movedrandomly,withnoapparentrelationtoeachother.Asthey moved,bothshapesoccasionallybumpedintothebordersofthe screenaswellasthebrownrectangles.Whenthathappened,the shapessimplybouncedoffandcontinuedtomoverandomly.The inanimatemotionalsoincludedaspecificbouncingsoundthatwas contingentonwhenthemainshapebouncedoffthesurfaces.

Thestudywaswithin-subjectdesign,meaningthateachinfant sawbothchasinginteractionandinanimatemotion.ThestaticERP testimagesthatfollowedtheinitialvideopresentationconsistedof randomlyalteredstillimagesdepictingthegeometricshapeasso- ciatedwithchasing(orangetriangleorbluerectangle;20trials), orthegeometricshape associatedwithinanimatemotion(blue rectangleororangetriangle;20trials)butneverwithmorethan threeconsecutiveimagesofthesameshape.Theobjectwasshown againstthesamebackgroundasthepreviouslyseenanimations butwithoutanyotherobjectspresent.Theshapewasalsoslightly zoomedininordertomaketheitstandoutfromthebackground andenhancetheinfant’sattentionexclusivelytotheshapeinvolved inthemotionratherthananyothershapes(suchasthegreycircle orbackgroundbarrierspresentedintheanimation).Therectangle was2.5(80pixels)×2.4visualdegrees(71pixels).Thetrianglehad

abaseof3.1(98pixels)andheightof2.4(77pixels)visualdegrees.

Tomakesurethatanydifferencesbetweenthegroupswerenot duetolow-levelvisualdifferences,wedouble-checkedthatthere wereequalnumberofsubjectsinthecounterbalancedgroups(as manysubjectssawchasingtriangles,n=9,aschasingrectangles, n=9).Eachtrialconsistedofablackimagewithawhitefixation- cross(1000msinduration)followedbyastillimageoftheorange triangleora bluerectangle(1000msin duration)withthecor- respondingsound(800msinduration).Thestillimagewasthen followedbyanotherfixationcross,followedbythenextimage,etc.

Afterapproximately40testtrials,orwhenaninfantstopped payingattentiontothescreen,eachchildwaspresentedwitha reminder animationset. Thisset consisted of onepresentation of each animation seen previously at the start of the stimulus presentation.Thiswasdoneinordertoremindinfantsofthepre- viouslyseen motions.In Study 1,each child observed between 3–6reminder video presentations (M=4.1). Afterthe reminder video,infantssawanothertestsetofstaticimagesuntiltheinfant stoppedattendingcompletely.Infantsattendedonaverageto56 trialsineachcondition(range:39–74)ofwhich56 werechaser trialsand55.9inanimateobjecttrials.Onaverage,theentirestim- uluspresentationwas5minand58s.Thisincludedtheinitialvideo presentation,stilltestimagesandtheremindervideos.

2.4. EEGrecordingandanalysis

Age appropriate 128-channel Geodesic Sensor Nets (HCGSN 130;EGI,Eugene,OR)wereusedtorecordEEGsignals.Thesignal relativetothevertexreferencedwassampledat250Hz,amplified byEGINetamplifier(GES300Amp;EGI,Eugene,OR)andstored foroff-lineanalysis.ContinuousEEGdataweredigitallyfiltered (0.3–30Hz)andsegmentedfrom300mspriortotheappearanceof thestillimageto1000msaftertheimage’sappearance.

Similarto prior research withinfant population (Gredebäck etal.,2015;Rosanderetal.,2007)themostanteriorandposterior electrodes(37electrodes)werenotincludedinthefinalanalysis duetohighnoiseandartifactfrequencycausedbypoorcontact withtheinfantscalp.Thedataweremanuallycheckedforarti- facts(suchaschannelglitchesandstrongdriftswithinindividual channels).Subjectswithlessthan10validtrialsineachcondition wereexcludedfromfurtheranalysis,which iscomparable with otherEEGstudiesusingvisualstimuliininfantpopulation(Kaduk etal.,2013;StetsandReid,2011;Stetsetal.,2012).Asaconse- quence,onaverage13.3(range:10–23)chasetrialsand14.2(range:

10–23)inanimatetrialsperinfantwereincludedinthefinalanal-

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Fig.2.GrandaverageERPdataforselectedchannelsfortheNccomponent(ingreen;topgraph)andP400(inred)componentoftheLeft(bottomleftgraph)andRight (bottomrightgraph)hemispherewithtimeofinterestshadedingray.(Forinterpretationofthereferencestocolorinthisfigurelegend,thereaderisreferredtotheweb versionofthisarticle.)

ysis(Pairedsamplet-testt(17)=−1.25,p=0.23).Segmentswere thenre-referencedtoaveragereferenceandalltrialswerebaseline correctedwiththeaverageamplitudebetween0and300msprior toappearanceoftheimage.Finally,thedatawereaggregatedto individualaveragesforeachtrialtype(chase/inanimate).Afigure withallchannelsandconditionsinthesensorlayoutisfoundinthe Supplementaryinformation.

Regions of interest were chosen to cover areas in the low occipital-temporalregionpreviouslyfoundtoelicitP400compo- nenttosocialinformation(Bakkeretal.,2015).Basedonthevisual inspectionoftheindividualaveragesweselected13channelsover posteriorarea(allchannelnumbers:62,66,67,70[01],71,72,74, 75[Oz],76,77,82,83[02],84;ofwhichleftchannelswere:66, 67,70,71,74;andrightchannelswere:76,77,82,83,84).1Analy- sesoftheP400componentwerebasedontheaverageamplitude ofthesechannelsandatimeintervalrangingfrom350to650ms aftertheobjectappearance.Asadependentvariable,theaggregate amplitudevaluewasenteredinaGeneralLinearModel(GLM)with theagent(chaser,inanimateobject)andhemisphere(left,right)as withinsubjectfactors.

Inaddition,ERPNccomponent(channelnumbers:5,6,7,12,13, 20,29,36,104,105[C4],106,111,112,118)wasexamined,asitwas previouslyidentifiedtomeasureattentionalsensitivitytoinani- mateoveranimatemotion(Kaduketal.,2013).TheNccomponent wasinvestigatedusingtheaverageamplitudeofthedesignated

1Channelsinthecentralmidline(62,72and75)werenotincludedintheleftnor rightanalysisfortheP400component.

channelsduringatimerangefrom400to600msaftertheappear- anceoftheimage.AmplitudedatafortheNcwasmeasuredina Pairedsamplet-testwithagentasanindependentvariable.Alldata setswerecheckedforoutliers(±3z-score)butnonewerefound.

2.5. Results

Basedonpreviouslysethypotheses,twocomponentsofinterest wereexamined:P400componentinthelateralposteriorregion encompassinglowoccipitalandposttemporalelectrodesaswell astheNccomponentovercentralfrontalelectrodes.

2.5.1. P400

A 2(chaser, inanimate agent)×2(hemisphere: left, right) repeatedmeasuresanalysisofvariancerevealedasignificantmain effectofagenttypeF(1,17)=5.05,p=0.038,␩2=0.229withasig- nificantlyhigheramplitudeforthechaser(9.45␮V,SE=2.25)than theinanimateagent(4.32␮V,SE=1.86)(Fig.2).

Theanalysisalsoindicateda significantmaineffectofhemi- sphere, F(1, 17)=48.39, p<0.001, ␩2=0.740, with a higher amplitude in the right (12.48␮V, SE=1.92) than left (1.28␮V, SE=1.88)channels.Therewasnosignificanthemispherebyagent interactionF(1,17)=0.944,p=0.345,␩2=0.053.

2.5.2. Nc

FortheNccomponent,aPairedsampledt-testdemonstratedno significantdifferencesbetweenagenttypes,t(17)=1.79,p=0.091 withapositiveamplitudeforthechaser(3.38␮V,SE=4.45)andthe inanimateagent(0.28␮V,SE=4.75).

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VisualinspectionofthedatafurtherindicatedtestoftheN290 componentintheP400-regionaswellasanearlierpositivecom- ponentpeakingataround200msfollowingstimulusonset(P200).

TheN290componentdemonstratedsignificantlyhigherpositive amplitudeforthechaser(1.67␮V,SE=9.27)thantheinanimate agent(−2.87␮V,SE=9.38),t(17)=2.30,p=0.034.AttheP200com- ponent,theamplitudeforthechaserwasslightly morepositive (4.87␮V,SE=2.42) thantheamplitude forthe inanimateagent (.19␮V,SE=2.45),butthedifferencewasonlymarginallysignif- icantt(17)=1.99,p=0.062.

Finally,forallthecomponentstested,nonecorrelatedsignifi- cantlywiththenumberofremindervideos(allps>0.05).

2.6. Discussion

TheresultsfromStudy1showthatwhenpresentedwithstill imagesoftwogeometricalshapes,9-month-oldinfantsareable todifferentiatebetweenthembasedonwhethertheysawthem previouslyengagedinachasinginteractionoraspartofaninan- imate motion. Specifically, findings demonstrate a significantly positiveP400ERPcomponentaround400msforthechasingagent comparedtotheinanimateagent.Basedonpriorfindingsdemon- stratingthattheP400isconsideredameasureofsocialperception (Bakker et al., 2014,2015, 2016;Gredebäck et al.,2010, 2015;

Melinderetal.,2015;Senjuetal.,2006)thecurrentfindingssuggest thatchasingisperceivedasasocialeventalreadyearlyininfancy.

InadditiontotheP400component,presentfindingsindicate anegativedeflectionaroundN290.Asmentionedpreviously,the infantN290,alongwiththeP400,hasbeenfoundtobethepre- cursoroftheadultN170component,whichmoststudiesfindin responsetosocialstimulisuchashumanfaces(Csibraetal.,2008;

deHaanetal.,2002;Halitet al.,2003).Thus, theN290compo- nentfoundininfantstowardtheendofthefirstyearcanalsobe usedasamarkerofsocialstimuliprocessing.TheP200,whichwas marginallysignificant,mayalsoberelatedtosocialprocessingin infantsandmeritsfurtherinvestigation.

ThelackofdifferenceintheNccomponentovercentralfrontal areawasunexpected,sinceithasbeenpreviouslyfoundinresponse toinanimateversusanimatemotionofasingleagent(Kaduketal., 2013).Apotentialreasonforthedifferentialfindingsmighthave todowiththemethodologicaldifferencesbetweenthetwostud- ies–herewepresenttwoobjectsengagedinaninteraction,while thepreviousstudypresentedinfantswithasingleobjecteither followingorviolatinguniversallawsofphysics.Itisalsoimpor- tanttopointoutthat inthepresentstudywedidnotfindany significantdifferencesbetweenthetwoobjectsacrossconditions withintheNccomponent,whichtypicallyreflectsattentionorgen- eralarousal,suggestingbothobjectstobeequallyinteresting.Given thatthesignificantdifferencesbetweenconditionswithintheP400 componentisnottypicallyreflectiveofattentionalorperceptual processing,andthelackofthesignificantNccomponentwhichtyp- icallyis,suggeststhatattentionalorperceptualprocessingalone isnotresponsibleinexplainingthedifferencebetweenthetwo motiontypes.Rather,thepresentfindingsarecompatiblewiththe ideathatitisthesocialnatureofthechasinginteractionthatdrives thedistinction.

WhiletheresultsinStudy1arenovelandimportantforunder- standingthedevelopmentofchasingperception,itmaybeargued thatthesocialnessofthestimuliisrelatedtotheindividualagents, and not tothe interaction betweenthem. In Study 2 we again presentedinfantswithachasing motionbut compared ittoan animationwherethegoal-directednessofthechaserwasreplaced withrandomanimatemotion,whicheffectivelyeliminatestheper- ceptionofinteractivitybetweenthetwoagents.Wehypothesize thatifthecontingencybetweenthetwoagentsisthemainfactor elicitingtheP400component,weexpectthesameP400component

inthesecondcomparison.GivenfindingsinStudy1,wealsoexpect asignificantN290componentwhenchasingmotioniscompared torandom.Finally,wedonotexpectasignificantdifferenceinthe Nccomponent.

3. Study2:chasingversusrandom 3.1. Methods

InordertoexaminewhethertheresultsinStudy1aredueto9- month-olds’sensitivitytotheinteractionbetweenthetwoagents, ratherthananimacyofindividualagents,hereweexamineinterac- tionthroughcorrelatedmotionasasourceofsocialness.Unlikein Study1,herebothtypesofanimationsdepictedobjectsthatmoved oftheirownenergysourceratherthanasamechanicalresultofcol- lisionwithstationaryobjectswithinthedisplayoritsboundaries.

InStudy2,keepinganimacyconstant,wevariedthemotioncon- tingency.Whileinthechasinginteractionthechasingagentmoved inagoal-directedwaytowardthetarget,asthetargetmovedaway inresponse,intherandommotionbothobjectsmovedinnorela- tiontoeachother.Inthiscase,themotionofoneobjecthadno consequenceonthemotionofthesecondobject.

3.2. Participants

Eighteen9-month-oldinfants(6female;meanage=280days;

9months7days)wereincludedinthefinalsample.Allparticipants werefull-termwithoutknownneurologicalordevelopmentaldis- abilities.Additional15infantsweretestedbutwerenotincluded intheanalysisduetofailuretomeettheinclusionarycriterionof minimum10artifactfreetrialsforeachstimulusset.Noneofthe infantswhoparticipatedinStudy1participatedinStudy2.

3.3. Stimuliandprocedure

TheprocedurewasidenticaltotheoneinStudy1,inthatall childrensawblockswithvideoanimationsfollowedbythestatic ERPimages.Themaindifferencebetweenthetwoprocedureswas thatthestimulipresentedwerethechasinginteractionfromStudy 1andanewrandommotionanimation.

3.3.1. Randommotionanimation

TheRandommotionanimationwascreatedonthebaseofthe Chasinginteraction.AsintheChasinginteractionanimation,the Randommotionanimationdepictedthemainshape(orangetrian- gle/bluerectangle)movecontinuouslyataconstantvelocityof0.4 visualdegrees/frame(12pix/frame).Themotionofthegraycirclein therandommotionanimationwassimilartoitsmotioninthechas- inginteraction.Thatis,thegraycirclemovedatabaselinevelocity of0.2visualdegrees/frame(6pix/frame).Justlikeinthechasing interaction,thegraycircleacceleratedto0.8visualdegrees/frame (24pix/frame)for24framesandreturnedtoitsoriginalvelocity4 timesduringthetrial.But,unlikeinthechasinginteraction,here bothshapesmovedindependentlyofeachotherfollowingdiffer- enttrajectories,neveroverlapping.Justlikethechasingmotion,a 4-notesoundwasused.Thesoundwasthesameastheoneused inchasingmotionbutwithalowerpitch.Here,ratherthanbeing dependentonaproximityofthechasertothetarget(sincethey movedindependentlyfromeachother)thesoundoccurredatthe sametimeasinthechasingmotion,momentsbeforethetarget’s accelerationbouts.Thus,inbothconditionsthesoundwascontin- gentonthetarget’saccelerationprofile.

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3.4. EEGrecordingandanalysis

TherecordingandanalysisprocedurewasidenticaltoStudy1.

Onaverage,infantsattendedto58.5trials(range:40–74ofwhich 58.6werechasertrialsand58.4wererandomagenttrials).The samecriteriawereusedforchannelandtrialrejectionasinStudy1.

Asaconsequence,onaverage13.4chasertrials(range:10–24)and 13.4randomagenttrials(range:10–26)perinfantwereincludedin thefinalanalysis,Pairedsamplet-testt(17)=0.039,p=0.970.Again, theaggregatedERPamplitudefortheP400waswithintheinterval 350–650msafteronsetoftheimageandwithin400–600msfor theNccomponent.

Eachchildobservedbetween2–5remindervideopresentations (M=3.5,SD=0.90)andonaveragetotalstimulipresentationlasted approximately6min9s.

3.5. Results

3.5.1. P400

AsinStudy1fortheP400component,a2(chaser,inanimate agent) x 2(hemisphere: left, right) repeated measures analy- sisof variance revealed a significantmain effect of agent type F(1, 17)=12.20, p=0.003, ␩2=0.418 with a significantly higher amplitude for the chaser (8.48␮V, SE=2.70) than the random animateagent(-0.221␮V,SE=2.69)(Fig.3).Theanalysisalsoindi- cated a significant main effect of hemisphere, F(1, 17)=44.47, p<0.001,␩2=0.723,withahigheramplitudeintheright(13.26␮V, SE=3.05)thanleft(-5.0␮V,SE=2.44)channels.Therewasnosig- nificanthemispherebyagentinteractionF(1,17)=0.472,p=0.501,

2=0.027.

3.5.2. Nc

For theNc component, a Paired samplest-test furtherindi- catednosignificantdifferencesbetweenagenttypes,t(17)=0.586, p=0.566 with positive amplitudes for the chaser (1.26␮V, SE=0.88)andtherandomlymovingagent(.87␮V,SE=0.75).

3.5.3. P200andN290

As in Study 1, there was a positive inflection at around 200msfollowedbyanegativedeflectionataround300mspost stimulusonset.Here,asinStudy1,theN290componentdemon- strated significantly higher positive amplitude for the chaser (3.38␮V,SE=3.21),andanegativeamplitudefortherandomagent (−6.56␮V,SE=3.33),t(17)=3.60,p=0.002.UnlikeinStudy1,at theP200component,thedifferencebetweentherandomagent (−6.85␮V,SE=2.64)andthechaser(0.59␮V,SE=2.42),wassig- nificantt(17)=2.88,p=0.010.

Finally, as in Study 1, for all the components tested, none correlatedsignificantlywiththenumberofremindervideos(all ps>0.05).

3.6. Discussion

TheresultsfromStudy2showthat9-month-oldinfantsareable todifferentiatebetweenanagentpreviouslyengagedinachasing interactionandananimateagentthatpreviouslymovedrandomly inrelationtoanotheragent.AsinStudy1,findingsdemonstratea significantlypositiveERPcomponentaround400msforthechasing agentcomparedtotherandomagentandasignificantdifference characterizedbyanegativedeflectioninbothagentsaround290ms (N290).Thesefindingssuggestthatchasingisperceivedasasocial eventinvolvingtwo(orpossiblymore)interactingagentsearlyin infancy.JustlikeinStudy1,therewasnosignificantdifferencein theNccomponentinStudy2,againindicatingthattheobjectsin bothconditionswereequallyattentiongrabbing.

Thedifferenceinfindingsbetweenthetwostudiesisthathere unlikeinStudy1,theP200showsloweramplitudefortherandom agentcomparedtothechaser.Thisfindingisinterestingasitsig- nifiesthatthechaserisidentifiedandprocessedasaninteracting entityveryrapidly.Suchstrongandfastreactioninresponsetothe agentwhosemotioniscorrelatedwithanotheragentsuggestthat socialinteractionsand/orrelationsareinvolvedinverybasicper- ceptualprocessesthatmayinfluencelater processingstages-an importantquestionforfutureresearch.

4. Generaldiscussion

Theprimary purposeofthepresent studieswastotest two theoretical perspectivesonanimacy perception in infancy.One explanationclaimsthatanimatedinteractionsareconceptualized associaleventsbasedona combinationofmotioncuessuchas self-propulsion,goal-directednessandinteractivity(motioncon- tingency)betweenagents.Anotherclaimsuggeststhatpreference for thesocial motionsinvolves a low-levelperceptual process- ingofindividualmotionparameterscausingtheattentionalshift towardthefeaturesofthemotion.Inaddressingthistheoretical distinction,weexaminedwhetherby9-monthsinfantsareable todifferentiatebetweenanagentthatwaspreviouslyengagedin achasing interactionfromanobjectthatengagedina different typeofmotion.Acrosstwostudieswepresentedinfantswithshort videosdepictingtwogeometricalshapeseitherbeinginvolvedin achasinginteraction(Study1and2),movinginanimately(Study 1)ormovingrandomly(Study2).Withthesecomparisonswevar- iedtheobject’sanimacy(Study1)andinteractivitybetweenthe agentswhilekeepinganimacythesame(Study2).Indoingso,we haveprovidedthefirstevidencefortheneuralcorrelatesofchas- ingperceptioninyounginfants,whichprovidedsupportforthe involvementofthesocialnetworkduringobservationofchasing.

Bothstudiespostulateevidenceofastrongpositiveamplitude forthechasingagentinthelowoccipitalandposttemporalareas 400mspoststimulusonset.Giventhatpriorresearchexamining earlyperception tosocial information in infancyfound a simi- larP400component(Bakkeretal.,2015,2016;Gredebäcketal., 2010;Melinderetal.,2015;Senjuetal.,2006),presentfindingsare compatiblewiththenotionthatthechasinggeometricalshapeis processedasasocialagentcomparedtoaninanimateobjectora randomlymovingobject.Thishighlightsthatanimacyalonemay notfullyexplaintheeffectbutratherthesocialnessofthechas- ingeventthatdrivestheeffect.Furthermore,giventhattheP400 componenthasbeenfoundtobeanindexforadultpSTSactivity whichinturnhasbeenshowninresponsetointeractinganimated interactionsofwhichchasingmaybeconsideredthehallmark(Gao etal.,2009),itislikelythattheinfantP400foundherehasitsmain sourcesinthepSTS.

In both studies, we find a main effect of hemisphere with higherP400amplitudeintherightthanleftchannels.Thisfinding corroborateswithpreviousadultresearchthathasfoundhigher engagementoftherightpSTSwhenobservingcorrelatedmotion suchaschasing(Schultzetal.,2005).Inotherstudies,theengage- mentoftherightpSTShasbeenespeciallysensitivetogoalsand intentionsbehindmotion(Gaoetal.,2012)aswellasinresponse tounsuccessfulcomparedtosuccessfuloutcomesofgoal-directed actions(Shultzetal.,2011).

In additiontotheP400component, herewefindanegative deflectionaround290ms.Forboththerandomandtheinanimate agent,theN290waslarger(morenegative)followedbyalower (lesspositive)P400amplitudeincomparisontothechasingagent.

Previousresearchsuggeststhatthisamplitudepatternmayappear fornovelratherthanfamiliarstimuliin9-month-olds(Keyetal., 2009butseealsoKeyandStone,2012;Scottetal.,2006),suggesting

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Fig.3.GrandaverageERPdataforselectedchannelsfortheNccomponent(ingreen;topgraph)andP400component(inred)oftheLeft(bottomleftgraph)andRight (bottomrightgraph)hemispherewithtimeofinterestshadedingray.(Forinterpretationofthereferencestocolorinthisfigurelegend,thereaderisreferredtotheweb versionofthisarticle.)

ittobe involvedin longerprocessing and greatervisualatten- tion.Itisthuspossiblethattheinanimateagentandtherandom animateagentrequiredmorevisualprocessing,whilethechasing agentwasmoreeasilyrecognizedassuch.Increasedvisualatten- tiontorandomlymovingshapeshasalsobeenpreviouslyfoundin 5-month-oldinfantswhenpresentedwithadisplayshowingdiscs chasenexttoadisplayswithinanimatelymovingdiscs(Rochat etal.,1997).

TheinfantN290/P400complexhasbeensuggestedtobethe precursortotheadultN170(deHaanetal.,2003,2002;Halitetal., 2003),whichinadultshasbeenlocalizedtothefusiformgyrusand thesuperiortemporalsulcus(ItierandTaylor,2002,2004)acti- vatedduringperceptionof socialstimuli, biologicalmotionand animatemotion.Herewefindsimilarcomponents,suggestingthat theamplitudedifferenceduringchasingperceptionmayberelated tothesocial aspectsofinteractionsrather thanthepresenceof motioncuespertainingtoanimacyasdefinedbytheviolationof theNewtonianlawsofmechanics.However,whichaspectsofthe chasinginteractionsmayberesponsiblefortheemergenceofthe N290/P400complexisanimportantquestionforfutureresearch andonethatisbeyondthescopeofthepresentpaper.Goodcandi- datesforfurtherassessmentmaybecorrelatedmotionbetween thechaser and thetarget,such asthegoal-directednessof the chaserandthecontingentreactionofthetarget.Sincetheprocess- ingresponsesaresorapid,visualpop-outparadigmscouldpossibly beusedinparallelwithneurophysiologicalmeasures.

Study 1 did not find any differences in the Nc component betweenanimateandinanimateobjects,asKaduketal.(2013)did.

Thedifferentfindingsmighthavetodowiththewayanimacywas

measuredin bothstudies.InKaduketal.(2013)asingleobject wasmovingthroughanobstaclecoursecontinuouslyeitherviolat- ingorabidingbytheNewtonianlawsofphysicsfromasideview.

Incontrast,inthepresentstudy,infantswerepresentedwithtwo objectsfroma topview,andtheyhad toprocess notonlyhow theobjectsmoveintheirenvironmentbutalsohowtheymove inrelationtoeachother.Giventhefindingthatinanimatemotion engagesincreasedattention(Kaduketal.,2013),itispossiblethat motioncuespertainingtoasociallycontingentinteractionbetween agentsrequiredsimilarattentionaleffortastheinanimatemotion, renderingtheeffectnull.Itcouldalsobethatwehavea“ceiling effect”sincetheinfantshadtotrackmultipleobjects.Inallcases,it seemslikeallconditionsinourstudieswereequallyengagingfor theinfants.

InadditiontotheN290/P400complex,in bothstudiesthere wasapositivepeakaround200msfollowingthestimulusonsetto thechasingagentcomparedtoinanimateandrandomagent.But, thedifferenceinamplitudeswasonlysignificantwhenthechas- ingagentwascomparedtotherandomlymovingagentinStudy2, wheretheamplitudefortherandomagentwasnegative.Previous researchinadultpopulationfoundthatthevisualP200component intheposteriorareaisinvolvedincognitiveprocessessuchasfea- turedetectionandretrieval(LuckandHillyard,1994),memoryload performance(Klaveretal.,1999),andsemanticprocessingaswell ashigher-orderperceptualprocessing(Freunbergeretal.,2007).In onestudy,Yorioetal.(2008)suggestthattheearlypositivewave hastodowiththeformationofperceptualcategoriesbetweenfirst andsecondobjectsaswellasavisualdiscriminationandrecollec- tionofpreviouslyseenitems.Otherstudiesfoundtheamplitude

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aroundtheP200toincreasefollowingvisualdiscriminationtrain- ing(Dingetal.,2003),proposingthattheP200mightbeinpart responsibleforstimulusencodingandlaterrecall.Inourcase,the higherpositiveamplitudeforthechasingcouldthereforeindicate categorizationofthestillimagesbasedonpreviousdifferencesin motionaswellasvisualdiscriminationofthechaserfromtheoth- ers.Furthermore,giventhattheonlydifferencebetweenthetwo studieswasinthepresenceofasignificantdifferenceintheP200 whenchasingwascomparedtorandommotion,itmayhavetodo withthepresenceofmotioncontingencybetweentheobjects.It wouldbestrikingiftheP200wefoundininfancyisindicativeof earlyperceptionofsocial relationshipsformingafoundationfor highercognitiveprocessing.To us,this isanimportant finding, whichmeritsfutureresearchtoinvestigatethisissueindetail.

Apotentialconfoundinthepresentstudyhastodowiththe auditorydifferences between theconditions. While the sounds mayhaveaidedindifferentiatingbetweentheshapes,theydonot accountfortheseeneffects.Currentliteratureonauditorypro- cessingsuggeststhatadetectionofamismatchtopitchchanges, suchasthoseinStudy2resultsinaslowpositivewavebetween 100and400msatthefrontalandcentralregions,withareversed polarityattheparietal,occipitalandtemporalregionsininfants(He etal.,2007).Otherstudies,dependingontheexperimentaldesign, findthepresenceofaP300(peakbetween250and350ms)com- ponentovercentralandparietalareasininfantswhenpassively listeningtovaryingtones(McIsaacandPolich,1992),whileothers findthesamecomponentoverfrontalandcentralelectrodesites (Kushnerenkoetal.,2002;Leppänenetal.,1997).Inthepresent study,wedonotfindtheP300component.Intheposteriorsiteswe findanegativedeflectionataround300ms,whileinthefrontalcen- tralareasasmeasuredbytheNccomponent,wefindslightlymore positiveamplitude,butnosignificantdifferencesbetweencondi- tions.Thus,thespecificeffectisunlikelyattributedtotheauditory differences.

Inconclusion,thepresentfindingsdemonstrateforthefirsttime thatneuralcomponentsresponsibleforthechasingperceptionis differentfrominanimateandrandommotionprocessing.Weshow thatsimilartoadults,chasingisevaluatedasasocialinteractionin infantsasyoungas9months,whichwasindexedbythedifferences inthesociallyvalencedN290/P400complex.Wealsoshowthat theP200ismodulated,whichindicatesthatthesocialproperties ofobjectsareinvolvedveryearlyinvisualprocessing.

Acknowledgements

Wethanktheparentsandinfantsfortheirenthusiasticcooper- ation.ThisresearchreportwassupportedbytheSwedishResearch Council(VR-2011-1528)andERCStGCACTUS(312292).

AppendixA. Supplementarydata

Supplementarydataassociatedwiththisarticlecanbefound,in theonlineversion,athttp://dx.doi.org/10.1016/j.dcn.2016.05.005.

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