Neural mirroring and social interaction: motor system involvement during action observation relates to early peer cooperation

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ContentslistsavailableatScienceDirect

Developmental Cognitive Neuroscience

jou rn a l h om ep ag e : 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

Neural mirroring and social interaction: Motor system involvement during action observation relates to early peer cooperation

H.M. Endedijk

^a,b,∗

, M. Meyer

^a

, H. Bekkering

^a

, A.H.N. Cillessen

^b

, S. Hunnius

^a

aDondersInstituteforBrain,CognitionandBehaviour,RadboudUniversity,Nijmegen,TheNetherlands

bBehaviouralScienceInstitute,RadboudUniversity,Nijmegen,TheNetherlands

a r t i c l e i n f o

Articlehistory:

Received23June2016 Receivedinrevisedform 24November2016 Accepted3January2017 Availableonline7January2017

Keywords:

Neuralmirroring Interpersonalcoordination Cooperation

Socialinteraction Peers

Earlychildhood

a b s t r a c t

Whetherwehandoverobjectstosomeone,playateamsport,ormakemusictogether,socialinteraction ofteninvolvesinterpersonalactioncoordination,bothduringinstancesofcooperationandentrainment.

Neuralmirroringisthoughttoplayacrucialroleinprocessingother’sactionsandisthereforeconsid- eredimportantforsocialinteraction.Still,todate,itisunknownwhetherinterindividualdifferencesin neuralmirroringplayaroleininterpersonalcoordinationduringdifferentinstancesofsocialinteraction.

Arelationbetweenneuralmirroringandinterpersonalcoordinationhasparticularlyrelevantimplica- tionsforearlychildhood,sincesuccessfulearlyinteractionwithpeersispredictiveofamorefavorable socialdevelopment.Weexaminedtherelationbetweenneuralmirroringandchildren’sinterpersonal coordinationduringpeerinteractionusingEEGandlongitudinalbehavioraldata.Resultsshowedthat 4-year-oldchildrenwithhigherlevelsofmotorsysteminvolvementduringactionobservation(asindi- catedbylowerbeta-power)weremoresuccessfulinearlypeercooperation.Thisistheﬁrstevidencefor arelationbetweenmotorsysteminvolvementduringactionobservationandinterpersonalcoordination duringotherinstancesofsocialinteraction.Theﬁndingssuggestthatinterindividualdifferencesinneural mirroringarerelatedtointerpersonalcoordinationandthussuccessfulsocialinteraction.

1. Introduction

Ourdailylifecontainsamultitudeofsocialinteractionsinwhich we coordinateouractions withothers. Theinvolvement ofthe mirrorsystemin action perception, monitoring,and prediction (e.g.,Bekkeringetal.,2009;Kilneretal.,2007;Southgateetal., 2009;Stapeletal.,2010)isthoughttohelpusprepareandexecute ourownactionsincoordinationwithothers(Kourtisetal.,2013;

Sebanzetal.,2006).Convergingneuroimagingevidencehasshown thatourmotorsystembecomesactivatedbothwhenperforming anaction,andwhenobservinganaction(MarshallandMeltzoff, 2011;RizzolattiandCraighero,2004;RizzolattiandFogassi,2014).

Thisneuraloverlapbetweenactionproductionandperceptionhas beencalledneuralmirroring(e.g.,HariandKujala,2009).Ithasbeen suggestedthatneuralmirroringprovidestheneurocognitivebasis forprocessing others’ actionsand thereforeplaysa crucial role

∗ Correspondingauthor.Presentaddress:UtrechtUniversity,Heidelberglaan1, 3584CSUtrecht,TheNetherlands.

E-mailaddresses:h.m.endedijk@uu.nl(H.M.Endedijk),m.meyer@donders.ru.nl (M.Meyer),h.bekkering@donders.ru.nl(H.Bekkering),a.cillessen@psych.ru.nl (A.H.N.Cillessen),S.Hunnius@donders.ru.nl(S.Hunnius).

insuccessfulinterpersonalcoordinationduringsocialinteraction (Bekkeringetal.,2009;HariandKujala,2009).

Previous findings supportthis hypothesis ofa close relation between neural mirroring and interpersonal coordination. For instance, adults who showed more motor system involvement whenobservinga partner’smovementsinafingertappingtask alsocoordinatedtheirmovementsbetterwiththepartner(Naeem et al., 2012).While imitative actionsoccur during social interaction, especially complementaryactions arerelevant in which individualsperformdifferentactions(Bekkeringetal.,2009),for examplewhenpassingandcatchingaball.Complementaryactions werealsorelatedtomotorinvolvementoftheneuralmotorareas duringactionobservation(Ménoretetal.,2014).Comparablefind- ings are present for children, as youngchildren who mirrored anadultactionpartnermorethananotheradultinaturn-taking gamemadefewererrorsininterpersonalcoordinationduringthat game(Meyeretal.,2011).Similarly,recently,Filippietal.(2016) foundthatelevatedlevelsofmirroringin7-month-oldinfantspre- dictedtheirimitationofothers’toychoices.Thesefindingssupport a linkbetweenneuralmirroringandinterpersonalcoordination withinthesamelaboratorytask. However,thedegreetowhich interindividualdifferencesinneuralmirroringsupportthesuccess invariousinstancesofsocialinteractionisunknown.

https://doi.org/10.1016/j.dcn.2017.01.001

0/).

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34 H.M.Endedijketal./DevelopmentalCognitiveNeuroscience24(2017)33–41

Whiletheroleofinterindividualdifferencesinneuralmirroring forinterpersonalcoordinationisunclear,studiesofsocialcogni- tion(e.g.,empathy,perspectivetaking)highlightaroleofmirroring forsocial skillsthat arenot task-speciﬁc.In adults,neuralmir- roringisrelatedtohigherlevelsofperspectivetaking(Woodruff etal.,2011),empathy(Gazzolaetal.,2006;Hookeretal.,2010;

KaplanandIacoboni,2006),andsocialcompetenceasassessedwith questionnaires(Pfeiferetal.,2008).Inthisstudy,weinvestigated whetherinterindividualdifferencesinneuralmirroringalsomight playaroleininterpersonalcoordinationduringsocialinteractions outsidethespeciﬁctask.

Insocialinteraction,two typesofinterpersonalcoordination occuroften:cooperationandentrainment.Whileincooperation, coordinationisplannedandtypicallyinvolvesagoal-directedtask, in entrainment, coordination emerges spontaneously without a jointgoal(Knoblichetal.,2011).Forinstance,soccerplayerscoop- eratebykeepingtrackofeachotherandadjustingtheirpositions accordingly to obtainthe ball and shoot it at the goal.During applause,ontheotherhand,peopleentrainbycoordinatingtheir clappingbehaviorspontaneously.In cooperation,itisimportant tomonitorothers’actionswithrespecttotheachievementofthe commongoal.Inentrainmentthefocusratherisonthemonitor- ingoftheothers’movements.Importantly,boththeobservationof movementsandgoal-directedactionswerefoundtoactivatethe humanmirrorsystem(RizzolattiandCraighero,2004;Rizzolatti andFogassi,2014).Therefore,weexpectedthathigherlevelsof mirroringwouldberelatedtobothhigherlevelsofcooperation andentrainmentsituationsoutsidethespeciﬁcmirroringtask.

Activation of the mirror system during action observation alreadyhasbeendemonstratedininfancy(MarshallandMeltzoff, 2011). Investigating therelationbetween neuralmirroring and interpersonalcoordinationisespeciallyimportantinearlychild- hood,since proﬁciency in social interactionat this age,mainly withpeers,predictssocialcompetencelaterinlife(e.g.,Hayetal., 2009;Rubinetal.,2006).Childrenalreadydemonstrateactioncoor- dinationwithpeersintoddlerhood (e.g.,Ashley and Tomasello, 1998;Brownell,2011;Endedijketal.,2015a;Hunniusetal.,2009).

Duringthepreschoolyears,children’sinterpersonalcoordination continuestodevelop,astheybegintorespondmorequicklytothe behaviorofothersandbecomemorestableincoordination,both incooperation(AshleyandTomasello,1998;Endedijketal.,2015a;

Fletcheret al., 2012)and in entrainmenttasks (Endedijk et al., 2015b).Throughoutearlychildhood,childrengainampleexperi- encewithinterpersonalcoordination.Childrenwhofacedifﬁculties withsocialinteractionsearlyinlifemoreoftenexperiencerejec- tionbypeerslateron(Friedlmeier,2009;NICHDEarlyChildCare ResearchNetwork,2008)withsubsequentnegativeconsequences fortheirsocialfunctioninginadolescenceandadulthood(Bagwell etal.,1998).Clarifyingtheprocessesinvolvedinearlyinterpersonal coordinationwithpeersisveryimportantforunderstandingsocial development.

Thecurrent study examinedtherelation betweeninterindi- vidualdifferencesinneuralmirroringandyoungchildren’ssocial interactionskills.Children’sneuralmirroringwasassessedbymea- suringoscillatorybrainactivity(bymeansofEEG)duringaction observation.Inparticular,themu-andbeta-frequencybandsover motor areas have been associated with motor system involve- mentduringactionobservation(cf.Meyeretal.,2011;Pfurtscheller andLopesdaSilva,1999;Pineda,2008;SabyandMarshall,2012;

Vanderwertetal.,2013).Toinvestigatetherelationbetweenneural mirroringandinterpersonalcoordinationwithpeers,motorsystem involvementduringactionobservationwasassessedin4-year-old children.Aspartofalongitudinalstudytheirinterpersonalcoor- dinationhadbeenassessedearlierat28,36,and44months,ina cooperationtaskandinanentrainmenttaskwithdifferentpeers.

Basedonpreviousresearchsuggestingthefunctionalinvolvement

ofneuralmirroringduringinterpersonalcoordination(Meyeretal., 2011;Naeemetal.,2012),wehypothesizedthatinterindividualdif- ferencesinchildren’sneuralmirroringofothers’actionswouldbe associatedwithbothformsofinterpersonalcoordination(cooperationandentrainment).

2. Method 2.1. Participants

Thesampleconsistedof29children(10boys)whoparticipated inanEEGexperimentat52monthsofage(M=52.48,SD=1.94).

Interpersonalcoordinationwithpeershadbeenassessedinplay sessionsat28months(M=27.96,SD=0.33),36months(M=35.98, SD=0.34),and44months(M=43.83,SD=0.34).Theparticipants werepartofalargersampleof181childrenwhosesocialdevelop- mentwasstudiedlongitudinallyfromtoddlerhoodtoearlyschool age.Childrenwere selectedfromthelargersample iftheyhad participatedinthreeplaysessions(i.e.hadnotmissedasession) andwerewillingtoparticipateinEEGresearch.Theplaysessions tookplaceinthelabwithanunfamiliarsame-genderpeer(also ofthelongitudinalstudysample),eachplaysessionwithadiffer- entpeer.AllchildrenwereDutchandfrommixedsocio-economic backgrounds.Allwerehealthyandhadnoindicationsofatypical development.Parentswereinformedofthestudyandgavewrit- tenconsent.Aftereachtestingsession,childrenreceivedabookor asmallamountofmoney“fortheirpiggybank”asathankyoufor participation.

2.2. Procedure

TheEEGsessiontookapproximately60minincludingfamiliar- izationwiththeexperimenters,preparing theEEGcap,andthe measurementitself(seeSection2.3).Duringtesting,childrenwere videotapedfromtwovisualangles(withonecameradirectedat thechild’supperbody andtheotheroneat thechild’slegs)in ordertoremovetrialsinwhichthechildwasmovingordidnot payattention.

Previously,childrenhadparticipatedinthreeplaysessionsto assesstheirinterpersonalcoordination(seeSections2.4and2.5).

Theplaysessionsstartedwith10–30minoffreeplayduringwhich childrengotfamiliarizedwitheachotherandtheexperimenters.

The introductory phase was followed by the cooperation task, whichtookabout5min.Theentrainmenttaskfollowedwithamax- imumdurationof5min.Parentswereinstructedtominimizetheir interactionswiththeirchildandifthechildwasclingingtothem, respondinwaystostimulateinvolvementinthesessionwithout helpingwiththetasks.Eachsessionlastedabout45minandwas videotapedfromtwovisualanglesusingtwovideocameras.

2.3. Actionobservationtask

Toassesschildren’sindividuallevelsofneuralmirroring,EEG was measuredwhile they watched videos of actions. The task hadtwo conditions:actionobservationand abstractmovement observation.Intheactionobservationcondition(Fig.1,toprow), childrenobservedavideoofanadultperformingdifferentactions onobjects(e.g.,stackingcupsormovingatoycarintoagarage).

In theabstract movement condition(Fig.1,bottom row), chil- drenobservedabstractshapesmovingacrossthescreen,similar toascreensaver.Thisabstractmovementconditionwasincluded tocontrolfornon-humanmovementperception.Thereweresix action videos and six abstract movement videos, each lasting approximately7s. During both action observationand abstract movementobservationcondition,eachvideowasrepeatedthree timesandprecededbya1000msﬁxationcrossthatfunctioned

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Fig.1.Exampleoftheactionobservation(toprow)andtheabstractmovementobservation(bottomrow)stimuliprecededbythebaseline(ﬁxationcross).

asbaseline(seeFig.1).Theactionobservationconditionwasrun twicewithtwodifferenttaskinstructions(toimitatetheactionor tonamethecoloroftheobjectaftertheobservationofthevideos;

blockedandcounterbalancedbetweenchildren)aspartofadif- ferentstudy.Thus,eachactionobservationvideowasshownsix timesintotalandeachabstractmovementvideothreetimes.After twoactionobservationvideos,oneabstractmovementobserva- tionvideowasshown.Toassesschildren’sneuralactivityduring actionexecution,EEGalsowasrecordedwhilechildrenimitated theactionsafterhavingobservedthem.EEGdataduringtheverbal responsewerenotusedintheanalysis.

Behavioralresponseswerecodedforboththeimitationinstruc- tionandcolornaming.Childrenwereproﬁcientinthecolornaming task,withonechildnaming3outof6,twochildrennaming5out of6,andtheremainingchildrennamingallcolorscorrectly.Forthe imitationtask,theactionsweredividedinthreeparts,e.g.driving thecarto,into,andoutofthegarage.Childrenreceived1pointfor eachpartoftheactiontheyimitated,resultinginamaximumscore of3foreachimitationtrial.Childrenwereatceilinglevelwithan averageimitationperformanceof2.59(range1–3).

EEGrecordingswereconductedusingchild-sizedEEGcapswith 32electrodesitesonthescalp.TheAg/AgClactiveelectrodeswere placedinanactiCap,arrangedaccordingtothe10–20system,and referencedtoelectrodeFCzoverthecentralmidline.Thesignalwas amplifiedusinga32-channelBrainAmpDCEEGamplifier,band- passfiltered(0.1–125Hz),anddigitizedat500Hz.Westrivedto keepallimpedancesbelow60k.

Analogoustopreviousstudies(seeMarshallandMeltzoff,2011;

for a review), we analyzed motor systemactivity by meansof mu-andbeta-oscillatorypoweroversensorimotor areas.Motor system involvement was analyzed during action observation, abstractmovementobservation,andactionexecution.Dataanaly- siswasperformedusingFieldTrip,anopensourceMatlabtoolbox (Oostenveldetal.,2011).Alldatawasdividedinto1-ssegments andre-referencedtotheaverageofallelectrodes.Segmentsdur- ingwhichchildrenmovedordidnotlookatthestimulusdisplay wereremoved.Wevisuallyinspectedtheremainingsegmentsto excludeEEGartifacts(suchasnoisychannelsoreyeblinks).One

child was removedfrom theanalyses due tothe lack of base- linetrialsduringtheabstractmovementobservationcondition.On average,per child120segmentsremainedfortheactionobser- vation(range 33–246),38 segmentsfortheabstractmovement observation(range4–81),12segmentsforthebaselinepreceding theactionobservationstimuli(range3–24),and5segmentsforthe baselineprecedingtheabstractmovementstimuli(range1–12).A DFTﬁlterwasusedtoremovelinenoisefromthedata,andforeach segmentwetookoutpotentialoffsetdifferencesbysubtractingthe meansignaloftheentiretrialfromthesignalateachtimepoint.

WethencalculatedspectralpowerestimatesusingtheFastFourier transformonthe1-ssegmentsincombinationwithaHanningtaper asappliedonthesegmentswithoutoverlap.Finally,wecalculated anaveragepowerforeachconditionforeachchild,touseinthe analysis.

Basedonpreviousresearch(seePfurtschellerandLopesdaSilva, 1999),wefocusedouranalysesonelectrodesovermotorcortices (C3,C4).Tocontrolforinterindividualdifferencesinabsolutepower duetodifferencesinscalpthicknessandelectrodeimpedance,the ratioofpowerduringtheconditionrelativetobaseline(fixation cross)wascomputedforeachcondition.Sincetheseratioswere notnormallydistributed,alogtransformationwasapplied.These scoreswereusedtoindicatechildren’smotorsysteminvolvement ineachcondition(actionobservation,abstractmovementobservation)andduringactionexecution.Asmallerlogratioindicated moresuppressioninaconditioncomparedtobaseline.Basedonthe actionexecutionratio,thesample-specificmu-andbeta-frequency rangewasidentified(seeSection3.1).Normalizedpowervalues werepooledoverthecentralelectrodes(C3,C4)perconditionin theidentifiedmu-andbeta-frequencybandsforfurtheranalysis.

2.4. Cooperationtask

Thecooperationtaskwasa peerversion of Warnekenetal.

(2006)double-tubetask.Thesetupconsistedoftwo1-m-longtubes mountedinparallelonaboxwitha45^◦incline(seeFig.2A).The childrenweregivenaPlaymobilﬁgureinaswimsuitandasmall swimmingpool.Theywereinstructedthattheﬁgurewantedtogo

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Fig.2.Childrenperformingthecooperationtask(A)andentrainmenttask(B).

throughtheslidingtubetotheswimmingpool.Becausethetubes weretoolongforonechildtosimultaneouslyholdtheswimming poolandinserttheﬁgureintothetube,thetwochildrenhadto cooperatetoperformthetasksuccessfully.Adetaileddescription ofthetaskcanbefoundinEndedijketal.,(2015a).

Eachchild’sbehaviorwascodedoff-linefromthevideorecord- ings.Foreachtrial(definedasaslideofthefigurethroughthetube), itwascodedwhethercooperationwassuccessfulornot.Coopera- tiontrialswerecodedassuccessfulifboththechildwhoinserted thefigureintothetubeandthechildwhoheldtheswimmingpool chosethesametube.Cooperationtrialswerecodedasunsuccessful ifchildrenchosedifferenttubesorifonechildperformedthetask alone,resultinginthefigurefallingonthefloor.Tocontrolforthe totalnumberoftrials,thedataweretransformedintoaproportion ofsuccessonthetaskforeachdyad.Forthelongitudinalstudy,the recordingsof20%ofthedyadsateachtimepointwerecodedby twoobservers.Cohen’skappawas0.94onaverage(SD=0.11).

2.5. Entrainmenttask

Fortheentrainmenttasktwo10-inchdrumsofaHaymanchil- dren’sdrumsetandtwoplasticstickswereused(seeFig.2B).The drumswereplacedonastandthatcouldbeadjustedtotheheight ofeachchildsothattheycouldcomfortablydruminstandingposi- tion.Thedrumswereconnectedviapiezocontactmicrophones placedonthedrumheadstocollectMIDIdataviaanAlesisD4drum module.PerformanceswererecordedwithLogicExpress.Children wereinstructedseparatelytostartdrumminganddidnotreceive anyinstructionsaboutdrummingtogetherorcoordinatingtheir drummingwiththeirdyadpartner.

Cross-correlationscommonlyareusedin interpersonalcoordination studies to investigate entrainment (Repp, 2005). We calculated maximum cross-correlations that indicated how a child’shitsbestrelatedtotheirpartner’shitsrhythmicallyacross time.Forthispurpose,thetimebetweenthehitsproducedbyeach childweremeasured.Timeseriesoftheseinter-tap-intervalsofthe twochildrenwereshiftedalongsideeachothertoﬁndthehighest correlationbetweenthetwotimeseries.Thereby,themaximum cross-correlationmeasuredescribesthecoordinationofchildren’s rhythmicbehaviors.

2.6. Analyses

To examine whether interpersonal coordination predicted motor system involvement during action observation(a proxy

forneuralmirroring),twohierarchicalregressionswererun,one predictingnormalizedmu-powerandonepredictingnormalized beta-bandpowerduringactionobservation.Tocontrolformotor systeminvolvementduetonon-humanmovement,thenormal- izedpowerduringobservationofabstractmovementwasentered inStep1ofeachregression.InStep2ofeachregression,themea- suresofinterpersonalcoordinationwereentered:theproportion ofcoordinatedtrialsduringcooperation,andthemaximumcross- correlationduringentrainment.Thescoresforthesetwovariables werestandardizedforeachplaysessionandaveragedacrossthe threesessions, resultinginmeasuresof interpersonalcoordina- tionaggregatedoversessionsandinteractionpartners.Thesethree averagedz-scoreswereenteredinStep2oftheregressionanalysis.

3. Results

3.1. Neuralmirroring

Basedontheobservedsuppressionofpowerduringactionexe- cution(seeFig.3,top),thefrequencybandswereidentiﬁedonthe basisofthegrandaverageasfollows:mufrom7to12Hzandbeta from16to20Hz.Thetopographicdistributionofthesefrequency bandssupportsthea-prioriselectionofelectrodesovermotorcor- tices(seeFig.3,bottom).

Theanalysisofthesespecifiedfrequencybandsyieldedposi- tivenormalizedpowervaluesforbothmuandbetaduringaction observation,M=0.23,SD=0.28,andM=0.20,SD=0.31,andabstract movementobservation,M=0.25,SD=0.44,andM=0.22,SD=0.44, indicatingrelativelymorepowerduringexperimentalconditions thanatbaseline.Similartoactionexecution,thetopographicdis- tributionofnormalizedpowerinmu-andbeta-frequencybands showedarelativelyconfinedpatternofactivationoverlayingmotor cortices(especially at electrode sites C3 and C4) during action observation(Fig.4,toprow).Thetopographicdistributionduring abstractmovementobservationappearedlessconfinedbutmore widespreadalongthemidline(Fig.4,bottomrow).

3.2. Relationbetweenneuralmirroringandinterpersonal coordination

Table1summarizestheresultsofthehierarchicalregressions.

Instep1,motorsysteminvolvementduringabstractmovement observationwasrelatedtoactionobservationvaluesforthemu- frequencyband,butnotforthebeta-frequencyband.Addingthe measuresofcooperationandentrainmentinStep2resultedina

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Fig.3.Top:Normalizedpowerrepresentedasafunctionoffrequency(Hz)withtheleftblue-shadedareaindicatingtheselectedmu-frequencyband(7–12Hz),andtheright yellow-shadedareaindicatingtheselectedbeta-frequencyband(16–20Hz).Negativenormalizedpowervaluesrepresentsuppressionduringactionexecutionwithrespect tobaseline.Bottom:Thetopographicdistributionofthenormalizedpowerinmu-andbeta-frequencybandsduringactionexecution,withwarmcolorsrepresentinghigher normalizedpower(enhancement)andcoolercolorsrepresentinglowerpower(suppression).

signiﬁcantlybettermodelforthebeta-frequencyband,F_change(2, 21)=5.14,p=0.02,R²=0.39,butnotforthemu-frequencyband, F_change(2,21)=0.31,p=0.74,R²=0.02.Forbeta,whilecontrolling fornon-humanmovement,powerreductionwasstronglyrelated to children’s performance on the cooperation task (␤=−0.52, p=0.01).Childrenwhoweremoresuccessfulincooperationwith peersalsoshowedmoreinvolvementofthemotorsystemdur- ingactionobservation.Therewasnosigniﬁcantrelationbetween entrainmentandbeta-bandpower.

4. Discussion

Inthisstudy,weexaminedtherelationbetweeninterindivid- ualdifferences inneural mirroringin youngchildren and their

socialinteractionwithpeersinacooperationandanentrainment task.Wefoundthatyoungchildrenwhoshowedmoremotorsys- teminvolvementwhenobservingothers’actions(asindicatedby a relative reduction in betapower), showedbettercooperation skillswithpeers.Theexplainedvariancewashigh,suggestingthat interindividualdifferencesinmirroringarerelevantforinterper- sonalcoordinationwithpeersinearlychildhood.

Therelationbetweenmotorsysteminvolvementduringaction observationandchildren’speercoordinationisconsistentwithpre- viousﬁndingsthatmirroringisrelatedtomorereliableimitation (Bernieretal.,2007;Filippietal.,2016;Warreynetal.,2013),bet- terinterpersonalcoordinationofﬁngermovements(Naeemetal., 2012),andfewerturn-takingerrors(Meyeretal.,2011).However, thesepreviousstudiesmeasuredneuralmirroringandbehavioral

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Fig.4.Topographicdistributionofnormalizedpowerinmu-(left)andbeta-frequencybands(right)duringactionobservation(toprow)andabstractmovementobservation (bottomrow).Warmcolorsrepresenthighernormalizedpower(enhancement)fortheconditionascomparedtothebaselineandcoolercolorsrepresentlowerpower (suppression)fortheconditionascomparedtothebaseline.

Table1

StepwiseRegressionAnalysisWithNormalizedMuandBetaPowerValuesDur- ingActionObservationasDependentVariables,andNormalized MuandBeta PowerValuesDuringAbstractMovementObservation,CooperationPerformance andEntrainmentPerformanceasIndependentVariables.

Mu(7–12Hz) Beta(16–20Hz)

R² ␤ p R² ␤ p

Step1

Abstractmovement observation

0.46 0.02^* 0.29 0.15

Total 0.22 0.02^* 0.09 0.15

Step2

Abstractmovement observation

0.48 0.03^* 0.17 0.38

Proportioncoordinated trials

0.14 0.47 −0.52 0.01^*

Maximum cross-correlation

0.05 0.79 0.19 0.31

Total 0.24 0.12 0.39 0.02^*

Note.

R²indicatestheamountofexplainedvariancebythepredictors,and␤arestan- dardizedregressioncoefﬁcients.

* p(probability)<0.05.

performanceduringthesameinstanceofsocialinteraction(i.e.one laboratorytask)andthusdidnotaddresswhetherthisrelationis task-specificorreflectsinterindividualdifferencesthatgeneralize tosocialinteractionsoutsidethespecifictask.

Tocapturevariousformsofpeerinteraction,weinvestigated twotypesof interpersonalcoordination:goal-directedcoopera- tion,andentrainmentwithoutanovertcommongoal.Wefound thatneuralmirroringwasrelatedtochildren’sperformanceinthe cooperationtaskbutnotintheentrainmenttask.Thisisconsistent

withpreviousresearchthathighlightedtheimportanceofgoals foraction mirroring(Koskiet al.,2002).Bekkeringetal.(2009) arguedthatmonitoringandpredictinganotherperson’sgoalrather thantheirmovementsisimportantforinterpersonalcoordination becauseitoftenrequiresco-actorstoperformdifferentmovements toachieveacommongoal.Inthecurrentcooperationtaskalso,chil- drenhadtoassumecomplementaryrolesthatrequiredmonitoring ofeachother’sactions.

Theobservedlinkbetweenneuralmirroringandcooperation wasevidentforbetapower(16–20Hz).Formupower(7–12Hz), however,no indicationfor sucha relationwasfound.Previous researchhasshownthatbothmuandbetapoweraremodulated duringactionobservation,althoughtheyhavebeenassociatedwith slightlydifferentfunctions(Caetanoetal.,2007;Meyeretal.,2011;

QuandtandMarshall,2014;Schuchetal.,2010).Mu-bandactiv- ityissuggestedtobeinvolvedintranslatingsensoryinputinto motorprocesses(Naeemetal.,2012;Pineda,2005;Vanderwert etal.,2013),whichmatcheswithitsmoreposteriorlocalization over sensorimotor regions of the brain (Ritter et al., 2009). In contrast,thelocationofbetaoscillatoryactivityistypicallymore anterioranditisassociatedwithactivityinthemotorandpre- motorcortex(Ritteretal.,2009).Ithasbeensuggestedthatboth mu-andbeta-bandoscillationsareinvolvedinactionpredictions (Southgateetal.,2009;Stapeletal.,2010),whilebeta-bandactivity isassociatedspeciﬁcallywithpredictionupdatinganderrormon- itoring(Arnaletal.,2011;Koelewijnetal.,2008).Exactlythese processes–monitoringothers’actionsandintegrating informa- tioninordertoupdateactionpredictions–areimportantduring cooperation(Kourtisetal.,2013;Sebanz etal.,2006).Updating actionpredictionsandmonitoringwereessentialforthecurrent peercooperationtask.Predictingwhich tubethepartnerwould

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choose,monitoringthepartner’sbehaviortocheckwhetherthe predictionwascorrect,andupdatingone’spredictionswerenec- essarytosucceedonthetask.Thismightalsoexplainwhyarelation betweencooperationperformanceandoscillatorymodulationwas observedinthebeta-band,ascontinuouspredictionandupdating ofpredictionsareinherenttoactionobservation(Falck-Ytteretal., 2006;GredebäckandMelinder,2010;Kilneretal.,2007).Still,the exactfunctionaldifferencesbetweenmu-andbeta-bandoscilla- tionsandtheirrespectiverolesduringactionobservationhaveto bedeterminedinfutureresearch.

For bothmu- andbeta-power,we observedthat powerval- ueswerehigherduringactionobservationthanbaselineindicating enhancementratherthan suppression.Atﬁrstsight,this issur- prisingsincepreviousresearchsuggeststhatsuppressionofmu- andbeta-powerindicateincreasedinvolvementofthemotorsys- tem(MarshallandMeltzoff,2011;RizzolattiandFogassi,2014).

However,severalrecentstudiesalsofoundthatpowerinthese frequency bands is not significantly suppressed during action observation(Cannonetal.,2016;Nyström,2008;PerryandBentin, 2010)orevenenhanced(Marshalletal.,2013).Althoughinour studytheneuralresponseshowedanunexpecteddirectionality withregardtobaseline,weareconfidentthatthemu-andbeta- band activityreflects a response of the motor systemfor two reasons.First,theeffectwasrelativelyconfinedtoelectrodesites overlayingovermotorareas(C3,C4),whichsuggestsamodulation ofthemotorsystem.Second,childrenwereaskedtositmotion- lessandwatchthreerepetitionsofeachactionvideoonthescreen beforetheywereallowedtorespond.Thus,childrenlikelytriedto activelyinhibitanovertmotorresponseduringtheactionobser- vation,and this wasassociatedwithanincrease inbeta-power (Gilbertsonetal.,2005).Notably,thismotorinhibitiondidnotaffect thedirectionoftherelationwefound.Thatis,lessbetapowerwith respecttobaseline(indicatingrelativelymoremotoractivity)was relatedtomoresuccessduringpeercooperation.Althoughchil- drenthuslikelysuppressedtheirmotoractivityingeneraltositas motionlessaspossible,interindividualdifferenceswithrespectto howsensitivetheirmotorsystemwastoactionobservationwere stillrelatedtotheircooperationbehavior.Totestwhetherinhibi- tionindeedplaysarole,itisimportanttostructurallyinvestigate thisinfuturestudiesbyincludingaconditionwithoutanyinstruc- tioninwhichchildrenobserveexactlythesameactions.

Ourresultssuggest thatinterindividual differencesinneural mirroringare related to successfulcooperation. Yet,the causal directionunderlyingthisrelationremainsanopenquestion.Bet- terinterpersonalcoordinationlikelyistheresultofhighergeneral levelsofneuralmirroring.Previousresearchhasshownthatneural mirroringsupportsprediction(e.g.,Southgateetal.,2009;Stapel etal.,2010)andmonitoringofothers’actions(Becchioetal.,2012;

Bekkeringetal.,2009)aswecanuseourownactionsystemto predicttheactionsofapartner(Kilneretal.,2007).Enhancedpre- dictionand monitoring,in turn,might helpus preparefor and executeourownactionsaccordingly(Kourtisetal.,2013;Sebanz etal.,2006).Basedonthisreasoning,individualswithhigherlevels ofneuralmirroringmightbebetteratcoordinatingtheiractions withothers. However, neuralmirroring and cooperationmight alsobothbetheresultofathirdfactor,suchassocialmotivation.

Childrendifferintheirmotivationtobeinvolvedinsocialinterac- tions(BrownellandHazen,1999),whichcouldimpactboththeir level ofmirroringand theircooperationsuccess. Neuroimaging studiesinadultshaveshownaroleofsocialmotivationformir- roringastheyfoundenhancedmirroringwhenparticipantswere sociallyprimed(HogeveenandObhi,2012;Obermanetal.,2007), andenhancedmirroringforin-groupmembersthanforout-group members(Gutselland Inzlicht,2010; Molenberghset al.,2013;

Rauchbaueretal.,2015).Studieswithadultsalsosupporttheroleof socialmotivationininterpersonalcoordination:Adultswithapro-

socialorientationcoordinatedtheiractionsbetterthanadultswith apro-selforientation(Lumdsenetal.,2012).Whetherchildren’s neuralmirroringisreallyatthebaseoftheirinterpersonalcoor- dinationorwhetherbotharetheresultoftheirsocialmotivation hastobeaddressedinfutureresearch.Hereby,itwouldespecially beinformativetodevelop stimulusvideosactedbychildrenfor children,asthesevideoswouldbemoresociallyrelevantforthem.

Thequestionarisestowhatextentinterindividualdifferences inneuralmirroringplayaroleinchildren’ssocialdevelopment.

Friedlmeier (2009) suggested that adapting behavior might be an indicatorofsocial competence.And Cirelliet al. (2014)and KirschnerandTomasello(2010)foundmorehelpingbehaviorin children aftertheyexperiencedsmooth interpersonalcoordination.Thisincreasedprosocialitycouldbeanindicatoroflikeability, therebysuggestingthathigherlevelsofmirroringresultinbetter peerrelationsviasuccessfulinterpersonalcoordination.However, a relation betweeninterpersonalcoordination and peerprefer- encewasnotpresentinarecentlongitudinalstudyweconducted (Endedijketal.,submitted).Ontheotherhand,theincreasedhelp- ingbehaviorasresponsetointerpersonalcoordinationalsocould suggestthatmirroringsupportsestimationoftheneedsofpeers.

Baimeletal.(2015)arguedthatcoordinatinginterpersonallyhelps reasoningaboutothers’mind,therebyfosteringperspectivetaking andempathicconcern.Althoughtheexactsocialconsequencesof peercoordinationareunclear,theselinesofreasoningsuggestthat interindividualdifferencesinneuralmirroringmayhaveseveral implicationsforchildren’ssocialdevelopment.

In summary,ourfindings suggestthat interindividualdiffer- encesinthedegreetowhich childrenmirrorothers’actions(as indexedbyrelativebeta-powerdecrease)arecloselyrelatedtohow welltheycoordinatetheirownactionsduringcooperationwith peers.Toourknowledge,thesefindingsprovidethefirstevidence thatinterindividualdifferencesinmotoractivationduringaction observationarerelatedtointerpersonalcoordinationoutsidethe specificmirroringtaskandthussuccessfulsocialinteraction.

Conﬂictofinterest None.

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