Infancy. 2021;00:1–18. | 1wileyonlinelibrary.com/journal/infa

Received:20January2020 | Accepted:29August2021

DOI:10.1111/infa.12438

R E S E A R C H A R T I C L E

Exploring developmental changes in infant anticipation and perceptual processing: EEG responses to tactile stimulation

Guannan Shen1 | Staci M. Weiss1 | Andrew N. Meltzoff2 | Olivia N. Allison3 | Peter J. Marshall1

©2021InternationalCongressofInfantStudies(ICIS)

GuannanShenandStaciM.Weissarecontributedequallytothismanuscript.

1DepartmentofPsychology,TempleUniversity,Philadelphia,Pennsylvania,USA2InstituteforLearningandBrainScience,UniversityofWashington,Seattle,Washington,USA3DepartmentofRadiology,Children'sHospitalofPhiladephia,Philadephia,USA

CorrespondenceGuannanShen,DepartmentofRadiology,Children’sHospitalofPhiladelphia,Philadelphia,PA19104,USA.Email:sheng1@chop.edu

Funding informationOverdeckFamilyFoundation;BezosFamilyFoundation

AbstractThereisanincreasinginterestinalpha-rangerhythmsin theelectroencephalogram(EEG) in relation toper-ceptual and attentional processes. The infant murhythmhasbeenextensively studied in thecontextoflinkages between action observation and action pro-duction in infancy, but less is known about the murhythm in relation to cross-modal processes involvingsomatosensation.Weinvestigateddifferencesinmure-sponsestocuedvibrotactilestimulationofthehandintwoagegroupsofinfants:From6to7 monthsand13to14 months.Wewerealso interested inanticipatoryneuralresponsesinthealphafrequencyrangepriortotactilestimulation.Tactilestimulationofinfants’leftorrighthandwasprecededbyanaudiovisualcuesignal-ing which hand would be stimulated. In response tothe tactile stimulus, infants demonstrated significantmudesynchronizationoverthecentralareascontralat-eral to thehandstimulated,withhighermupeak fre-quencyandgreatercontralateralmudesynchronizationforolderinfants.Priortothetactilestimulus,bothagegroupsshowedsignificantbilateralalphadesynchroni-zationoverfrontocentralsites,whichmaybeindicativeof generalized anticipation of an upcoming stimulus.

2 | SHEN et al.

1 | INTRODUCTION

Advancesindevelopmentalcognitiveneurosciencearesheddinglightondiverseaspectsofper-ceptualandcognitiveabilitiesinhumaninfants.Thearrayofavailablemethodologiesforinfancyresearchersincludestheelectroencephalogram(EEG)andmagnetoencephalogram(MEG),bothofwhichhavebeenuseful foradvancingtheunderstandingof infantcapabilities (Meltzoff&Marshall,2020).OneaspectofdevelopmentalEEGworkhasfocusedonsensorimotorneuralos-cillations,particularlythemurhythm,whichismaximalovercentralelectrodesitesinthealphafrequencyrange(Marshalletal.,2002).

Studiesoftheinfantmurhythmhaveoftenbeencarriedoutinthecontextoflinkagesbetweentheactionobservationandexecution(Cuevasetal.,2014;Marshall&Meltzoff,2011;Southgateetal.,2009),includingactionimitation(forreviewsseeMarshall&Meltzoff,2014;Meltzoff&Marshall,2018),andtheperceptionofbodilycorrespondencesbetweenselfandotherininfancy(Sabyetal.,2013).Theemphasisintheinfantmuliteratureontheconnectionsbetweenactionobservationandexecutionisconsistentwiththenotionofthemurhythmasbeingtiedtosenso-rimotorexperience(Cannonetal.,2016;Cuevasetal.,2014).

Giventhatthemurhythmappearstohaveoriginsinthesomatosensorycortex(Ritteretal.,2009),thereisalsointerestintheconnectionsbetweenthemurhythm,somatosensation,andthedevelopmentofmapsofthebodyintheinfant'sbrain(Marshall&Meltzoff,2015;Meltzoff&Marshall,2018).Here,webuildonthislineofworkbyexamininginfantmurhythmresponseselicitedtotactilestimulationofthehand,withanadditionalnovelfocusonpotentialanticipa-toryresponsesofthemurhythmtoupcomingstimulation.Wewereparticularlyinterestedinexploringwhetherinfantscanuseaninformativeaudiovisualcuetopredictthetemporalandspatialpropertiesofupcomingtactilestimulation.

1.1 | Neural correlates of somatosensory processing

Inadults,tactilestimulationofthehandelicitsadesynchronization(decreaseinpower)ofthemurhythmintheEEGoverthecontralateralcentralregion(Anderson&Ding,2011;Haegensetal.,2012;Shenetal.,2017).ContralateralmudesynchronizationtotactilestimulationofthehandinadultshasalsobeenreportedusingMEG(Gaetz&Cheyne,2006;vanEdeetal.,2014).Incomparison, there isvery littleworkfocusingonthe infantoscillatoryresponses followingsomatosensorystimulation,withdevelopmentalstudiesinsteadoffocusingonevent-relatedpo-tentials(ERPs)elicitedtotactilestimulation.Thesestudieshaveshownthatstimulationofthehands,feet,lips,orfaceofinfantselicitsspatialpatternsofERPresponsesacrossthescalpthatareconsistentwiththehomuncularorganizationofthesomatosensorycortex(Meltzoffetal.,2018,2019;Sabyetal.,2015;Shenetal.,2018).

AstudyofEEGmurhythmresponsestotactilestimulationininfancyby(Drewetal.,2018)reportedthattactilestimulationoftherighthandof6-month-oldselicitedadesynchronizationofthemurhythmovertheleft(contralateral)centralregion,whilestimulationoftherightfoot

The findings highlight the potential of examining thesensorimotormurhythminthecontextofinfantatten-tionaldevelopment.

| 3SHEN et al.

wasassociatedwithamuresponseoverthemidlineatthecentralregion.Murhythmdesynchro-nizationatcentralmidlineelectrodestofootstimulationwasalsoevidentinarecentstudyof10-montholds(Piccardietal.,2021).

Here,weexamineinfantmuresponsestotactilestimulationoftheleftandrighthandacrosstwoagegroups(from6-to7-montholdsand13-to14-montholds).Wewerealsointerestedinwhetherexternalcuescanenabletheinfanttoregisterattentiontoaparticularbodilylocationpriortothedeliveryofthetactilestimulus.Tactilestimulationwasappliedseparatelytotheleftandrighthands,enablinganinvestigationofspatiallyandtemporallydistinctneuralmodulationforvisuotactilemapping,bytracingmurhythmresponsestoinfanthandstimulation(deliveredinperipersonalspace)followingareliable,spatiallyinformativevisualcue(deliveredinextrap-ersonalspace).

1.2 | Neural correlates of anticipation

Aswellastestingtheinfantmurhythmresponsetostimulationoftheleftandrighthands,afurtheraimofthecurrentstudywastoemployEEGmethodstoexploreneuralaspectsofantici-pationininfancy.Specifically,wetestedforanticipatoryalpha-rangeEEGresponses(includingapossibleanticipatorymurhythmresponse)followingaudio-visualcuesthatweredesignedtosignalanimpendingvibrotactilestimulusthatwasdeliveredtoinfants’leftorrighthands.

Prior work has suggested that attentional control in the first year of life shifts from moreexogenous,reactiveprocesses toreflect increasinglyendogenous,proactiveprocessesofselec-tiveattention(Colombo,2002;Johnson,1990;Posneretal.,2012).Studiesofanticipationinthevisualmodalityhaveusedmeasuressuchaslookduration(Reynoldsetal.,2013),visualfixation(Kannass&Oakes,2008),aswellaspsychophysiologicalresponses(Richards&Casey,1991;Xieetal.,2018).There isalsoevidencethat infantsdeployanticipatoryattentionbymovingtheirbodiesandorientingtheireyes,head,andhandsinexpectationofchangesintheirenvironment(Amso&Johnson,2006;Reddyetal.,2013;Yu&Smith,2016).Fromanindividualdifferencesperspective,behavioralmeasuresofanticipationhavebeenassociatedwithself-regulationandattentionalorientingabilitiesbetween6and8 monthsofage(Gomesetal.,2000;Rothbartetal.,2011).Xieetal.(2018)reportedashiftininfantvisualattentionthatwasapparentbetween10and12 monthsofage(andnotinyoungerinfants),whereintheshiftfromexogenous,cue-elicitedorientingtoendogenous,sustainedattentionisaccompaniedbyattenuationofalpha-rangeEEGresponses.Thereisalsoevidencefromanticipatoryeyemovementsthatsuggestsasimilartransi-tioninanticipatoryalpharesponsesmightbeevidentby13–14 monthsofage(Martinez-Alvarezetal.,2017).

Muchoftheworkonanticipatoryaspectsofinfantattentionhasbeencarriedoutsolelywithinthevisualmodality.Infantbehavioralresponsestostimulipresentedsimultaneouslyacrossdif-ferentmodalitiesremainatopicofcurrentinterest(BegumAlietal.,2021;Thomasetal.,2018),althoughthereislessworkusingtemporallyseparatedcrossmodalstimuluspairings.Ofpartic-ular relevance to thecurrent studyare thedevelopmentalneuroscience findings showing theevidence of anticipatory infant brain responses between temporally separated auditory/visualcuesandtargetstimuli(Kouideretal.,2015;Mento&Valenza,2016).

Studiesinadultsandolderchildrenhaveshownthatwhentactilestimulationofaspecificbodilylocation(typicallyoneofthehands)isprecededbyaspatiallyinformativevisualorau-ditorycue,thereisananticipatorydesynchronizationofthemurhythmovercentralelectrodesitescontralateraltotheexpectedsiteofstimulation.Inadults,theextentofthislateralization

4 | SHEN et al.

ismodulatedbythesideoftactilestimulationbothintermsofthelocationonthebodyandthelocationinspace(Schubertetal.,2019).Inastudyofchildrenagedbetween6and8 years,Weissetal. (2018) reportedacontralateralanticipatorydesynchronizationof themurhythm in theepochleadinguptotactilestimulationoftheleftorrighthand,followingaspatiallyinformativevisualcue.Notably,themagnitudeoftheanticipatorymudesynchronizationwasassociatedwithchildren'sscoresonanexecutivefunctionbattery(Weissetal.,2018).Thepreverbaloriginsanddevelopmentofthisanticipatorymurhythmresponsehaveyettobeaddressed.Inadults,theextentofanticipatorymuattenuationiscorrelatedwithpropertiesofthebehavioralresponsetothesubsequenttactilestimulus(Anderson&Ding,2011;Jonesetal.,2010;Linkenkaer-Hansen,2004;Schubertetal.,2009),andisassociatedwiththeamplitudeofearlycomponentsoftheERPresponsetothetactilestimulus(Zhang&Ding,2010).

Findingsinadultsandchildrenofanticipatorydesynchronizationofthemurhythmaheadofcuedtactilestimulationareconsistentwithbroaderworksuggestingaroleforalpha-rangeoscillationsinattentionalcontrol(Gomez-Ramirezetal.,2016).Inthesomatosensorymodality,researchinthisareahasfocusedonthemurhythmoverthecentralscalpregion,whileinthevisualmodality,thealpharhythmoverposteriorsites(the“visualalpharhythm”)hasbeenofparticularinterest.Studiesofanticipatorychangesintheamplitudeofthevisualalpharhythmtypicallyinvolveaspatiallyinformativecentralcueprecedingatargetvisualstimulusthatap-pearsontheleftorrightsideofamonitorscreen.Modulationsofvisualalphaamplitudehavebeenconsistentlyreported in the interval leadingupto the targetstimulus.Morespecifically,desynchronizationofthevisualalpharhythmattheoccipitalelectrodecontralateraltotheex-pectedfieldofpresentation(left/right)occursalongsideanipsilateralincreaseinalphapower(Klimesch,2012;Sadaghiani&Kleinschmidt,2016;Wordenetal.,2000).

Theanticipatoryalphaattenuationseenovercontralateralelectrodesforthesensorimotormurhythm(inadultsandchildren)andthevisualalpharhythm(inadults)mayreflectthereleaseof task-relevantsensorycorticalareas frominhibition(Gomez-Ramirezetal.,2016;Klimeschetal.,2007).Thisreleasefacilitatesasubsequentincreaseinlocalcortexexcitability,whichinturnincreasestheperceptualsalienceofincomingtactilestimuli(Foxe&Snyder,2011;Zhang&Ding,2010).Anticipatorymodulationofalpha-rangerhythms(e.g.,sensorimotormu/visualalpha) over different scalp regions (central/occipital) has been suggested to reflect modality-specificattentionalprocessesthatsharethiscommonmechanism(Freyetal.,2015;Schroeder&Lakatos,2009).Althoughworkinchildrentoinvestigateanticipatorymodulationofalpha-rangeoscillationsisstillverysparse,wesuggestthatrelatedstudiesarepossibleinstillyoungerpopu-lations,ininfants.Suchworkhasthepotentialtoexpandourunderstandingoftheontogenesisofselectiveattentionanditsneurobehavioralcorrelates.

1.3 | Rationale and plan for the current infant study

ThecurrentstudyaimedtoadvancetheunderstandingofEEGresponsespriortoandfollowingtactilestimulationoftheinfant'shand,withafocusonsomatosensorymurhythmacrosstwoagegroups(6–7 monthsand13–14 months).Theagerangefrom6to14 monthsofageisaperiodofdistinctgrowthintheamplitudeoftheinfantmurhythm(Marshalletal.,2002),butlittleisknownaboutthechangesinthetemporalandspatialpropertiesofthemuresponsetotactilestimulation(anditsmagnitude)overthistime.Further,asnotedabove,thisagerangeisalsoofbroaderinterestintermsofthedevelopmentofperceptualandattentionalabilities,bothintermsofanticipatoryattentionandthecapacitytorelatestimuliacrossdifferentmodalities.

| 5SHEN et al.

Weemployedanage-appropriatesomatosensoryselectiveattentionparadigminwhichEEGwascollectedduringaseriesoftrialsinvolvingaspatiallyinformativeaudiovisualcuepresentedinextrapersonalspace,priortothedeliveryofvibrotactilestimulationtotheinfants’leftorrighthand.Theterm“cue”isusedheretodenotetheonsetofspatiallyinformativevisualandaudi-toryinformationthatwastemporallyassociatedwiththesubsequenttactilestimulation.Giventheagerangeoftheparticipants,nobehavioralresponsetothetactilestimuluswasrequiredormeasured.

Analysesaddressedthethreeinterrelatedaims:(i)toexaminethedevelopmentofthesomato-sensorymurhythmusinganindividualdifferencesapproachtomupeakidentification,(ii)toassesswhethertheinfantmurhythmresponsetotactilestimulationoftherightandlefthandreflectslateralizedmodulation,asisevidentinadults,(iii)totestforanticipatoryEEGresponsesduring a cue–target paradigm across modalities (audiovisual cue and tactile target). Plannedcomparisonstesteddifferencesinalpha-rangeresponsesoverdifferentscalpregionsacrossthetwoagegroupsandacrossthehandstimulated(left/right).WewereparticularlyinterestedinthepossibleanticipatorymodulationoftheEEGsignalduringtheintervalbetweentheaudiovisualcueandthedeliveryofthetactilestimulus.

2 | METHOD

2.1 | Participants

This study was carried out with approval from the institutional review board at TempleUniversity,withinformedconsentobtainedfromtheparentofeachinfantbeforeparticipa-tion. Forty-three infants across two age groups were recruited to participate in this cross-sectionalstudy.Eleveninfantswereexcludedfromfurtheranalysesduetohardwarefailure(n  =  1), technical problems with EEG signal acquisition (n  =  3), or excessive movement(younger = 3;older = 4)thatprecludedtherecordingofaminimumnumber(20)ofartifact-free trials for each condition (left-hand stimulated/right-hand stimulated). The EEG datafrom32infantsagedfrom6to7 months(n = 17)and13–14 months(n = 15)metthecriteriafor furtheranalysis.Theyoungeragegroupcomprisedof infants from6 months0 days to7 months31 days(M = 222 days,SD = 13,7 male,10female).Infantsintheolderagegrouprangedfrom13 months0 daysto14 months31 days(M = 419 days,SD = 17,7 male,8fe-male). From this point, we refer to these groups as “younger infants” and “older infants,”respectively.Allparticipatinginfantswerereportedbyparentsasbeingtypicallydeveloping,andallwerebornwithin15 daysoftheirduedate.Infantswithtwoleft-handedparentswereprecludedfromstudyparticipation.

2.2 | Experimental procedure

Infantsinitiallyvieweda2-minutevideotofamiliarizethemwiththeElmoandCookieMonstercharactersthatwerepartofthespatialcues.FollowingtheEEGcapplacement,electrodeprepa-ration, and placement of the vibrotactile stimulators and mittens (see below), the infant wasseatedonthelapoftheircaregiver,facinganLCDmonitor.Theparentswereseatedinachairpositioned60 cmawayfromthedisplay(24in/60 cmviewable).Thehandsoftheinfantswerenotrestrained.

6 | SHEN et al.

Atthebeginningofeachtrial,afixationimageofaninfant'sfacewasdisplayedinthecenterofthemonitorscreen.After1000 ms,thefixationimagewasreplacedbyavisualcueconsistingofanimageofaSesameStreetcharacter(ElmoorCookieMonster)thatwaspresentedeitherontheleftortherightsideofthescreen.Thelocationofthecueonthescreen(leftorright)wascongruentwiththehandtowhichavibrotactilestimuluswaspresented2000 msaftercueonset(leftorrighthand).Thevisualcuewasdisplayedfor3000 ms.Theassociationofcuecharacter(Elmo/CookieMonster)andvisualcuelateralization(left/right)wasconsistentwithineachpar-ticipantandwascounterbalancedacrossparticipants.Simultaneouswiththeonsetofthevisualcue,anaudioclipofthespecificsoundmadebyElmoorCookieMonster(700 msduration)waspresentedviaaloudspeakerplacedbehindthemonitor.AschematicshowingthestructureofasingletrialisshowninFigure1.

To further increase the salience of the correspondence between the cues and the hand towhichthevibrotactilestimuluswaspresented, infants’handswerefittedwithpuppetmittensoftheSesameStreetcharacterssuchthateachmittenwasonthesamehand(left/right)asthesideofthematchingvisualcue.Themultimodalcombinationofcueswasdesignedtopromotelearningoftheassociationsbetweenthecuesandthehand(left/right)towhichvibrotactilestim-ulationwaspresented.

Thefullprotocollastedabout22 min,withinfantsreceivingtactilestimulationtotheright(n = 100)orleft(n = 100)handinarandomizedorderacross200trials.Inpreliminaryanalyses,wefoundnodifferencesinEEGresponsestothevariouscombinationsofaudiovisualcuestimulithatwereemployed.

StimuluspresentationwascontrolledbySTIMsoftwarefromJamesLongCompany.Vibrotactilestimuliweredeliveredusingcustomdevicesplacedoninfants’leftandrightpalms.Eachdeviceconsistedofaplasticdisc(seeFigure2)containinga10-mmdiscmotor(10,000 rpm/166 Hz),withacableconnectingthedevicetoacontrolbox.Thediscswereattachedtotheinfant'spalmwithmedicaltape,withthecableorientedtowardthearm(Figure2).Themotorpatterngenerat-ingthevibrotactilestimulushada45-msrisetime,940 msofpeakmovement,anda15-msbraketime,foratotalof1000 msofstimulation.Thevibrotactilestimulusdidnotproduceasoundthatwasaudibletotheinfant.

F I G U R E 1 Trialstructure:Apictureofaninfant'sface(servingasfixation)wasfirstdisplayedcentrallyfor1000 ms.Theonsetofthedirectionalvisualcue(SesameStreetcharacterdisplayedcontinuouslyfor3000 ms)wassimultaneouswiththeonsetofa700 msauditorystimulusconsistingof“Elmo”or“Cookie”viaopenfieldspeakers.Thedeliveryofthevibrotactilestimulustotheleftorrighthandoccurred2000 msfollowingthecueonset.Thevibrotactilestimuluswasdeliveredcontinuouslyfor1000 ms

| 7SHEN et al.

2.3 | EEG acquisition and analysis

EEGsignalswereacquiredfrom32electrodessecuredinastretchcap(ANTNeuro)andplacedaccordingtotheInternational10–20format.Asapartofcappreparation,eachelectrodewasfilledwithasmallamountofconductivegel.TheEEGsignalswerecollectedreferencedtoCzwithanAFzgroundandwerere-referencedofflinetotheaverageoftheleftandrightmastoidspriortoanalysis.Scalpimpedanceswerekeptunder25 kΩ.AllEEGsignalswereamplifiedbyoptically isolated,highinputimpedance(>1 GΩ)bioamplifiersfromSAInstrumentationandweredigitizedusinga16-bitA/Dconverter(±2.5 Vinputrange)atasamplingrateof512 Hzusing Snap-Master data acquisition software (HEM Data Corp.). Bioamplifier gain was 4000andhardwarefiltersettingswere0.1 Hz(high-pass)and100 Hz(low-pass)witha12 dB/octaveroll-off.

ProcessingandinitialanalysisoftheEEGsignalswereperformedusingtheEEGLAB13.5.4btoolbox(Delorme&Makeig,2004)implementedinMATLAB.Epochsof5000 msdurationwereextracted from thecontinuousEEGdata,witheachepochextending from−3000 to2000 msrelativetovibrotactilestimulusonset.Theexperimentalsessionwasrecordedonthevideoforthepurposeofcodinginfantmovement.Duringrecording,averticalintervaltimecode(VITC)

F I G U R E 2 Top:Renderingofthevibrotactiledevice.Bottom:Placementofthedeviceonthehandofaninfantparticipant,aftersecuringwithmedicaltapeandabandage

8 | SHEN et al.

wasplacedonthevideosignalthatwasalignedwithEEGcollectionatthelevelofoneNTSCvideo frame.Videos were coded offline and trials were rejected if they contained upper limbmovementsfortheentire5000 msanalysisepoch.Furthertrialswerediscardediftheyincludedorientingof thehead to thecueor stimulus in the2000 mswindowprior to tactile stimuluspresentation.Aftervideocoding,olderinfantshadameanof52 validtrialspercondition(left-handstimulationorright-handstimulation),andyounger infantshadameanof63trialspercondition,duetomoremovementinolderinfantsthanyoungerinfants.VisualinspectionoftheEEGsignalwasusedtorejectepochscontainingsignificantmuscleartifacts.Themeannumberof artifact-free trials per condition (left-hand stimulation or right-hand stimulation) was 33.5forolderinfants(left:M = 32,SD = 14;right:M = 35,SD = 13)and33foryoungerinfants(left:M = 33.5,SD = 14;right:M = 32.9,SD = 15).Aone-wayANOVAshowednosignificantdiffer-enceinthenumberofusabletrialsbetweenconditions(p = .572).Therewasalsonodifferenceinusabletrialnumbersbetweenthetwoagegroups(p = .965).

2.4 | Identification of age- specific mu rhythm peak frequency

Priorworkhasshownthatthemeanpeakfrequencyoftheinfantmurhythmincreasesfromaround6 Hzat6 monthsofage,tojustabove7 Hzby12 months(Berchiccietal.,2011;Marshalletal.,2002).Toassistwiththeselectionofage-specificmufrequencybands,oscillatoryactivityinthe4–12 Hzrangewascomparedbetweentwoepochs:Duringthepresentationofthefixationstimulus(baseline:−3000to−2000 ms)andanepochfollowingvibrotactilestimulation(post-stimulus:200to1200 ms).Tocapturethemaximummuattenuationevokedbytactilestimuli,analysesfocusedonthemuresponsetotheright-handstimulationconditionattheleftcentralelectrode (C3). Time-frequency analysis was performed using Morlet wavelet decomposition,with100overlappingwindowsstartingwitha0.8-cyclewaveletatthelowerfrequency.Powerspectrafromthetwoepochswerecomparedtoquantifythemurhythmpeakfrequencyforeachparticipant,whichwasidentifiedasthefrequencyshowingthemaximumpowerdifferencebe-tweenthetwoepochs.ThepeakfrequencywasfirstidentifiedusingaroutineinR(version3.5.3)andwasthenconfirmedwithavisualinspectionofindividualpowerspectrumplots.

2.5 | Mu rhythm responses in relation to vibrotactile stimulation

Basedonpriorstudiesofadultsandchildrenexaminingoscillatorymurhythmresponsesduringanticipationoftactilestimulation(Shenetal.,2017;Weissetal.,2018),analysesfocusedonthefrontocentralandcentralscalpregions(i.e.,electrodesFC5/FC6andC3/C4).InitialexaminationofERSPresponsesshowedthemtobemainlyoverfrontalandcentralsites(Figure6),furtherguidingthisfocus.AlthoughsomeinfantEEGstudiescombineresultsfromthefrontalandcen-tralsites,wekeptthemseparatesincewewereinterestedinpossibledifferentialeffectsacrosstheseregions.Further,thelow-densityelectrodearrayinthecurrentstudyprecludedaveragingacrosselectrodeclusters.BasedonpriorinfantEEGworkandtheresultsoftheindividualizedmupeakfrequencyanalysis(above),themufrequencyrangesusedwere5–8 Hzfortheyoungeragegroupand6–9 Hzfortheolderagegroup(Marshalletal.,2002).

Tocharacterizechanges inEEGoscillationsprior toand following thepresentationof thevibrotactilestimulus,time-frequencydecompositionsofsingle-trialdatawereconductedusingevent-relatedspectralperturbation(ERSP)analysis(Makeig,1993).ERSPwascomputedusinga

| 9SHEN et al.

Morletwaveletdecompositionoverafrequencyrangeof5–30 Hz,with100overlappingwindowsstarting with a 0.8-cycle wavelet at the lowest frequency.The baseline for the ERSP analyseswasdefinedasa900-mswindowpriortocuepresentation,duringthepresentationofthefixa-tionstimulus(−3000to−2100 ms).Thepre-stimulusanalysiswindowwasdefinedas−1300to−300 msandthepost-stimuluswindowwas200–1200 ms.

Trial-by-trialERSPvaluesatelectrodesFC5,FC6,C3,andC4wereaveraged foreachpar-ticipant.Repeated-measuresANOVAswereconductedseparatelyforpre-stimuluswindowandpost-stimuluswindow,withfactorsagegroup(younger,older),region(frontocentral,central),hand(left,right),andhemisphere(left:FC5,C3;right:FC6,C4).

3 | RESULTS

3.1 | Age- related change in peak mu rhythm frequency

ApeakatelectrodeC3inthe4–12 Hzrangewaspresentin13of17youngerinfantsand12of14olderinfants.Aone-wayANOVAonthepeakmufrequencywithfactoragegroupshowedamaineffectofagegroup,F(1,23) = 5.3019,p = .03,η2 = .188,withsignificantlylowerpeakfrequencyforyoungerinfants(mean = 6.56 Hz,SD = 1.38)thanolderinfants(mean = 7.73 Hz,SD = 1.13).Theseresultsareinlinewiththepriorfindingsofagradualincreaseinmodalmupeakfrequencyfrom6to7 Hzduringthefirstyearoflife(Berchiccietal.,2011;Marshalletal.,2002).

3.2 | Post- stimulus mu rhythm modulation

Time-frequencyplotsandtopographicmaps(Figures3–6)indicatethatthevibrotactilestimuluselicitedmurhythmdesynchronizationatcentralsitescontralateraltothevibrotactilestimula-tion.Thiseffectwasobservedinallindividualparticipants.

Arepeated-measuresANOVA(2 × 2 × 2 × 2;ageGroup × hand × hemisphere × region)onpost-stimulusERSP(300–1300 mswindow)showednosignificantmaineffectofagegroup,F(1,30) = 1.55,p = .223,hand,F(1,30) = 0.09,p = .757,hemisphere,F(1,30) = 0.193,p = .663,orre-gion,F(1,30) = 0.03,p = .863.Therewasasignificantinteractionbetweenhandandhemisphere,F(1,30) = 48.99,p < .001,η2 = .156.Posthoctestsshowedthatpost-stimulusmudesynchroni-zation was greater for contralateral sites than ipsilateral sites (for left-hand stimulation, righthemisphere((mean = −1.21 dB,SD = 1.26) < lefthemisphere(mean = −0.26 dB,SD = 1.11),F = 25.537,p < .001,η2 = .149;forright-handstimulation,lefthemisphere(mean = −1.22 dB,SD = 1.5) < righthemisphere(mean = −0.17 dB,SD=0.96),F=34.559,p<.001.η2=.163).

TheANOVAalsoshowedasignificantthree-wayinteractionbetweentheagegroup(6–7vs.13–14 montholds),hand(leftvs.right),andhemisphere(leftvs.right),F(1,30)=8.676,p=.006,η2= .031.Posthocanalyseswereconductedusingpair-wise t-tests.Forleft-handstimulation,olderinfantsshowedgreaterdesynchronizationintherighthemisphere(M = −1.486,SD = 0.596)comparedwithyoungerinfants(M = −1.067,SD = 1.346,t = 2.17,p = .034).Therewasnosig-nificantdifferencebetweenagegroupsinipsilateral(left)ERSP(olderM = 0.254,SD = 1.136,p =  .361;youngerM = −0.303,SD = 1.040, t = 0.922,p =  .361).Similarly, fortheright-handstimulation,olderinfantsexhibitedgreatercontralateral(left)desynchronization(M = −1.955,SD = 1.225)thanyoungerinfants(M = −1.132,SD = 1.725;t = 2.482,p = .016)andtherewereno

10 | SHEN et al.

differencesinipsilateral(right)ERSPbetweenolderinfants(M = 0.017,SD = 0.655)andyoungerinfants(M = −0.162,SD = 1.152;t = 0.512,p = .608).

3.3 | Stimulus anticipation: pre- stimulus alpha rhythm modulation

Figure3 showstopographicplotsforalphaERSPacrossthepre-stimulusandpost-stimulustimewindows.Figure6 showstime-frequencyplotsofsignificantERSPchangesrelativetobaseline,withFDRcorrection,followingthecueandfollowingtactilestimulationoftherighthand.Asshowninthesefigures,alphadesynchronizationwasapparent inthetimeperiodpriortotheonsetofthetactilestimulus:Startingfromaround−1300 ms,analpha-rangedesynchronizationwaspresentthatappearstobestrongestoverfrontocentralsites.Thispre-stimulusalphadesyn-chronizationwasobservedin14ofthe17youngerinfantsand13ofthe14olderinfants.

Fortherepeated-measuresANOVAcomparingpre-stimulusERSPacrossagegroupsandcon-ditions,therewasasignificantmaineffectofregion,F(1,30) = 30.729,p < .001,η2 = .07,withgreaterdesynchronizationatfrontocentralelectrodes(M=−1.02 dB,SD=1.14)thanatcentralelectrodes(M=−0.44 dB,SD=0.98).Therewasnosignificantmaineffectofagegroup,F(1,30) = 0.048,p = .8277,hand,F(1,30) = 1.441,p = .239,hemisphere,F(1,30) = 0.195,p=.662,andtherewerenosignificantinteractionsbetweenanyofthefactors.

To confirm that there was a significant desynchronization from the baseline epoch to thetimewindowpriortotheonsetofthetactilestimulus,meanpowerinthealphafrequencyrange

F I G U R E 3 Topographicmapsofalpha(5–8 Hzforyoungerinfants,6–9 Hzforolderinfants)ERSPin400 msintervals.Thetoppanels(a)displayalphaERSPintheepochpriortothetactilestimulus,whichwasdeliveredatt = 0 ms.Theaudiovisualcuewasdeliveredat−2000 ms.Thelowerpanels(b)showalphaERSPevokedbytactilestimulationoftheleftorrighthand

| 11SHEN et al.

(5–8 Hzfortheyoungerinfants,6–9 Hzfortheolderinfants)atfrontocentralandcentralsiteswascomparedusingarepeated-measuresANOVAwithafactoroftimewindow(baseline:−2500to−2100 ms;pre-stimuluswindow:−1300to−300 ms).Thisanalysisrevealedasignificantmaineffectoftimewindow,F(1,30)=22.489,p<.0001,η2=.209,withlowerpowerintheprestimu-luswindow(mean=−0.73 dB,SD=1.1)thaninthebaselineepoch(M=−0.13 dB,SD=0.32).

4 | DISCUSSION

Theresultsofthecurrentstudyextendpriorfindingsonthedevelopmentofalpha-rangerhythmsininfancy,andfurtherinformtheunderstandingofinfantEEGresponsestotactilestimulation.Thisstudyalsoexploredtheneuralconcomitantsofinfantanticipation,applyingadevelopmen-talcognitiveneuroscienceapproachtoaddressquestionsfirstraisedinstudiesaboutbehavioralanticipation.

Analysesexaminedalpha-bandactivityintheEEGsignalprecedingandfollowingcuedvi-brotactilestimulationoftheleft-orright-handininfants.Infantsintwoagegroups(from6to7 monthsand13to14 months)wererecruitedtoexaminethedevelopmentalchangesinEEGoscillationsaround tactile stimulation.Consistentwith thepriorwork (Berchicci et al., 2011;Marshalletal.,2002;Thorpeetal.,2016),themeanpeakfrequencyofthecentralsomatosensorymurhythmininfantsincreasedfromaround6.5 Hzininfantsagedbetween6and7 monthsoldto7.7 Hzat13–14 monthsofage.

F I G U R E 4 ERSPwaveformsforthealphabandatFC5/FC6(upperpanel)andC3/C4(lowerpanel)foryoungerinfants(lefttwocolumns)andolderinfants(righttwocolumns).Theshadowsaroundthelinerepresentstanderrorswithineachgroup.Thealphafrequencyrangeusedwas6–9 Hzforolderinfantsand5–8 Hzforyoungerinfants.Theaudiovisualcuewaspresentedat−2000 ms(thefirstverticalline).Time0 mscorrespondstotactilestimulusonset(thesecondverticalline)

12 | SHEN et al.

Thestudyof the infantmuresponse to tactilestimulationof thehandwasrestricted tostimulationoftherighthand(Drewetal.,2018),whereasthecurrentstudyemployedstim-ulation of left and right hands. Contralateral desynchronization to tactile stimulation wasobservedforstimulationofinfants’leftandrighthands,whichaddsadevelopmentalperspec-tivetoworkdonewithadults(Haegensetal.,2012;VanEdeetal.,2014).Althoughthiseffectwas significant at both ages, older infants showed greater contralateral desynchronizationthanyoungerinfantsinresponsetothetactilestimulus,comparedtoyoungerinfants.Thisdesynchronization to the tactile stimulus did not significantly differ between frontocentraland central sites. This observation is consistent with the fact that frontocentral electrodeshave sometimes been included with central sites in electrode clusters used to index infantmu(Bacheetal.,2017;Stapeletal.,2010).Thelargerdesynchronizationinolderinfantsalsoaligns with the findings of a larger magnitude of mu desynchronization noted during theactionproductioninolderinfants(Cuevasetal.,2014).Thisfindingcanalsobeconsideredinthelightofstudiesshowingthattheinfantbehavioralreactionstotactilestimulationofdifferentbodypartsbecomemoreefficientoverthefirstyearoflife(Leedetal.,2019;Somogyietal.,2018).

Thefindingsfromthecurrentstudycanbeplacedwithinthegrowingliteratureonbodyrep-resentationsininfancy.Withinthefirstmonthsoflife,thesomatotopicorganizationofthebasicinfantbodymapappearsconsistentwiththatofolderchildrenandadults(Dall'Orsoetal.,2018;Meltzoffetal.,2018,2019;Sabyetal.,2015;Shenetal.,2018,2020).Workwitholderinfantshasrevealedanadult-likesomatotopicpatternofmurhythmresponses,observedseparatelyduringtheactionobservationandactionexecution(Marshalletal.,2013;Mülleretal.,2017;Sabyetal.,2013).Insix-month-oldinfants,asomatotopicpatternofmuresponseswasevidentfollowing

F I G U R E 5 MeanalphaERSPatcontralateralandipsilateralcentralsites(C3andC4)forthe1000 msfollowingtheonsetoftactilestimulation.***p < .001

| 13SHEN et al.

tactilestimulationoftheinfant'shandorfoot,andconcurrentobservationofanadulthandorfootdidnotmodulatetheseeffects(Drewetal.,2018).Thecurrentresultsaddtothesestudiesthroughthefindingoflateralizedresponsesfollowingthevibrotactilestimulation.

InadditiontodocumentingchangesintheinfantEEGresponsetotactilestimulation,afur-theraimofthepresentstudywastoexplorealpha-rangeoscillatoryactivitiespriortotheonsetofthevibrotactilestimulus,followingaspatiallyinformativecuethatsignaledthehand(leftorright) towhich the tactile stimulationwouldbedelivered.Significantbilateralattenuation inalpha-rangepowerwasevidentforbothagegroupsoverfrontocentralsites(FC5andFC6)intheepochprecedingthetactilestimulus.Thisnovelfindingofbilateralanticipatoryattenuationofalpha-rangeEEGoscillationssuggeststhatinfantswereabletoutilizetheaudiovisualcueintheserviceofexpectingtheupcomingstimulus.Asimilardesynchronizationwasnotapparentatcentralelectrodesites(C3andC4),unlikeanticipatoryresponsesprecedingtactilestimulationseeninstudiesofadults(Anderson&Ding,2011;Haegensetal.,2012;Jonesetal.,2010)andchildren(Weissetal.,2018).

Thefrontocentral,butnotcentral,natureofthedesynchronizationpriortothetactilestimu-lussuggeststhatthisresponsemaynotbespecifictothetactilemodality,butmaybeamoregen-eralanticipatoryresponse.RecentERPstudieshavesuggestedthatinfantscangeneratetemporalpredictionsaboutupcomingvisualevents fromaudiovisualcues (Kouideretal., 2015;Mento&Valenza,2016),withthesourceoftheseneuralresponsesassociatedwiththefronto-parietal

F I G U R E 6 Time-frequencyplotsshowingsignificantchangesinalphaERSPfollowingright-handstimulationrelativetobaselineforyoungerinfants(lefttwocolumns)andolderinfants(righttwocolumns).FDRcorrectionwasappliedtoallplots.Twoblackverticallinesintheupperleftplotindicatetheonsetoftactilestimulationattime0 msandtheaudiovisualcueat−2000 ms.Theblueintheimagesindicatessignificantdecreasesandyellow/redindicatessignificantincreasesofERSPcomparedtobaseline(p < .05).Greenareasdepictnon-significant(p > .05)ERSPchangesfrombaseline.Theelectrodearrayisalsoshown,withthelabeledelectrodescorrespondingtothesitesforwhichtime-frequencyplotsareshown

14 | SHEN et al.

attentionalnetworks(Petersen&Posner,2012).Itispossiblethatthefrontocentralmodulationofalpha-rangepowerintheepochleadinguptothevibrotactilestimulusisalsoreflectiveofactivityinthesenetworks.

AnadditionalargumentagainstthespecificityoftheinfantanticipatoryEEGresponseisthelackofalateralizedresponseleadinguptothetactilestimulation,whichwouldhavesuggestedapredictiveresponseinvolvingtheanticipatedlocationofthetactilestimulus.Thecurrentstudyusedvisualcuesconsistentwiththespatiallocationoftactilestimulation(leftvs.rightsideofthebody)aswellasconcurrentauditorycuesthatwereconsistentlyassociatedwiththesideoftactilestimulation.The lackof lateralization in thealphadesynchronizationduring theprestimulusepochmaybeafurtherindicatorofageneralanticipatoryresponsereflectingageneralassocia-tionbetweenthecueandthetargetstimulus.WefurthernotethatstudiesofanticipatoryEEGresponsesinolderchildrenandadultsalsorequireparticipantstoovertlyrespondtothetargetstimuliinsomeway,whichwasnotpossibleinthecurrentinfantstudyandmayhaveinfluencedthenatureofanticipationof,orinfantreadinessfor,thedeliveryofthetactilestimuli.Wealsonotethattheproceduredidnotincludeconditionswherethecueandprobewereincongruent,oraconditionwheretherewasnocue.FuturestudiescouldaddressthefeasibilityofincludingsuchconditionswhilemaintainingadequatetrialnumbersforEEGanalysis.

The lackofa lateralizedanticipatoryEEGresponse in thecurrent study isnot to say thatinfantscannotutilizespatiallyinformativecuestoorganizeresponsestotargetstimuli.Inwork,usingbehavioralmeasuresofinfantvisualattention,infantsasyoungas3–6 monthsmakeas-sociationsbetweenspatiallyinformativecuesandtargetstimuli,asindicatedbyfasterandmoreaccurateeyemovementstovisualtargetstimulithatareprecededbyabriefvisualcue(Atkinson&Braddick,2012;Wentworth&Haith,1992).Thereisalsosomeevidencethatinfantscanmapspatialcuesacrossmodalities(Kouideretal.,2015;Mento&Valenza,2016),althoughlittleofthisworkhasinvolvedsomatosensorystimuli.

Ourfindingofbilateralfrontocentralalphadesynchronizationinanticipationoftactilestim-ulationmayreflectanendogenous,amodalshiftofattentiontoanupcomingevent.Giventheincreasinginterestinthedevelopingrelationsbetweenthevisualandtactilemodalities(Drewetal.,2018;Filippettietal.,2015;Rigatoetal.,2014), furtherworkcanaddresshowchildrencometomapspatialcuesinextrapersonalspacetoexpectedstimulationofspecificbodyparts(Weissetal.,2018). Itwouldbe interesting to further studyhowthebilateralalpha-rangere-sponsethatweobservedatfrontocentralsitesduringtheprestimulusepochdevelopsintothefocalanticipatoryresponseatcontralateralcentralelectrodesitesthathavebeenreportedinthestudiesofolderchildrenandadults involvingtactileanticipation(Haegensetal.,2012;Weissetal.,2018).Althoughtheprocessesunderlyingsucha(potential)shifthaveyettobeelucidated,workinadultshassuggestedthatashiftfromfrontalalphadesynchronizationtodesynchroniza-tionofthecentralmurhythmmayreflectaspectsofsensorimotorlearning(Marshalletal.,2009)oractionsimulation(Colletal.,2015).Fromadevelopmentalperspective,thisshiftalsolikelyinvolveschangesfrominfancytochildhoodintheabilityofparticipantstocompletetasksthatrequireovertbehavioralresponsestothetargetstimulus,whichwouldbeexpectedtosharpenprestimulusattentionalfocus,whichinturnwouldlikelyimprovethemodalspecificityoftheanticipatoryresponse.

Inconclusion,thepresentstudyaddstoourknowledgeaboutthedevelopmentalproper-tiesofalpha-rangeEEGrhythmsininfants.Comparedwiththeyoungerinfants,olderinfantsshowedhighermupeakfrequencyandgreatercontralateraldesynchronizationinresponsetotactilestimulationofthehand.Theresultsalsosuggestananticipatoryalphaattenuationininfantsthatoccurredinadvanceoftactilestimulation.Thisalphadesynchronizationwas

| 15SHEN et al.

observedbilaterallyoverfrontocentralsites,incontrasttothecontralateralcentralresponseshowninsomatosensoryanticipationtasksinadults(Gomez-Ramirezetal.,2016)andolderchildren(Weissetal.,2018).Ourconjectureisthatthefrontalalphaattenuationwithintheanticipatoryepochmightindicatethatinfantscanuseaudiovisualcuestopredictthetimingof an impending stimulus. There was limited evidence to support the sensory and spatialspecificityofthisanticipatoryresponse.Giventhepotentialimportanceofanticipationasacomponentofselectiveattention(Weissetal.,2018),futureworkshouldcontinuetoexaminethedevelopmentofanticipatoryabilitiesoverinfancyandthebehavioralandcognitivecon-comitantsoftheseabilities.

ACKNOWLEDGEMENTSTheauthorsthankNathanSmyk,RebeccaLaconi,OliviaAllison,andMeganShaudfortheirhelpwithdatacollection.ThewritingofthisarticlewassupportedinpartbytheOverdeckFamilyFoundationandtheBezosFamilyFoundation.Theauthorsdeclarenoconflictsofinterestwithregardtothefundingsourceforthisstudy.

ORCIDGuannan Shen  https://orcid.org/0000-0002-7097-0403Andrew N. Meltzoff  https://orcid.org/0000-0001-8683-0547

REFERENCESAmso,D.,&Johnson,S.P.(2006).Learningbyselection:Visualsearchandobjectperceptioninyounginfants.

Developmental Psychology,42,1236–1245.Anderson,K.L.,&Ding,M.(2011).Attentionalmodulationofthesomatosensorymurhythm.Neuroscience,180,

165–180.Atkinson,J.,&Braddick,O.(2012).Visualattentioninthefirstyears:Typicaldevelopmentanddevelopmental

disorders.Developmental Medicine & Child Neurology,54,589–595.Bache, C., Springer, A., Noack, H., Stadler, W., Kopp, F., Lindenberger, U., & Werkle-Bergner, M. (2017).

10-month-oldinfantsaresensitivetothetimecourseofperceivedactions:Eye-trackingandEEGevidence.Frontiers in Psychology,8,1170.

BegumAli,J.,Thomas,R.L.,MullenRaymond,S.,&Bremner,A.J.(2021).Sensitivitytovisual-tactilecolocationonthebodypriortoskilledreachinginearlyinfancy.Child Development,92,21–34.

Berchicci, M., Zhang, T., Romero, L., Peters, A., Annett, R., Teuscher, U., Bertollo, M., Okada, Y., Stephen,J, & Comani, S. (2011). Development of mu rhythm in infants and preschool children. Developmental Neuroscience,33,130–143.

Cannon,E.N.,Simpson,E.A.,Fox,N.A.,Vanderwert,R.E.,Woodward,A.L.,&Ferrari,P.F.(2016).Relationsbe-tweeninfants’emergingreach-graspcompetenceandevent-relateddesynchronizationinEEG.Developmental Science,19,50–62.

Coll,M.-P.,Bird,G.,Catmur,C.,&Press,C.(2015).Cross-modalrepetitioneffectsinthemurhythmindicatetac-tilemirroringduringactionobservation.Cortex,63,121–131.

Colombo,J.(2002).Infantattentiongrowsup:Theemergenceofadevelopmentalcognitiveneuroscienceperspec-tive.Current Directions in Psychological Science,11,196–200.

Cuevas,K.,Cannon,E.N.,Yoo,K.,&Fox,N.A.(2014).TheinfantEEGmurhythm:Methodologicalconsider-ationsandbestpractices.Developmental Review,34,26–43.

Dall’Orso,S.,Steinweg,J.,Allievi,A.G.,Edwards,A.D.,Burdet,E.,&Arichi,T.(2018).Somatotopicmappingofthedevelopingsensorimotorcortexinthepretermhumanbrain.Cerebral Cortex,28,2507–2515.

Delorme,A.,&Makeig,S.(2004).EEGLAB:Anopensourcetoolboxforanalysisofsingle-trialEEGdynamicsincludingindependentcomponentanalysis.Journal of Neuroscience Methods,134,9–21.

Drew,A.R.,Meltzoff,A.N.,&Marshall,P.J.(2018).Interpersonalinfluencesonbodyrepresentationsintheinfantbrain.Frontiers in Psychology,9,2601.

16 | SHEN et al.

Filippetti,M.L.,Lloyd-Fox,S.,Longo,M.R.,Farroni,T.,&Johnson,M.H.(2015).Neuralmechanismsofbodyawarenessininfants.Cerebral Cortex,25,3779–3787.

Foxe,J.J.,&Snyder,A.C.(2011).Theroleofalpha-bandbrainoscillationsasasensorysuppressionmechanismduringselectiveattention.Frontiers in Psychology,2,154.

Frey,J.N.,Ruhnau,P.,&Weisz,N.(2015).Notsodifferentafterall:Thesameoscillatoryprocessessupportdiffer-enttypesofattention.Brain Research,1626,183–197.

Gaetz,W.,&Cheyne,D.(2006).LocalizationofsensorimotorcorticalrhythmsinducedbytactilestimulationusingspatiallyfilteredMEG.NeuroImage,30,899–908.

Gomes,H.,Molholm,S.,Christodoulou,C.,Ritter,W.,&Cowan,N.(2000).Thedevelopmentofauditoryattentioninchildren.Frontiers in Bioscience,5,D108–D120.

Gomez-Ramirez,M.,Hysaj,K.,&Niebur,E.(2016).Neuralmechanismsofselectiveattentioninthesomatosen-sorysystem.Journal of Neurophysiology,116,1218–1231.

Haegens,S.,Luther,L.,&Jensen,O.(2012).Somatosensoryanticipatoryalphaactivityincreasestosuppressdis-tractinginput.Journal of Cognitive Neuroscience,24,677–685.

Johnson,M.H.(1990).Corticalmaturationandthedevelopmentofvisualattentioninearlyinfancy.Journal of Cognitive Neuroscience,2,81–95.

Jones,S.R.,Kerr,C.E.,Wan,Q.,Pritchett,D.L.,Hämäläinen,M.,&Moore,C.I.(2010).Cuedspatialattentiondrivesfunctionallyrelevantmodulationofthemurhythminprimarysomatosensorycortex.The Journal of Neuroscience,30,13760–13765.

Kannass,K.N.,&Oakes,L.M.(2008).Thedevelopmentofattentionanditsrelationstolanguageininfancyandtoddlerhood.Journal of Cognition and Development,9,222–246.

Klimesch,W.(2012).Alpha-bandoscillations,attention,andcontrolledaccesstostoredinformation.Trends in Cognitive Sciences,16,606–617.

Klimesch,W., Sauseng, P., & Hanslmayr, S. (2007). EEG alpha oscillations:The inhibition–timing hypothesis.Brain Research Reviews,53,63–88.

Kouider,S.,Long,B.,LeStanc,L.,Charron,S.,Fievet,A.C.,Barbosa,L.S.,&Gelskov,S.V.(2015).Neuraldynam-icsofpredictionandsurpriseininfants.Nature Communications,6,8537.

Leed,J.E.,Chinn,L.K.,&Lockman,J.J.(2019).Reachingtotheself:Thedevelopmentofinfants’abilitytolocal-izetargetsonthebody.Psychological Science,30,1063–1073.

Linkenkaer-Hansen,K.,Nikulin,V.,Palva,S.,IlmoniemiR.,J.,&PalvaJ.,M.(2004).Prestimulusoscillationsen-hancepsychophysicalperformanceinhumans.The Journal of Neuroscience,24,10186–10190.

Makeig, S. (1993). Auditory event-related dynamics of the EEG spectrum and effects of exposure to tones.Electroencephalography and Clinical Neurophysiology,86,283–293.

Marshall,P.J.,Bar-Haim,Y.,&Fox,N.A.(2002).DevelopmentoftheEEGfrom5monthsto4yearsofage.Clinical Neurophysiology,113,1199–1208.

Marshall,P.J.,Bouquet,C.A.,Shipley,T.F.,&Young,T.(2009).EffectsofbriefimitativeexperienceonEEGde-synchronizationduringactionobservation.Neuropsychologia,47,2100–2106.

Marshall,P.J.,&Meltzoff,A.N.(2011).Neuralmirroringsystems:ExploringtheEEGmurhythminhumanin-fancy.Developmental Cognitive Neuroscience,1,110–123.

Marshall,P.J.,&Meltzoff,A.N.(2015).Bodymapsintheinfantbrain.Trends in Cognitive Sciences,19,499–505.Marshall,P.J.,Saby,J.N.,&Meltzoff,A.N.(2013).Imitationandthedevelopingsocialbrain:Infants’somatotopic

EEGpatternsforactsofselfandother.International Journal of Psychological Research,6,22–29.Marshall, P. J., & Meltzoff, A. N. (2014). Neural mirroring mechanisms and imitation in human infants.

Philosophical Transactions of the Royal Society B: Biological Sciences,369,20130620.Martinez-Alvarez,A.,Pons,F.,&deDiego-Balaguer,R.(2017).Endogenoustemporalattentionintheabsenceof

stimulus-drivencuesemergesinthesecondyearoflife.PLoS One,12,e0184698.Meltzoff,A.N.,&Marshall,P.J.(2018).Humaninfantimitationasasocialsurvivalcircuit.Current Opinion in

Behavioral Sciences,24,130–136.Meltzoff,A.N.,Saby,J.N.,&Marshall,P.J.(2019).Neuralrepresentationsofthebodyin60-day-oldhumanin-

fants.Developmental Science,22,e12698.Meltzoff,A.N.,&Marshall,P.J.(2020).Importanceofbodyrepresentationsinsocial-cognitivedevelopment:New

insightsfrominfantbrainscience.Progress in Brain Research,254,25–48.

| 17SHEN et al.

Meltzoff,A.N.,Ramírez,R.R.,Saby,J.N.,Larson,E.,Taulu,S.,&Marshall,P.J.(2018).Infantbrainresponsestofeltandobservedtouchofhandsandfeet:AnMEGstudy.Developmental Science,21,e12651.

Mento,G.,&Valenza,E.(2016).Spatiotemporalneurodynamicsofautomatictemporalexpectancyin9-montholdinfants.Scientific Reports,6,36525.

Müller,B.C.,Meinhardt,J.,&Paulus,M.(2017).Embodiedsimulationofothersbeingtouchedin1-year-oldin-fants.Developmental Neuropsychology,42,198–206.

Petersen,S.E.,&Posner,M.I.(2012).Theattentionsystemofthehumanbrain:20yearsafter.Annual Review of Neuroscience,35,73–89.

Piccardi,E.S.,BegumAli,J.,Jones,E.J.H.,Mason,L.,Charman,T.,Johnson,M.H.,Gliga,T.,&BASIS/STAARSTeam.(2021).Behaviouralandneuralmarkersoftactilesensoryprocessingininfantsatelevatedlikelihoodofautismspectrumdisorderand/orattentiondeficithyperactivitydisorder.Journal of Neurodevelopmental Disorders,13,1–18.

Posner,M.I.,Rothbart,M.K.,Sheese,B.E.,&Voelker,P.(2012).Controlnetworksandneuromodulatorsofearlydevelopment.Developmental Psychology,48,827–835.

Reddy,V.,Markova,G.,&Wallot,S.(2013).Anticipatoryadjustmentstobeingpickedupininfancy.PLoS One,8,e65289.

Reynolds,G.D.,Zhang,D.,&Guy,M.W.(2013).Infantattentiontodynamicaudiovisualstimuli:Lookdurationfrom3to9monthsofage.Infancy,18,554–577.

Richards,J.E.,&Casey,B.J.(1991).Heartratevariabilityduringattentionphasesinyounginfants.Psychophysiology,28,43–53.

Ritter,P.,Moosmann,M.,&Villringer,A.(2009).RolandicalphaandbetaEEGrhythms’strengthsareinverselyrelated to fMRI-BOLD signal in primary somatosensory and motor cortex. Human Brain Mapping, 30,1168–1187.

Rigato,S.,Ali,J.B.,VanVelzen,J.,&Bremner,A.J.(2014).Theneuralbasisofsomatosensoryremappingdevelopsinhumaninfancy.Current Biology,24,1222–1226.

Rothbart,M.K.,Sheese,B.E.,Rueda,M.R.,&Posner,M.I.(2011).Developingmechanismsofself-regulationinearlylife.Emotion Review,3,207–213.

Saby,J.N.,Meltzoff,A.N.,&Marshall,P.J.(2013).Infants’somatotopicneuralresponsestoseeinghumanactions:I’vegotyouundermyskin.PLoS One,8,e77905.

Saby,J.N.,Meltzoff,A.N.,&Marshall,P.J.(2015).Neuralbodymapsinhumaninfants:Somatotopicresponsestotactilestimulationin7-month-olds.NeuroImage,118,74–78.

Sadaghiani,S.,&Kleinschmidt,A.(2016).Brainnetworksandα-oscillations:Structuralandfunctionalfounda-tionsofcognitivecontrol.Trends in Cognitive Sciences,20,805–817.

Schroeder,C.E.,&Lakatos,P.(2009).Low-frequencyneuronaloscillationsasinstrumentsofsensoryselection.Trends in Neurosciences,32,9–18.

Schubert,J.T.W.,Buchholz,V.N.,Föcker,J.,Engel,A.K.,Röder,B.,&Heed,T.(2019).Alpha-bandoscillationsreflectexternalspatialcodingfortactilestimuliinsighted,butnotincongenitallyblindhumans.Scientific Reports,9,9215.

Schubert,R.,Haufe,S.,Blankenburg,F.,Villringer,A.,&Curio,G.(2009).Nowyou'llfeelit,nowyouwon't:EEG rhythms predict the effectiveness of perceptual masking. Journal of Cognitive Neuroscience, 21,2407–2419.

Shen,G.,Saby,J.N.,Drew,A.R.,&Marshall,P.J.(2017).Exploringpotentialsocialinfluencesonbrainpotentialsduringanticipationoftactilestimulation.Brain Research,1659,8–18.

Shen,G.,Weiss,S.M.,Meltzoff,A.N.,&Marshall,P.J.(2018).Thesomatosensorymismatchnegativityasawin-dowintobodyrepresentationsininfancy.International Journal of Psychophysiology,134,144–150.

Shen,G.,Meltzoff,A.N.,Weiss,S.M.,&Marshall,P.J.(2020).Bodyrepresentationininfants:Categoricalbound-ariesofbodypartsasassessedbysomatosensorymismatchnegativity.Developmental Cognitive Neuroscience,44,100795.

Somogyi,E.,Jacquey,L.,Heed,T.,Hoffmann,M.,Lockman,J.J.,Granjon,L.,Fagard,J.,&O’Regan,J.K.(2018).Which limb is it? Responses to vibrotactile stimulation in early infancy. British Journal of Developmental Psychology,36,384–401.

Southgate,V.,Johnson,M.H.,Osborne,T.,&Csibra,G.(2009).Predictivemotoractivationduringactionobserva-tioninhumaninfants.Biology Letters,5,769–772.

18 | SHEN et al.

Stapel,J.C.,Hunnius,S.,vanElk,M.,&Bekkering,H.(2010).Motoractivationduringobservationofunusualversusordinaryactionsininfancy.Social Neuroscience,5,451–460.

Thomas,R.L.,Misra,R.,Akkunt,E.,Ho,C.,Spence,C.,&Bremner,A.J.(2018).Sensitivitytoauditory-tactilecolocationinearlyinfancy.Developmental Science,21,e12597.

Thorpe,S.G.,Cannon,E.N.,&Fox,N.A.(2016).Spectralandsourcestructuraldevelopmentofmuandalpharhythmsfrominfancythroughadulthood.Clinical Neurophysiology,127,254–269.

vanEde,F.,Szebényi,S.,&Maris,E.(2014).Attentionalmodulationsofsomatosensoryalpha,betaandgammaoscillationsdissociatebetweenanticipationandstimulusprocessing.NeuroImage,97,134–141.

Wentworth,N.,&Haith,M.M.(1992).Event-specificexpectationsof2-and3-month-oldinfants.Developmental Psychology,28,842.

Weiss,S.M.,Meltzoff,A.N.,&Marshall,P.J.(2018).Neuralmeasuresofanticipatorybodilyattentioninchildren:Relationswithexecutivefunction.Developmental Cognitive Neuroscience,34,148–158.

Worden,M.S.,Foxe,J.J.,Wang,N.,&Simpson,G.V.(2000).Anticipatorybiasingofvisuospatialattentionin-dexedbyretinotopicallyspecificα-bandelectroencephalographyincreasesoveroccipitalcortex.The Journal of Neuroscience,20,RC63.

Xie,W.,Mallin,B.M.,&Richards,J.E.(2018).DevelopmentofinfantsustainedattentionanditsrelationtoEEGoscillations:AnEEGandcorticalsourceanalysisstudy.Developmental Science,21,e12562.

Yu,C.,&Smith,L.B.(2016).Thesocialoriginsofsustainedattentioninone-year-oldhumaninfants.Current Biology,26,1235–1240.

Zhang,Y.,&Ding,M.(2010).Detectionofaweaksomatosensorystimulus:Roleoftheprestimulusmurhythmanditstop-downmodulation.Journal of Cognitive Neuroscience,22,307–322.

How to cite this article:Shen,G.,Weiss,S.M.,Meltzoff,A.N.,&Marshall,P.J.(2021).Exploringdevelopmentalchangesininfantanticipationandperceptualprocessing:EEGresponsestotactilestimulation.Infancy,00,1–18.https://doi.org/10.1111/infa.12438