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A VEP study in sleeping and awake one-month-old infants and its relation with social behavior

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A VEP study in sleeping and awake one-month-old infants and its relation with social behavior
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  Int.J.DevlNeuroscience41(2015)37–43 ContentslistsavailableatScienceDirect International    Journal   of    DevelopmentalNeuroscience  j   ournal   home   page:www.elsevier.com/locate/ijdevneu A   VEP   study   in   sleeping   and   awake   one-month-oldinfants   and   its   relation   with   social   behavior Sara   Cruz a , ∗ ,Alberto   Crego a ,Eugénia   Ribeiro b ,   Óscar   Gonc¸    alves a , c , d ,Adriana   Sampaio a a NeuropsychophysiologyLaboratory,CIPsiSchoolof    Psychology,Universityof    Minho,Braga,Portugal b CIPsiSchoolofPsychology,UniversityofMinho,Braga,Portugal c DepartmentofCounselingandAppliedEducationalPsychology,BouvéCollegeof    HealthSciences,NortheasternUniversity,Boston,MA,USA d SpauldingCenterofNeuromodulation,Departmentof    PhysicalMedicine&Rehabilitation,SpauldingRehabilitationHospitalandMassachusettsGeneralHospital,HarvardMedicalSchool,Boston,MA,USA a   r   t   i   c   l   e   i   nf   o  Articlehistory: Received24October2014Receivedinrevisedform11December2014Accepted11December2014Availableonline15   December2014 Keywords: InfancyStateVEPsNeurobehavioralassessmentNBASDevelopment a   b   s   t   ra   ct With   the   presentstudy   we   aimedto   analyze   the   relationship   betweeninfants’   behavior   andtheir   visualevoked-potential   (VEPs)response.   Specifically,wewantto   verify   differences   regarding   the   VEP   responseinsleeping   andawake   infants   andif    an   association   between   VEP   components,   inbothgroups,with   neuro-behavioral   outcome   could   be   identified.Todo   so,thirty-two   full-term   and   healthy   infants,   approximately1-monthof    age,   were   assessedthrough   aVEPunpatterned   flashlight   stimuli   paradigm,   offered   intwo   dif-ferentintensities,   and   were   assessedusinganeurobehavioral   scale.   However,   only18infants   have   bothassessments,   and   therefore,   these   isthetotal   included   inbothanalysis.Infantsdisplayed   amature   neu-robehavioral   outcome,expectedfor   their   age.Weobserved   that   P2andN3   components   werepresentinboth   sleeping   and   awake   infants.Differences   between   intensities   werefound   regarding   the   P2   amplitude,but   only   inawake   infants.Regression   analysis   showed   thatN3   amplitude   predictedanadequate   socialinteractive   andinternal   regulatorybehavior   in   infants   who   wereawake   during   the   stimuli   presentation.Taking   intoaccountthat   social   orientationand   regulatorybehaviors   are   fundamental   keys   for   social-likebehavior   in1-month-old   infants,   thisstudy   provides   animportantapproachfor   assessing   physiologicalbiomarkers(VEPs)   andits   relation   with   social   behavior,   very   early   inpostnatal   development.   Moreover,weevidence   theimportance   of    theinfant’s   state   when   studyingdifferencesregarding   visual   thresholdprocessing   and   its   association   with   behavioral   outcome.©2014Elsevier   Ltd.All   rights   reserved. 1.Introduction Frombirth,infantsresponddifferentlytothesurroundingenvi-ronmentbychangingtheirstate,beingabletoattendto   distinctvisualstimuli.Thisabilityisespeciallynoticeableintheirpref-erenceforthehumanface,particularlytheirmother’s,whichisaddressedbytheinfant’seyegazeandtheimitationof    face-likepatterns( Johnsonetal.,   1991).Oncethisorientationbehaviortowardstheenvironmentisdisplayedveryearly,severalauthorshavebeeninterestedin   characterizingyounginfantsaccord-ingtotheirreactivityto   externalstimuli(Mikkolaetal.,   2007;Pihkoetal.,2004;Ceponieneetal.,2002).Thisreactivitycan ∗ Correspondingauthorat:NeuropsychophysiologyLaboratory,Schoolof    Psy-chology,UniversityofMinho,CampusdeGualtar,4710-057,Braga,Portugal.Tel.:+351253604220. E-mailaddress: saracruz@psi.uminho.pt(S.Cruz). be   decodedthroughdifferentbehavioralcharacteristics(Rothbart,2007;Calkinsetal.,1996).Forinstance,FeldmanandEidelman(2006)showedthatfull-termnewbornsexhibitmatureneuro-behavioralprofilesemphasizingtheirstateorganization,motormaturityandhigherorientationscoresto   bothsocialandnonso-cialstimuli,aswellasmoresettledcognitivedevelopmentandinteractivebehaviorwhenassessedlater.Acrosstheinfancyperiod,developmentalandbehavioralchangesareaccompaniedbybrainalterationsastheinfant’sresponsetotheenvironmentalstimulichangesin   parallelto   brainmaturationmechanism(Huttenlocher,2009).Differentstudieshaveusedpsychophysiologicaltechniques,suchasevent-relatedpotentials(ERP),toassesschangesin   theinfant’sbrainactivitythatoccurin   responsetoa   stimulusthatis   repeatedlypresented.Particularly,thestudyofvisualevokedpotentials(VEPs)hasbeenwidelyusedto   expandourknowledgeaboutthedifferentneurode-velopmentalpathwaysinveryyounginfants,allowingforfurthercomprehensionaboutthevisualmaturationandcorticalfunction http://dx.doi.org/10.1016/j.ijdevneu.2014.12.0060736-5748/©2014ElsevierLtd.Allrightsreserved.  38 S.Cruzetal./Int.J.   DevlNeuroscience41(2015)37–43 mechanisms,aswellasvisualsensoryprocessing(McGloneetal.,2013).EvidencefromVEPstudieshassuggestedthat,atapproximately1monthofage,thepresenceof    earlyVEPcomponents,suchasP2orN3,playanimportantroleasindicatorsof    healthybraindevelopment,astheirpresenceisassociatedwithvisualprocess-ingandproperneuralmaturationof    thevisualcortex(McGloneetal.,2013;KatoandWatanabe,2006;Benaventeetal.,2005;Kraemeretal.,1999).Indeed,evidencefromseveralstudieshasshownthattheP2   andN3arepresentin   earlyages,beingcharacter-izedasthemostrobustcomponentsinsensorystimuliprocessing,translatingamatureVEPneuraldevelopment(McGloneetal.,2013).However,thereseemstobelittleconsensusregardingtheVEPcharacteristicswhenassessedin   awakeorsleepinginfants(Mercurietal.,1995;Whyteetal.,1987).Infact,somestudies havesuggesteddifferencesregardingVEPcomponents’latencyandamplitudedependingontheinfant’salertnessstate,particularlyreportingthatawakeinfantsdisplaygreaterP2amplitudesandshorterlatencies(Benaventeetal.,2005;Mercurietal.,   1995).Inastudy,conductedbyShepherdetal.(1999),   withonlya   full-terminfant,theauthorshavefounddifferencesregardingtheN1andP2amplitudeandpeaklatenciesdependingontheinfant’sbehavioralstate.Indeed,infants’stateanditsimplicationsfordevelopmenthavebeenaddressed,indicatingthatbothsleepingandawakestatesseemessentialfordevelopmentandneuralmat-urationmechanisms(MentoandBisiacchi,2012;Fiferetal.,   2010).Morecommonly,alterationsin   VEPmorphologyarelinkedtoatypicaldevelopmentalfeaturesthataremirroredin   neurobe-havioralchanges,withimplicationsforbothcognitiveandsocialdomains(Liuetal.,2010;KatoandWatanabe,2006;Tsuneishietal.,1995).Thesephysiologicaldifferences,whencorrelatedwithneu-rodevelopmentaloutcomes,may   beusedasphysiologicalmarkersfortheearlyidentificationof    developmentalpathways(Liuetal.,2010;Isleretal.,2007;Majnemeretal.,1990).Associatingvisualprocessingthrougha   VEPassessmentinveryyounginfantsmaybeausefulapproachtoidentifyabnormaldevelopmentalchar-acteristics(Stanleyetal.,   2009),thereby,contributingto   a   betterunderstandingaboutitsimplicationsincognitiveandbehaviorabnormalities(Kirketal.,2013;Sampaioetal.,   2008).Therefore,withthepresentstudy,ourobjectivewas   to   identifyVEPcomponentsin1-month-oldinfants’responsetoanunpat-ternedflashlightvisualstimulusofferedin   twodifferentintensitiesinawakeandsleepinginfants.Additionally,weaimedtoanalyzeif theVEPresponsecanpredictadjustedneurobehavioraloutcomes.Takingintoaccountpreviousstudies,ourhypothesiswas   thattheVEPcomponentscouldbeidentifiedinveryyounginfantsin   thetwointensities,withgreateractivationbeingdisplayedin   responsetothehigherintensitystimulus.Moreover,wehypothesizedthatthisresponsedifferedaccordingto   theinfants’state(sleepingvs.awakeinfants),withthisphysiologicalresponsepredictingmatureneurobehavioralprofileswithrespecttotheirreactivitytobothexternal(orienting/interactivecharacteristics)andinternalstimuli(regulationcharacteristics). 2.Materialsandmethods  2.1.Participants Thisstudywasreviewedandacceptedbytheethicalcom-mitteefromHospitalPedroHispanoinMatosinhos,Portugal.Mother/infantdyadswererecruitedattheObstetricDepartmentwhentheinfantwasborn.Thirty-twohealthy,full-terminfants,aged1-month-old,wereassessedregardingtheirVEPresponse(17[53%]sleepingand15[47%]awake).Fromthistotal,welost14participants’neurobehavioralassessmentduetodifferentdistress  Table1 Infant’shealthcharacteristicsat   thetimeof    recruitmentandcollection.Participant’scharacteristicsAtrecruitmenttime Gestationalage(meanweeks)39Weight(meankg)3235Height(meankg)48.7Apgarscore(10thmin)10At   collectiontime Age(meandays)33Total   withVEPs   32Total   withNBAS   18Total   withVEPs   andNBAS18 presentedatthemomentof    datacollection(infant’sbehavioraldistress,mothers’availabilityorevendueto   feedingroutines).Therefore,overall,thetotalofinfantshavingboththeVEPandneu-robehavioralassessmentsis18(10girlsand8boys;9inthesleepgroupand9intheawakegroup)–seeTable1.Forthestatecharacterizationweusedthestatesconceptdevel-opedanddescribedbyBrazeltonandNugent(BrazeltonandNugent,1995).We   consideredasbeinginsleepingstatethoseinfantswho   presentedeyesclose,regularrespirationandno   orlittlespontaneousbodymovements(eitherindeeporactivesleep).Theawakeinfantswerecharacterizedashavingbrightlook,directedtothestimuli,minimalmotoractivityandreactivetothestimuli.Inthiscategory,wealsoincludedinfantsthatwereirritableduringthestimulipresentation.  2.2.VEPstimuli WhiteflasheswerepresentedusingthelampofaGrassPS33-PlusPhoticStimulator(Astro-MedInc.,Warwick,USA),positionedat50-cmdistancefromtheinfant.Thestimuluswasofferedin   twoblocksof    repeatedflasheswiththesamefrequency(2Hz)sep-arately,andeachblockwitha   differentintensity,during1min.Thestimulationintensitywas   setat1(0.09J   –   intensity1)and2(0.18J–intensity2)in   theflashposition(Odometal.,2010).Foreachblockpresentation,theflashpositionwasorganizedforthepurposeof    achievingdifferentcombinationsandofferedin   apseudo-randomizedway   (1   and2;2and1)sothatwe   couldcontrolthepresentationordereffect.  2.3.VEPdatarecordingandanalysis Electroencephalographicactivitywas   recordedwitha   Quick-AmpTMsystem,witha   32-electrodeActicapTMSysteminsertedinacapwithafrontopolargroundandaveragereferenced.32record-ing   electrodeswereplacedatFp1,Fp2,F3,F4,Fz,F7,F8,   FC1,FC2,FC5,FC6,T7,C3,Cz,C4,   T8,TP9,CP1,CP2,CP5,CP6,TP10,P3,P4,Pz,P7,P8,PO9,O1,Oz,O2,PO10inaccordancewiththeinternational10–20system( Jasper,1958)andelectrodeimpedanceswerekeptbelow10k  forallparticipants.EEGsignalswerecontinuouslyamplified,digitizedatsamplerateof250Hzandfilteredon-linewitha0.01–100Hz(12dB/octaveslope)bandpassfilterusingaQuick-AmpTMsystemamplifierandBrainVisionRecordersoft-ware(Version1.20).AllEEG   datawas   analyzedwithBrainVisionAnalyzersoftware(Version2.0.1).TheEEGwas   digitallyfilteredoff-linewitha   0.2–20Hzbandpassfilterand50Hznotchfilter.Itwasthencorrectedforocularartifactsbythesemiautomaticpro-cedurein   independentcomponentanalysis(ICA)( Jungetal.,   2000)andsegmentedintoepochsof    600msfrom100mspre-stimulusto   500ms   post-stimulus.Next,baselinecorrectionwasappliedand  S.Cruzet    al./Int.J.DevlNeuroscience41(2015)37–43 39  Table2 Mean(SEs)valuesforN2,   P2andN3peaksamplitude(  V)   andlatency(ms)recordedatO1,O2andOz.P2N3LatencyAmplitudeLatencyAmplitudeAwakeinfantsLowintensity204.36(8.86)5.69(1.43)340.84(15.68) − 2.52(0.64)Highintensity227.69   (15.89)8.61(1.86)377.24(15.32) − 1.76(0.66)SleepinginfantsLowintensity 199.71(11.20)6.24(1.33)320.31(15.04) − 2.30(1.01)Highintensity213.61   (15.30)5.98(1.28)335.16(18.99) − 3.44(1.17) epochsexceeding ± 200  Vatanyscalpelectrodewererejected.Finally,individualsubjectaveragesERPstime-lockedto   thetwodifferentstimuli(lowerandhigherintensity)werecomputedsep-arately.Aminimumof    30trialsperaveragewasrecordedandtheprocedurerepeatedtocheckreproducibility.GrandmeanaverageswerecomputedforeachstimulusandusedtodeterminethelatencyrangesinwhichthecorticalVEPcomponentsweremeasured.Theidentificationof    peaksin   indi-vidualaveragesweremadewitha   semiautomaticpeakdetectionprocedureand,subsequentlyreviewedandmanuallycorrectedatO1,OzandO2electrodesforeachparticipant.Whenpeakidentifi-cationwasdoubtful,responsesfromallelectrodeswerecompared,andtheresponsewascomparedtothegrandmeanaverages.Thevariabilityintheresponsewasconsiderable,whichis   com-monamonginfants,but,accordingto   thetypicalneonatalVEPwaveformmorphologyreportedbyMcGloneetal.(2013)itwasgenerallycharacterizedbya   positivewave(P2)peakingaround200ms   followedbyabroadnegativewave(N3)peakingaround350ms   (seeTable2),clearlyidentifiedin   allparticipants.Earlierpeaks,N1,P1andN2weremuchlessfrequentlyevokedandweresmallerincomparisonwiththelaterpeaks;therefore,thesecom-ponentswerenot   analyzed.  2.4.Neurobehavioralassessment  Fortheneurobehavioralassessment,weusedtheneonatalbehavioralassessmentscale(NBAS)(Alsetal.,   1977).   AtrainedandreliableexaminerontheNBAScarriedouttheassessmentandthecodificationprocess.Thisscaleassessesthenewborns’infantbehavioralrepertoirethrough28behavioralitemscodedona   9-pointscaleandtheneurologicalstatethrough18reflexitemscodedona4-pointscale.Itis   organizedinto7clusters(Lesteretal.,1982):habituation,orientation,motor,rangeof    state,regulationofstate,autonomicstabilityandreflexes.Takingintoaccounttheobjectivesof    thisstudy,weconsid-eredthefollowingclusterstocharacterizetheinfants’externalandinternalbehavior:(a)   orientation,forexternalbehaviorassess-ment,and(b)regulationofstatetoassesstheirinternalregulationability(Sprangleretal.,   1996;Lesteretal.,1982;Alsetal.,   1977).Indeed,bothclustersareassumedtomirrorsocialcharacteristicsinsuchyounginfantsassocialinvolvementimplyalertandorientingabilities,aswellasinternalregulatoryprocesses,in   ordertoattendandrespondtothesurroundingstimuli(BrazeltonandNugent,1995).Andoncethevisualassessmentis   proposedasanindi-catorofcorticalfunction(Atkinson,2002;BrazeltonandNugent,1995)whenassociatedtoinfants’externalandinternalresponsesto   stimuli,we   assumeitasa   psychophysiologicalmarkerof    socialbehavior.Fortheorientationscore,themeanof    theitemsinanimatevisual,inanimateauditory,inanimatevisual-auditory,animatevisual,animateauditory,animatevisual-auditoryandalertnesswascalculated;likewise,regardingtheregulationofstate,thescorewasobtainedbycalculatingthemeanof    theitemscuddliness,con-solability,self-quietingandhand-to-mouth.Inbothclusters,higherpunctuationsreflectmaturebehavioralperformances,asexpectedforthisage.  2.5.Procedure Datacollectionwascarriedoutina   quietroomwitha   temper-atureapproximately20–25 ◦ C   withluminosityandsoundfeaturescontrolled.Oncethefamilyarrived,theinformedconsentwasobtained.Westartedeitherwiththeneurobehavioralassessmentorwiththepsychophysiologicalrecordings,consideringthenew-borns’state.Regardingthephysiologicalprocedure,webeganthedatacollectionbycleaningtheinfant’sscalpwithdistilledwater,immediatelyfollowedbyplacingtheelectrodecapon   theinfant’shead.Then,theinfantwasplacedinhis/hermother’slap,asshewasseatedina   comfortablechair,andtheresearcherheldthestimu-latinglampata   50-cmdistancefromtheinfant’sfaceasflashesweredirectedtowardshis   or   hereyes.Motherswereaskedtostayquietduringthesessionsandnotto   movethemselvesortheinfant.Theuseofthepacifierwas   themaneuverrecommendedforcalmingdownthebabyifneeded.Whennecessary,theses-sionwasinterruptedtocalmdowntheinfantandafterwardsthestimulideliveringstartedfresh.Therefore,theinfant’sstatewasmaintainedin   eachvisualstimuliintensityblock.Thesessions’datacollectiondurationwas   approximately30min.  2.6.Dataanalyses 2.6.1.VEPs Datastatisticalanalysiswas   performedusingtheIBMSPSSStatistics22.Foreachcomponent(P2andN3),separaterepeated-measuresanalysesof    varianceANOVAswereconductedwithmeasurementsof    latency(ms)andamplitude(  V)fromanaverageofthethreeoccipitalelectrodes(O1,OzandO2),   theintensitystimulus(lowandhigh)aswithin-subjectfactor,andinfant’sstateasbetween-subjectsfactor(sleepingandawakeinfants).Theanalyseswereperformedwiththe32infantswherewe   hadEEGrecording. 1 Analphalevelof    0.05wasused,anddegreesoffreedomwerecorrectedbytheconservativeGreenhouse–Geisserestimate.All   posthocpairedcomparisonswereperformedwiththeBonferroniadjust-mentformultiplecomparisons(alphalevelof0.05).  2.6.2.NeurobehavioralassessmentanditsassociationwithVEPs FortheNBASanalysis,themeansandstandarddeviationsfortheinfant’sorientation/socialinteractionandregulationofstateclusterswerecalculated.Then,linearregressionanalyses,foreachVEPcomponentindependently,usingtheentermethod,waspre-formedto   verifywhethereachcomponentcouldpredictsleepingandawakeinfants’externalandinternalbehavior.Theassumptionsforperformingtheregressionanalysisweremet   (normaldistribu- 1 Anexploratoryanalysisconductedwith18infantswhohadbothVEPandneu-robehavioralmeasuresshowedsimilarresults.  40 S.Cruzetal./Int.J.   DevlNeuroscience41(2015)37–43 Fig.1. VEPresponseinsleepingandawakeinfantstothe2visualstimuliintensities.(a)   Grandaveragesof    VEPsforawakeandsleepinginfantsinresponsetothelowandhigh   intensities(blackandred   linesrespectively);(b)Voltagemapscorrespondingto   the   P2componentpeakinawakeandsleepinginfantsinresponseto   lowandhighintensities.(Forinterpretationofthereferencesto   colorinthisfigurelegend,thereaderis   referredto   the   webversionof    thisarticle.) tion;nomulticollinearity;homoscedasticity;independenterrors;independence;standardizedresiduals).Asreferredbefore,18par-ticipantswereincluded(9infantsaddressedtothesleepgroupandtheremaining9to   theawakegroup)inthisanalysis.Weconsid-eredthebehaviorclustersto   beourdependentvariableandtheVEPintensitiesstimuliourindependentfactor/variable. 3.Results Resultsarereportedintwosections:(1)theVEPresponseto   thetwovisualstimuliintensitiesinbothgroups(sleepingandawakeinfants)and(2)theneurobehavioralprofileanditsassociationwiththeVEPsinthetwogroups.  3.1.VEPresponseinsleepingandawakeinfants Thegrandaveragesof    theERPsforthetwostimuliintensities(lowandhigh)areshowninFig.1andtheamplitudeandlatencyvaluesofP2andN3componentsareshownin   Table2.TheanalysisoftheP2amplituderevealeda   significantinterac-tionbetweenintensityandtheinfant’sstate[F(130)=4.43,  p <   .05].Post-hocmultiplecomparisons(adjustedbyBonferronicorrection)indicatedthatP2amplitudescoresinawakeinfantsweresignif-icantlylargerinresponsetothehigh,comparingwiththelowintensity(  p =.01),whereasnointensitydifferenceswerefoundinthesleepinginfants(  p =.80).RegardingtheP2latency,nosignificantdifferenceswereobservedinrelationtotheintensitiesorinteractionwiththeinfant’sstate.N3amplitudeandlatencywas   notdifferentbetweenintensitiesorinitsinteractionwiththeinfant’sstate.  3.2.AssociationbetweenVEPandneurobehavioralclusters All   infantsdisplayedorganized,coherentandfocusedbehavior,observedin   theirneurobehavioralprofile(see   Table3).RegardingitsassociationwithVEPs,we   foundthattheN3com-ponentamplitudeinthelowerintensitywas   correlatedwithbothanadequateexternal,orientingbehavioralperformance( R 2 =0.38,  p =   0.04)andanadjustedinternalregulation( R 2 =   0.6,  p   =   0.009)butonlyinawokeninfants.However,nodifferenceswerefoundregardingtheN3latencyfortheorienting/socialinteractivebehav-ior( R 2 =0.2,  p   =   0.1)neitherfortheregulationof    state( R 2 =0.1,  Table3 Infants’neurobehavioralprofileconsideringalltheNBASclusters.NBASclusterMean(SD)Habituation6.6   (2.5)Orientation7.4   (1)Motorsystem5.7   (1.5)Rangeof    states4   (1.7)Regulationof    states5.4   (2)Autonomicsystem4.4   (1.5)Reflexes1.9   (0.3)  S.Cruzet    al./Int.J.DevlNeuroscience41(2015)37–43 41  Table4 Regressionanalysisresults,consideringtheVEPscomponents.SocialinteractionRegulationof    stateSleeping– R 2 adjustedsquare P    valueAwake– R 2 adjustedsquare P  valueSleeping– R 2 adjustedsquare P  valueAwake– R 2 adjustedsquare P    valueN2latencyIntensity1 − 0.0220.393 − 0.1430.89 − 0.050.458 − 0.1390.882N2   amplitudeIntensity1 − 0.1340.8170.047   0.276 − 0.0510.46 − 0.1340.817P2   latencyIntensity1 − 0.0560.474 − 0.1060.645 − 0.0570.475 − 0.0730.523P2   amplitudeIntensity1 − 0.0930.589 − 0.1130.68 − 0.060.484 − 0.1190.713N3   latencyIntensity1 − 0.093 0.589 0.202 0.125  − 0.0150.3780.105   0.206N3   amplitudeIntensity1 − 0.1190.7120.380.045 − 0.1340.8180.5940.009N2   latencyIntensity20.0740.242-0.1420.9540.1150.196 − 0.1150.69N2   amplitudeIntensity2 − 0.1340.8170.047   0.276 − 0.1390.876 − 0.1350.834P2   latencyIntensity2 − 0.0830.554 − 0.1430.990.0630.5150.052   0.555P2   amplitudeIntensity2 − 0.1190.709 − 0.1090.658 − 0.1350.829 − 0.1330.811N3   latencyIntensity2 − 0.1140.681 − 0.1410.925 − 0.1430.97 − 0.08   0.543N3   amplitudeIntensity20.1430.981 − 0.1420.9310.0340.295 − 0.1350.828  p =0.2).Similarly,wedidnotfindanassociationbetweenthehigherintensitywithorienting/socialinteractivebehavior[N3amplitude( R 2 =   − 0.14,  p =0.9);N3latency( R 2 = − 0.14,  p =   0.9)]andregulationofstate[N3amplitude( R 2 = − 0.14,  p =   0.8);N3latency( R 2 = − 0.08,  p =0.5)]inawakeinfants.Wedidnotfinda   statisticallysignificantassociationregardingtheP2component(amplitudeandlatency)inawokeninfantsandthebehaviorclustersinthelowerandhigherintensities(Table4).Finally,in   sleepinginfants,we   didnotfindassociationsbetweenVEPscomponents(N3andP2latencyandamplitude)regardingbothstimuliintensities(fordetailedinfor-mationseeTable4). 4.Discussion Withthepresentstudy,our   mainobjectiveswere:(a)determin-ingwhichVEPresponsecomponentswerepresentin1-month-oldinfantswhenpresentingthem2visualunpatternedflashstimuliintensities;(b)verifyingif    thereweredifferencesregardingthevisualstimuliprocessingintheinfantswhoweresleepingandawakeduringthestimulipresentation;and(c)understandingif theVEPcomponentscouldpredictanadjustedorientationand/orregulationbehaviorinone-month-oldinfants.Wefoundthatin   bothsleepingandawakeone-month-oldinfants,P2andN3componentswerepresentduringtheflashlightstimuli,inbothlowerandhigherintensities.Indeed,thepresenceofthesecomponentswasa   consistentandrobustfindingobservedamongallinfants.Theseresultsareconsistentwithpreviousfind-ings(McGloneetal.,   2013)   suggestingthatvisualcomponentssuchasP2orN3may   reflecta   maturebraindevelopmentinthefirstweeksoflife.Consideringtheflashstimuliintensities,ourresultsrevealedthattheinfantsdisplayedgreaterP2amplitudein   responsetothehigherintensitystimulus.Thiswasevidentonlywhentheinfantswereawoken.Therefore,theseresultssuggestthattheinfant’sstateiscrucialfordeterminingdifferentvisualprocess-ingthresholds.Infact,asithasbeenreportedbefore(Shepherdetal.,1999),infants’stateseemtoinfluencetheVEPpeakslatencyandamplituderegardingtheflashvisualresponse,onceinfantsthatareawakewerereportedtodisplaygreateramplitudesandshorterpeaklatencies(Benaventeetal.,2005).Thepresentstudy didnotcorroboratepreviousevidencesuggestingthattherearenodifferencesregardingtheVEPcharacterizationinsleepingandawakeinfants(Barnetetal.,1980;Ellingson,1970;Ferrissetal.,1967).However,itdemonstratedthatwhenstudyingdifferencesregardingthresholdprocessing,infants’stateis   essentialtotheVEPresponse.Thiscanbeduepossiblytothefactthatsimilarbehaviorstatemay   reduceintraandinter-subjectvariabilityinveryyounginfants,assuggestedbyApkarianetal.(1991).Ourstudysug- geststhattheinfant’sneuralresponsetodifferentstimulimay   bedependingontheirbehaviorstate(Prechtl,1974). Regardingtheneurobehavioralassessment,wehypothesizedthatone-month-oldinfantswouldrespondtosensorialstimula-tionintwobehavioralways:(a)throughanexternalresponsetothestimuli,and(b)throughtheinfants’abilityto   regulatethemselvesinordertorespondto   thatstimulation.Thesebehavioralcharac-teristicsaretranslatingsocialabilitiesdisplayedbyveryyounginfants(BrazeltonandNugent,1995).We   observedanassocia-tionbetweena   matureneurobehavioraloutcomeandtheVEP’spositiveN3amplitude(onceN3isanegativecomponenthigheramplitudemeansmorenegativity)inthelowerflashintensity.Moreover,onceagain,theseresultswereonlyevidentin   infantsthatwereawokenduringthevisualstimulation.Indeed,thebraindevelopmentatyoungagesischaracterizedasa   complexprocessthatoccursveryrapidly,namelya   fastincreaseinsynapticden-sityin   thevisualcortexinparallelwithintensemyelinationof thevisualtractsin   thefirstfourpostnatalmonths(Duboisetal.,2008).Theinfant’sphysiologicalresponsetosensorialstimulationistranslatedintobehavioralcharacteristicsthat   areassociatedwithspendingattentionalresourcesinordertodisplayadequateorient-ing/socialinteractiveandregulatingbehavioroutcomes(Atkinson,2002).Infact,infantsshowdifferentsensorialstimulationinputnecessitiesand/ordifficultiesthatarepresentearlyin   thedevel-opmentalprocess(Magneeetal.,2011).Forinstance,infantswho displaylowerstimuliprocessingthresholdsorseemtoodisorga-nizedtodealwiththeircontextwillneeddifferentstimuliinputsthanthoseinfantswho   arecalmerorrequiremorestimulationtoreact(BrazeltonandNugent,1995).Furthermore,ithasbeensug-gestedthatinthefirstmonthsoflifeinfantspresentanincrease
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