ContentslistsavailableatSciVerseScienceDirect
Developmental
Cognitive
Neuroscience
jo u r n al h om ep a ge :h t tp : / / w w w . e l s e v i e r . c o m / l o c a t e / d c n
Delayed
development
of
proactive
response
preparation
in
adolescents:
ERP
and
EMG
evidence
Clare
Killikelly
∗,
Dénes
Sz ˝ucs
∗CentreforNeuroscienceinEducation,DepartmentofPsychology,UniversityofCambridge,DowningStreet,Cambridge,CB23EB,UnitedKingdom
a
r
t
i
c
l
e
i
n
f
o
Articlehistory: Received1June2012
Receivedinrevisedform15August2012 Accepted16August2012
Keywords: Adolescents ERP
Electromyography
Contingentnegativevariation P3b
a
b
s
t
r
a
c
t
Thetransitionfromlateadolescencetoyoungadulthoodisoftenoverlookedinthecognitive neuroscienceliterature.Howeverthisisanimportantdevelopmentalperiodasevenolder adolescentshavenotyetreachedadultlevelabilityonmanycognitivetasks.Adolescents (16–17-yearolds)andyoungadults(23–30-yearolds)weretestedonacuedtaskswitching paradigmspecificallydesignedtoisolateresponsepreparationfromresponseexecution.A combinedERPandeletromyographic(EMG)investigationrevealedthatadolescentshave attenuatedcontingentnegativevariation(CNV)activityduringresponsepreparation fol-lowedbylargerP3bamplitudeandEMGactivityintheincorrectresponsehandduring responseexecution.Thisisconsistentwithdeficientresponsepreparationandareactive controlstrategy.Converselyyoungadultsengagedincreasedresponsepreparationfollowed byattenuatedP3bactivityandearlyEMGactivityinthecorrectresponsehandduring responseexecutionwhichindicatesaproactivecontrolstrategy.Throughrealtimetracking ofresponse-relatedprocessingweprovidedirectevidenceofadevelopmentaldissociation betweenreactiveandproactivecontrol.Weassertthatadoptionofaproactivecontrol strategybyadolescentsisanimportantstepinthetransitiontoadulthood.
© 2012 Elsevier Ltd. All rights reserved.
1. Introduction
Impulsivity,lackofforesight,andpoordecision-making
aretrademarksofadolescentbehaviour(Crone,2009;Paus,
2005;Steinberg,2005).Neverthelessasadolescents
tran-sitionintoadulthoodtheywillneedtoengageappropriate
goaldirectedbehaviourdespitedistractingcomplex
envi-ronments.Currentlytheneuralprocessesresponsiblefor
the transition from immaturity in adolescence to
goal-directed behaviour in young adulthood have not been
clearly established (Andrews-Hanna et al., 2011).Some
researchsuggeststhatmanyoftheimmaturebehavioural
characteristicsofadolescenceresultfromlackofcognitive
∗ Correspondingauthors.Tel.:+4401223767600; fax:+4401223767602.
E-mailaddresses:[email protected](C.Killikelly), [email protected](D.Sz ˝ucs).
controli.e.‘theinabilitytoregulatethoughtsandactionsin
accordancewithinternallyrepresentedbehaviouralgoals’
(Andrews-Hannaetal.,2011;Braver,2012;Manzietal., 2011).
Recentlycognitivecontrolhasbeendissociatedintotwo
components;proactiveand reactivecontrol(Braverand
Gray,2007;Jacoby,1999).AccordingtoBraverandGray’s DualMechanismsofControlmodel(DMC)(2007)proactive
controlreferstoa preparatory processthat canbe
sus-tainedoverthecourseofthetaskwhereasreactivecontrol
isatransientcontrolprocessthatisimplementeddirectly
followingtheperceptionofastimulus.Researchsuggests
thatadolescentsmayusea reactivecontrol strategyfor
completingcomplexcognitivetasks,whereasyoungadults
have developed a proactive control strategy (
Andrews-Hanna et al.,2011; Manziet al., 2011).The aimof the
currentstudyistodeterminetheneuro-cognitive
mech-anisms underlying thedevelopmental proactive control
fromadolescencetoyoungadulthood.
1878-9293/$–seefrontmatter © 2012 Elsevier Ltd. All rights reserved. http://dx.doi.org/10.1016/j.dcn.2012.08.002
Importantly,thekeydifferencebetweenreactiveand
proactivecontrolcouldlieindifferentialmanagementof
responsepreparation.AccordingtoAron(2011)the
crite-riaforproactivecontrolhavetwokeyelements(1)advance
preparation and (2) selective control for a particular
responsetendency(Aron,2011).Chenetal.(2010)
theo-rizedthattheproactivecontrolsystemaffectsbehaviourby
adjustingthethresholdforresponseinitiation.Forexample
increasedproactivecontrolmaybeobtainedbycarefully
amendingresponseinitiation(e.g.slowingresponses).The
pre-supplementarymotorarea(preSMA),therightinferior
frontalcircuitandthesubthalamicnucleus(STN)arefound
tobe involved in both reactive and proactivestopping
however,importantly,inproactivestoppingthisstopping
networkispre-activated(Aron,2011).Thereforethekey
differencesbetweenproactiveandreactivecontrolcould
lie in the temporal activation of preparatory response
relatedprocessing.
Additionally the developmental coursefor sustained
responsecontrolextendsintolateadolescence(Hämmerer
etal.,2010;Ladouceuretal.,2004;Lunaetal.,2004a,b; Shing et al., 2010; Williams et al., 1999). An fMRI
investigationfoundthattransient(reactive)activationof
neuralareassupportinginhibitorycontroldecreasedfrom
childhoodto adolescencewhereas sustained (proactive)
activationincreasedinadulthood(Velanovaetal.,2009).
Thisperhapsisduetothedevelopmentofaproactive
con-trolstrategy.In particularOrdazet al.(2010)concluded
thatlimitationsinadolescents’abilitytoinhibitaresponse
may be related to fundamental differences invoked to
preparearesponse.
Inordertoexaminedevelopmentaldifferencesin
proac-tivepreparationwedesignedaconditionaltaskswitching
paradigm that can separate response preparation from
responseexecution.Inthisparadigmparticipantsarefirstly
presentedwithacircleorsquarevisualcuethathasbeen
designatedatthestartoftheexperimenttoindicatethat
thesubsequenttrialwillmostlikelybea‘go’trial(press
onthesamesideasthestimulus)oraswitchtrial(press
ontheoppositesidetothestimulus).Secondlyafterthe
circleorsquare(shape)cueatoneisheardthatwill
indi-cateeithergo,switch,orstopresponses(Fig.1).Theblocks
alsoincludedtrialsofGOcuesfollowedbyswitchtones
(GO/sw)andSWITCHcuesfollowedbygotones(SW/go).
Thiswastoensurethattheparticipantsactivelyengaged
controlthroughout thetaskand didnotcometoexpect
certainstimulus-responsepatterns.Stoptrialswerealso
includedtoensurethatparticipantsattendtothestimuli
and not just the cue. The time betweenthe shape cue
andthetoneisconsideredaresponsepreparationphase.
Neural differences in proactive response preparation in
conditionsoflow control(GO cuefollowed bygotone)
and highcontrol (Switch cue followed by switch tone)
willbecomparedinthisresponsepreparationphase.Itis
thoughtthatincreasedproactivecontrolwillbeengaged
during the condition of high control (Switch cue
fol-lowedbyswitchtone).Theprimaryaimofthisstudyis
tocomparetheneuralactivityofadolescentsandyoung
adults during the response preparation phase to
iden-tifywhetherornot theyusea similarproactivecontrol
strategy.
Fig.1.Schematicofseveraltrials.Participantsweretoldthattheblue circleindicatesthatagotonewilllikelyfollowwhereastheredsquare indicatesthataswitchtonewilllikelyfollow.Thiswascounterbalanced. Responsepreparationwasanalysedbetween0and1150msandresponse executionwasanalysedbetween1150and2250msafterthetone.
ToexaminepreparatoryneuralactivitytwoERP
compo-nentsarecommonlyexamined:thelateralizedreadiness
potential (LRP) and the contingent negative variation
(CNV).TheLRPisthoughttorepresenttheinitiationofa
motorresponseasitmeasuresthedifferentialactivation
ofelectrodesovertheleftandrightmotorcortex(C3and
C4respectively)(Grattonetal.,1988).TheLRPcangive
precisetemporalinformationabouttheactivationofthe
motorcortexinthecontextofresponsehandpreparation.
ThedevelopmentalprogressionoftheLRPhasbeen
iden-tifiedinchildren(Bryceetal.,2011;Ridderinkhofandvan
derMolen,1995;Szucsetal.,2009a)howevernotin
ado-lescents. Interms ofchildhood developmentit isfound
thatcorrectresponsehandpreparationbecomes
increas-inglyfaster with age(Ridderinkhof and vander Molen,
1995)whileearlyincorrecthandactivityduring
interfer-encedecreaseswithage(Szucsetal.,2009a).
Similarlyneuralcorrelatesofpreparationcanbe
mea-suredusingtheCNV(Weertsand Lang,1973).Response
activityisnormallyprecededbyanincreasinglynegative
waveoverfrontalandcentralelectrodecites.This
negativ-ityisfoundtoreflectmotorpreparationfortheresponse
(LovelessandSanford,1975),sensoryanticipation(Gómez
etal.,2003)andactivationofattentionalnetworks(Fan
et al.,2007).AlthoughtheCNV is nota direct measure
ofresponse-relatedprocessingitprovidesinformationon
preparatoryprocessing.FewstudieshaveexaminedCNV
preparatoryactivityacrossdevelopment,particularlyina
cued task-switchingcontext. Howeverstudiesinvolving
theNo-Gotaskandacue-probetaskhavefoundeitherthe
completeabsenceoftheCNVinchildren(Floresetal.,2009;
PerchetandGarcia-Larrea,2005)orincreasingamplitude withage(Jonkmanetal.,2003;Jonkman,2006).Wepredict
thatifadolescentshaveimmatureproactivecontrolduring
theresponsepreparatoryphasetheywillexhibitdecreased
LRPandCNVamplitudecomparedwithyoungadults.
Asthefocus isonresponse-relatedaspectsof
prepa-ration,electromyography(EMG)providesarobustdirect
measureofmotor activityatthelevelofeffectors.
Elec-trodesareplacedoneachhandandthiscanrecordparallel
(SzucsandSoltész,2010a;Szucsetal.,2009b).Thiscan
providedirect evidenceof corrector incorrectresponse
preparationbeforetheovertreactiontimeresponse(Szucs
andSoltész,2010a;Szucsetal.,2009b).Although
previ-ouslyunexploredinadolescentsEMGhasbeenexaminedin
childhooddevelopment.RecentlyvandeLaaretal.(2012)
foundthatmotoractivityduringapreparatoryperiod(pre
motortime)wasmostsensitivetoagerelatedchangesin
8–12-year-oldchildrenandcontinuestodevelopbeyond
12 yearsof age.Interms ofreactivecontrol,therobust
EMGsignalcanbeusedtodetectminutereactivemotor
activitytoacuefollowedby‘justintime’correctionfrom
incorrecttocorrecthandactivity.Boulinguezetal.(2008)
examinedEMGactivationinresponsetoawarningsignalin
asimpleRTtask.Fromexaminingthedistributionoferrors
theyfoundthatwarningsignalstriggertransientautomatic
EMGactivation.Theysuggestthatactivitytriggeredbythe
warningstimulusrequires‘proactivevolitionalinhibition’
topreventprematureresponding.
Althoughthemainaimofthestudywastoexamine
response related preparatory processing, stimulus level
processingwillalsobeexaminedtoindexearly
develop-mentaldifferences.ThelatencyandamplitudeoftheP3b
arecommonlythoughttoindexthespeedofstimulus
cat-egorization(Donchin,1981).TheP3bis commonlyused
toseparatedevelopmental changeatthe stimuluslevel
fromchangeattheresponselevelastheP3bisthoughtto
representstimulusprocessingindependentlyofresponse
levelprocessing(Bashoreetal.,1989;Szucsetal.,2009b).If
developmentaldifferencesarefoundintheamplitudeand
latencyoftheP3bthiscouldindicatedifferencesin
percep-tualandcognitiveprocessing.Additionallyanothermarker
ofearlystimulusprocessingistheP3awhichisafrontal
activitythatoccursaround300msafterthestimulus.In
adultsthisactivityisthoughttoberelatedtogeneral
stim-ulusselection(Dienetal.,2004;Polich,2007).However
in a study examining response inhibition and
prepara-tion,Jonkmanetal.(2003)concludedthattheabsenceof
frontalP3aactivity wasrelated todevelopmentaldelay
inresponseinhibition.Itiscurrentlyunclearwhat
devel-opmentalchangesintheP3aindicate.Thereforeanother
importantaimofthisstudywastocorrelateneural
physi-ologicalfindingswithrealworldbehaviours.Weexamined
therelationshipbetweenbehaviouralmeasuresofshort
termmemoryandworkingmemory(digitspanforwards
andbackwards;WAISIII)andstimulusprocessing(P3band
P3a)tofurtherexplainthefunctionalsignificanceof
devel-opmentaldifferences.Ifadolescentsuseareactivecontrol
strategythismaybedrivenbytheirinabilitytoeffectively
engagestimulusprocessingasevidencedbylackofP3band
P3aactivity.Byexaminingtherelationshipbetween
neu-ralcorrelatesofreactivecontrolandskillssuchasworking
memorywecanascertainifreactivecontrolinadolescents
haswidespreadeffectsintheclassroomandeverydaylife.
Hereouraimwastoisolateneural–physiological
dif-ferencesinadolescentsandyoungadultsastheyengaged
either proactiveorreactivecontrolduring theresponse
preparationphaseofacued-taskswitchingparadigm.We
expectedthatyoungadultswouldshowimproved
proac-tivecontrolwhencomparedwithadolescents.Thiswould
manifestinincreasednegativityintheCNVamplitudeand
theLRPamplitudeindicatingearlyresponsepreparationas
wellasincreasedEMGamplitudeinthecorrectresponding
hand.Weexpectedthatadolescentswouldshowvery
lit-tleornoCNVamplitudeorLRPindicatinglackofresponse
preparationandincreasedincorrecthandpreparationin
EMGactivityasindicativeofareactivecontrolstrategy.We
alsoexaminedreactiontimeactivitytoidentifytheaffect
of proactiveor reactivecontrolstrategy on behavioural
performance.Finallyinordertoexploretherelationship
betweenproactiveresponsepreparationandother
cogni-tiveskillsshorttermandworkingmemorywerecompared
betweenthetwogroups.
2. Method
2.1. Subjects
Initially40participantswereexamined.Howeverdue
toEEGartefacts5participantsfromtheadolescentgroup
and 5 participants from the young adult group were
rejectedfromtheanalysis.Theremaindercomposedtwo
agegroups:adolescents(n=15,meanage16.55years,1
lefthanded,10females),youngadults(n=15,meanage
25.83,4lefthanded,11females).Handednesswas
deter-minedaccordingtodominantwritinghand.Allsubjects
werefluentinEnglish,hadnormalorcorrectedtonormal
visionandwerewithoutahistoryofpsychiatricdisorder.
Informedconsentwasobtainedfromeachparticipantand
fromtheparentorguardianoftheadolescentparticipants.
TheadultswerefromtheCambridgeshirearea(UK).
Ado-lescentswerestudentsfromlocal6thformcollegesaround
Cambridge,UK.Thestudyreceivedapprovalfromthe
Uni-versityofCambridgePsychologyEthicsBoard.
2.2. Taskandstimuli
Oneachtrialashapecuewaspresentedfollowedbya
tonestimulus.Theshapecuewaseitherabluecircleorared
square.Beforetheexperimentinstructionsdesignatedthe
bluecircleortheredsquareaseitheragocueoraswitch
cue.Forexamplewhenthebluecirclerepresentedagocue
thenparticipantscouldexpectagotonetofollowinmost
ofthetrials;whentheredsquarerepresentedaswitchcue
thenparticipantscouldexpectaswitchtonetofollowin
mostof thetrials.Thiswascounterbalancedacross
par-ticipants.Thetone stimuluscouldbe200Hz, 500Hz or
1800Hz.Instructionsalsodesignatedthemeaningofthe
tonesintermsofgo,stoporswitchresponses.Thiswas
alsocounterbalancedacrossparticipants.Participantswere
instructedtowatchthecomputerscreenandholdabutton
pressusingtheirleftandrightthumbs.Theyweretoldto
respondasquicklyaspossibleoncetheyhadheardthetone.
AstheaimwastoexamineLRP,verticalspatialorientation
(upanddownasopposedtohorizontal;leftandright)ofthe
stimuliwasusedtoavoidconfoundingandsimultaneous
lateralizedactivationoftheoccipitalcortex.Thereforethe
differentcombinationsofcuestimuliandtonescreated6
differentconditions(Table1).
For thepurposeof this investigationwe were
inter-estedin twoconditions:theGOcuefollowedbythego
Table1
Stimuliproportionsofthecuedtaskswitchingexperiment.
Cue Tone %oftotaltrials
GOcue GO 35% SWITCH 10% STOP 5% SWITCHcue GO 10% SWITCH 35% STOP 5%
tone(SW/sw).Thisallowsforthecomparisonofa
condi-tionwherelowcontrolisrequired(GO/go)withacondition
ofhighcontrol(SW/sw).Bothoftheseconditionsoccurred
with35%probabilityacrosstheexperiment.
Participantsperformedatotalof8blockswith80trials
perblock.Thestimuliwerepseudo-randomizedwhereby
eachsubjecthadadifferentrandomorderofstimuli
pre-sentation. This was to ensure that there would be no
randomeffectsduetooneparticularstimuli
randomiza-tion.Subjectswereseatedinasmallroomfacinga19in.
computerscreen.Stimuliwerepresentedonawhite
back-ground.Eachtrialstartedwithafixationpoint(pictureof
aneye)for300ms.Thiswasfollowedbyablankscreenfor
1000ms.Thecuestimulusthenappearedfor1050ms
fol-lowedbyblankscreen.Thetone,duration100ms,therefore
appeared1150msafterthecuestimulionset.Aresponse
periodof1000msfollowed.Participantswereinstructed
toblinkwhentheysawthefixationeye.Beforethe
experi-mentalblocksonepracticeblockwascompletedwith15
stimuli. Stimuli were presented using the
Neurobehav-ioralSystemsPresentation11 program.For thepurpose
ofthis investigationwewereinterested inexamininga
preparationphasebetweenthecueandthetonestimulus
(0–1050msrelativetocueonset)andaresponse
execu-tionphaseafterthetonestimulus(1250–2250msrelative
tocueonset)(Fig.1).In thestatisticalanalysisthe
vari-ableof‘pre/posttone’describesa comparisonof neural
activitybeforethetoneispresentedduringtheresponse
preparationphaseandafterthetoneispresentedduring
theresponseexecutionphase.
2.3. Datarecordingandanalysis
Inboththebehaviouralandphysiologicalanalysispost
hocTukeytestswereusedtoexaminethecontrasts.The
EEGanalysisandbehaviouralanalysisincludedonly
cor-rectlyrespondedtrials.
2.3.1. Behaviouraldata
ArepeatedmeasuresANOVAwasusedtoexamine
reac-tiontimeandaccuracy.Group(adolescents,youngadults)
wasthebetweensubjectsfactorwhilecondition(GO/go,
SW/sw)wasthewithinsubjectsfactor.
Additionallybehavioural measuresof working
mem-oryandshorttermmemorywereadministeredfromthe
WAISIIIdigitspanforwardanddigitspanbackward
assess-ments.Anindependentt-testwasusedtocomparetheraw
scoresoftheyoungadultandadolescentgroups.Pearson’s
parametriccorrelationwasperformedtocomparetheraw
scoresofworkingmemoryorshorttermmemorywithCNV
meanamplitudein theGO/goconditionandtheSW/sw
conditionduringpreparation.
2.3.2. EEGData
EEGdatawererecordedin anelectricallyand
acous-ticallyshieldedbooth using129-channelHydro-CellNet
fromanElectrical Geodesicssystem.Asamplingrateof
500Hzwasused.Anon-linebandpassfilterof0.01–70Hz
wasused.Offlinethedatawereband-passfilteredbetween
0.01and30Hzandrecomputedtoanaveragereference.
Epochswerefrom−100to2250msrelativetotheonset
ofshapecuepresentation.Datawasaveragebaseline
cor-rectedfrom−100to2250msbeforestimuluspresentation.
Individual channels were spineinterpolated if required
usingtheparametersdescribedbyPerrin(1990);anorder
of4anddegree10,lambda1E−05andweinterpolateda
maximumof10%ofthetotalelectrodesfollowingthe
rec-ommendationofElectricalGeodesics(EGI,Oregon,USA).
Participants were excludedduring preprocessingbefore
anydata analysisoccurred. Epochswereexcludedfrom
theanalysisifthefollowingartefactrejectioncriteriawere
violated;voltage deviations exceeding±120V relative
tobaseline,maximumgradientexceeding50V,andthe
lowest activitybelow 0.5V.Ifmore than 50%of trials
wererejectedforaparticipantthisparticipantwasthen
excludedfromanalysis.Afterartefactrejection,for
adoles-cents68.2%oftrialswereretainedfortheGO/gocondition
and69.1%fortheSW/swcondition.Foryoungadults69.4%
oftrialswereretainedfortheGO/goconditionand71.0%for
theSW/swcondition.EEGdatawereprocessedusingBrain
VisionAnalyzer(BrainProducts,Munich),Matlab7.9,SPSS
17.0andStatistica9.
FortheP3bcomponentapoolofcentro-parietal
elec-trodeswasexamined(electrodes54,55,61,62,67,72,77,
78,79).Theelectrodelocationsareshownintheschematic
topographyinFig.2.Theseelectrodeswerechosenbased
onpreviousliteraturethathasfoundtheP3b tobewell
definedatcentro-parietalsites(Donchin,1981;Luck,2005;
SzucsandSoltész,2010b).TheP3bpeaklatencyand
ampli-tudewereexaminedattwotimepoints;themostpositive
peakinthepreparatoryphase(250–600ms)andresponse
executionphase(1500–2000ms).P3bpeakamplitudesand
latencieswereenteredintoarepeatedmeasuresANOVAof
pre/posttonestimulus(2)×group(2)×condition(2).
TheP3aeffectwasobservedinatopographical
com-parisonofadolescentsandyoungadultsduringtheSW/sw
conditionfortheresponse executionphase. Thisfrontal
effect refersto anincreased positivityin thedifference
potentialbetweentheSW/swminusGO/goconditions.As
thiswasonlyobservedduringresponseexecutiontheP3a
effectwasidentifiedasthepositivemeanamplitudeina
frontalpoolofelectrodesbetween1500and1600msfor
eachagegroup(frontalelectrodes14,15,17,21)during
theSW/swcondition.Themeanamplitudeoftheaverage
ERPsintheSW/swconditionbetween1500and1600ms
wasexaminedinaonewayANOVA(group(2)×condition
(1))
TheLRPwascalculatedaccordingtoconvention(Coles,
1989): [(ER–EL)left hand response+(EL–ER) righthand
response]/2. ER representstheamplitude of theERP at
Fig.2.P3bactivityatcentro-parietalelectrodes.Verticallinerepresentsthetonestimulus.ThepeakamplitudeoftheP3bissignificantlygreaterinthe adolescentgroupduringresponseexecution(i.e.afterthetoneispresented)(F(1,28)11.326,p=0.0022).TheschematicheaddisplaystheP3bcentro-parietal electrodepool.Electrodes54,55,61,62,67,72,77,78,79(CpZ,P1,Pz,P2,Oz,O1,O2)arerepresentedbytheblacksquares.
representstheamplitudeoftheERPattheelectrodeover
theleft.Theleftandrightmotorcortexelectrodeswere
electrodes36and104respectively.Thesehavethe
equiv-alent of positions C3 and C4 in the traditional 10–20
electrodesystem.TherawLRPwaveformsweresmoothed
usinga50msmovingaveragewindowtoimprovesignal
tonoiseratio.Anadditionalbaselinecorrectionof100ms
before thecue was also applied. The peak latency and
amplitude ofstimulus lockedLRPs wascalculated from
400to800msrelativetocueonset.Themeanamplitude
of LRPwasexaminedbetween 600and800msrelative
tocueonset.Response-lockedLRPwasnotexaminedas
wewereinterestedinpreparatoryLRPactivityduringthe
responsepreparationphase(0–1050ms).Arepeated
meas-uresANOVAofgroup(2)×condition(2)wasperformed
onthepeaklatenciesandamplitudesaswellasthemean
amplitudeduringthespecifiedtimepoints.
ThemeanamplitudeoftheCNVwasexaminedatfrontal
(FcZ)andcentral(Cz)electrodesduringthepreparatory
periodof750–1050ms(Lutckeetal.,2008;Fanetal.,2007;
Floresetal.,2009).Anadditionalbaselinecorrectionof100
priortothecuewasperformed.Meanamplitudeduring
preparation (750–1050ms)wasenteredinto arepeated
measuresANOVAgroup(2)×condition(2)separatelyfor
theFcZandCzdata.
2.3.3. EMGdata
Muscleactivityinbothresponsefingerswasrecorded
usinganMP150dataacquisitionunit(BiopacInc.)EMGwas
measuredbyEMG110Camplifiers.110Sshielded
touch-proofleadswhereconnectedtotwodisposablecloth-based
hypoallergenicAg–AgClEL504recordingdiscelectrodes.
Theelectrodeswereplacedalongtheleftandright
flex-orsofthethumb(flexorpollicisbrevis).Anelectrodeon
the left elbow was used as a ground. Before the
elec-trodeswereappliedtheskinwaswashedwithsoapand
cleanedwithalcoholwipes.Theelectrodeswereattached
byadhesivesolidgel.EMGwassampledat2000Hz and
bandpassfilteredbetween10and500Hz.Thedatawas
thenrectifiedandscaledrelativetothemaximum
ampli-tudeineachindividualasmeasuredfromcontinuousdata.
EMGwasbaselinecorrectedbetween−100and0ms
rel-ativetocuepresentationandisdisplayedasapercentage
ofthemaximumvaluemeasured.Epochsextendedfrom
−100to2250msrelativetocuepresentation.The
grand-averagedEMGwaveswerecalculatedforeachcondition
andsmoothedwithamovingaverageof50mstoimprove
thesignal tonoise ratio.Peak latencyand peak
ampli-tudevalueswerecalculatedforcorrectandincorrecthand
activity during preparation (100–500ms) and response
execution(1500–2000ms).Forthepeaklatencyand
ampli-tudearepeatedmeasuresANOVAofgroup(2)×condition
(2) were performed separately for correct and
incor-rect hand activity as wellas together group (2)×hand
(2)× condition(2).
Themeanamplitudeofincorrecthandactivitywasalso
examinedduringpreparationbetween900and 1100ms
and during execution between 1700 and 2000ms. The
meanamplitude ofcorrect hand activitywasexamined
between200and300msinpreparationandbetween1500
and2000msinexecution.RepeatedmeasuresANOVAof
group(2)×condition(2)wasperformedseparatelyfor
cor-rectandincorrecthandactivity.At-testofallmeansagainst
zero wasperformed on incorrecthand activity in each
grouptoensureasignificantdeviationfrombaseline.A
dependentsamplest-testwasperformedtocomparethe
peaklatency,peakamplitudeandmeanamplitudeofthe
GO/goandSW/swconditionsintheadolescents’incorrect
handactivity.
3. Results
3.1. Behavioural
AccuracyandRTvaluesareshowninTable2.RTand
accuracyvalues wereobtainedafterexcludingpotential
fast guesses (responses faster than 150ms). RT during
SW/sw trials (1782ms) was 28ms slower than GO/go
trials (1754ms) (F(1,28) 6.995, p=0.0133). Additionally
therewasamarginalgroup×conditioninteraction(F(1,28)
2.981,p=0.095)wherebyyoungadultswereslightlyfaster
Table2
Reactiontime(ms),accuracy(%),standarderrorvaluesinbrackets.
Group Measure GO/go SW/sw
Adolescents RT 1789(±26.9) 1799(±32.5)
Accuracy 90.1(±2.47) 85.1(±3.34)
Youngadults RT 1718(±33.23) 1765(±33.9)
Accuracy 94.0(±2.10) 91.4(±1.83)
adolescentsdidnotshowthesameimprovementinRT
dur-ingtheGO/gotrials.Errorratesbetweenthetwogroupsdid
notsignificantlydifferandtherewerenointeractions.
3.2. P3b
GrandaveragedERPsofrepresentativecentro-parietal
electrodes(54,55, 61,62,67,72, 77,78,79)areshown
inFig.2.IntherepeatedmeasuresANOVApre/posttone
(2)× group(2)× condition(2)asignificantpre/posttone
stimulus×groupinteractionwasfoundforthepeak
ampli-tudeof the P3b (F(1,28) 11.326, p=0.0022). During the
responseexecutiontimewindow(postcue)theP3bpeak
amplitudewassignificantlygreaterinadolescents(6.2V)
when compared to young adults (3.4V) (p=0.0053).
TherewerenosignificanteffectsfortheP3bpeaklatency.
3.3. P3aeffect
ThetopographicaldifferencesbetweentheSW/swand
GO/gocondition(SW/swminusGO/godifference
topogra-phies)at a groupingof 4frontal electrodes(14,15, 17,
21)areshowninFig.3.For theonewayANOVA(group
(2)×condition (1)) a marginal group effect was found
(F(1,28) 3.907, p=0.0580) between 1460 and 1550ms.
ThemeanamplitudeoftheP3adifferencepotentialwas
significantlymorepositiveinyoungadultgroup(0.67V)
thanintheadolescentgroup(−0.40V)duringtheSW/sw
condition.
3.4. CNV
Grand averagedERPs ofrepresentative FcZ electrode
whereCNVshowedthemaximumamplitudeareshown
in Fig. 4. For the repeated measures ANOVA group
(2)× condition(2)asignificanteffectofgroupwasfound
(F(1,28)=5.03, p=0.0329)whereby youngadultshad an
enhancedCNVnegativity(−2.68V)comparedto
adoles-cents(−0.99V).ThemeanamplitudeoftheCNVwasalso
examinedatCzhowevernosignificantgrouporcondition
effectswerefound.
Therewerenosignificantgroupdifferencesbetween
young adults and adolescents on the workingmemory
backward digit span raw scores (t(28)=1.00, p=0.325).
However as seen in Fig. 5 in adolescents a significant
negativecorrelationwasfoundwhentheCNVmean
ampli-tudeduringtheGO/goconditionwascomparedwithraw
workingmemoryscoresontheWAISIIIbackwarddigit
spantest(r=−0.6214,p=0.013).Thiswasnotfoundfor
adults.Inadultsanadditionalcorrelationalanalysiswas
Fig.3. P3aeffectSW–swminusGO–godifferencetopographies.(A)AdultP3apositivityisvisiblebetween1460and1550ms.(B)AdolescentP3aisnot present.TheP3aeffectisclearlydissociablefromP3bactivity.
Fig.4.CNVFcZ.Verticallinerepresentsthepresentationofthetonestimulus.Asignificanteffectofgroupwasfound(F(1,28)=5.03,p=0.0329)whereby youngadultshadanenhancedCNVnegativity(−2.68V)comparedtoadolescents(−0.99V).Theschematicheaddisplayswhereanelectrodewas measuredfrontallyat6(Fcz)representedbyasmallcircle.
preformedwithouttheoutlyingdatapoint(x=8,y=−9in
theyoungadultgraph).Thisconfirmedourpreviousresults
andthereforedidnothaveanyundueinfluenceonthis
cor-relation.Withoutthisoutlyingdatapointtherewasstill
a non-significantcorrelationbetweenCNVmean
ampli-tudeandworkingmemoryscoreintheyoungadultdata
(r=−.1174,p=0.689).
3.5. LRP
Thepeaklatencyandamplitudeaswellthemean
ampli-tude of the LRP at severaldifferent time points during
preparationandexecutionwereexamined.Nosignificant
groupdifferenceswerefound.
3.6. EMG
GrandaveragedEMGactivityinthecorrectand
incor-rectrespondinghandsisshowninFig.6.EMGactivityduring
execution phase(1250–2000ms): Correcthand activity. A
repeatedmeasuresANOVAofgroup(2)×condition(2)of
thepeaklatencybetween1500and2000revealeda
signif-icantmaineffectofgroup(F(1,28)5.022,p=0.0331).The
EMGpeak occurredsignificantlyearlier inyoungadults
(1695ms) than in adolescents (1781ms). The repeated
measuresANOVAofgroup(2)×condition(2)onthemean
amplitude of correct hand activity between 1500 and
2000msrevealedasignificantgroup×condition
interac-tion(F(1,28)=7.398,p=0.0111).The meanamplitudein
youngadultssignificantlydifferedbetweentheGO/govs
SW/swconditions(1.25Vvs1.35V)whereastherewas
nosignificantdifferencebetweentheseconditionsin
ado-lescents(0.93Vvs0.91V).Thereisatrendinthepeak
latencyoftheEMGdataforincreasedlatencyduringthe
SW/sw condition(e.g. GO/go 1733.95ms versusSW/sw
1767.5ms)howeveritwasnotsignificant(F(1,28)=0.209,
p=0.6510).
3.6.1. Incorrecthandactivity
The t-test on the mean amplitude between 1700
and 2000ms confirmed that the adolescent incorrect
handactivitysignificantlydifferedfromzero(t(14)=2.56,
p=0.0224) whereas the young adult hand activity was
onlymarginallydifferentfromzeroandthiswasnot
sig-nificant(t(14)=1.93,p=0.0739).Theactivitysurrounding
an‘initial dip’in youngadultmeanamplitudewasalso
Fig.5. Pearson’sparametriccorrelationbetweenFcZCNVmeanamplitudebetween500and1050msandrawworkingmemoryscoresonWAISDigitspan backward.(A)Asignificantnegativecorrelationisfoundforadolescentsr=−0.6214,p=0.013.(B)NosignificantcorrelationwasfoundforadultsforCNV meanamplitudeatworkingmemoryscorer=−0.0911,p=0.747.
Fig.6.EMGactivity.(A)Correcthandactivity.Thepeaklatencybetween 1500and2000revealedasignificantmaineffectofgroup(F(1,28)5.022, p=0.0331).Youngadultsweresignificantlyearlierthanadolescents.(B) Incorrecthandactivity.Inadolescentsincorrecthandactivitysignificantly deviatedfromzero(t(14)=2.56,p=0.0224).Verticallinerepresentstone stimulus.
examinedbetween1150and1800ms(seeFig.6).Firstly
themeanamplitudewasexaminedfrom1150to1350ms
andnosignificantgroupeffectswerefound(F(1,28)=0.209,
p=0.6510). Secondlythepeak amplitudewasexamined
between1400and1500ms.Amarginalgroupeffectwas
found (F(1,28)=3.638, p=0.0667). Finally in the period
afterthedipfrom1500to1800msthemeanamplitudewas
examinedandtherewasnosignificantdifferencebetween
thegroups(F(1,28)=0.833,p=0.3691).
4. Discussion
The neural mechanisms responsible for the
trans-formation from the immature adolescent brain to the
goal-directedyoungadultbrainareelusive.Arecent
the-oryofcognitivecontrol,thedualmechanismsofcontrol
model(Braver and Gray,2007)suggeststhat variability
intheabilitytoperformcomplexcognitivetasksmaybe
duetotheuseoftwodifferenttypesofcontrol;proactive
andreactive.Ithasbeensuggestedthatadolescentsusea
reactiveasopposedtoproactivecontrolstrategyandthis
mayunderliemanyofthebehaviouraldifferencesobserved
betweenadolescentsand youngadults(Andrews-Hanna
etal.,2011).Here wesoughttopinpointdevelopmental
differencesintheneuralpropertiesofproactiveand
reac-tivecontrolduringtheresponse preparation phaseof a
cued-taskswitchingparadigm.
We found that adolescents did not use a proactive
responsepreparation strategy.Thelack ofCNVandLRP
amplitudeduringthepreparatoryphaseindicatesless
effi-cientresponsepreparation.EMGrevealeddelayedcorrect
handactivityandincreasedincorrecthandactivity.
Inter-estinglyincreasedP3bamplitudeintheexecutionphase
inadolescentsbutnotinyoungadultssuggeststhelackof
abilitytotranslatecueinformationintoefficientresponse
execution.Thisisdiscussedintermsofdifferentproactive
neuro-cognitivemechanisms.
Thebehaviouralresultsfollowedtheexpectedpattern.
The reaction time in theSW/sw trials wassignificantly
longerthantheGO/gotrials.Inpreviousstudiesahallmark
ofaproactivestrategyhasbeenslowerreactiontimes
dur-ingmoredifficulttrials(Aron,2007,2011).Thisconfirms
thattheSW/swconditioninthistaskprovidestheplatform
forengagingproactivecontrol.Additionallyintheyoung
adultgrouptheGO/goconditionandSW/swcondition
dif-feredby50mswhereasintheadolescentsthisdifference
wasonly10ms.Thiscouldindicatethatadolescentsdid
notusedifferentstrategiesforthesetwoconditionsand
insteadusedaslowerreactivestrategyforbothlowand
highconflictconditions.Thisisanon-significanttrendin
RTbutsignificantinEMGactivity.
Arguably it is beneficial to have similar behavioural
performance betweentwo agegroupsasthis allowsfor
theanalysisof neuralactivitywithoutbehavioural
con-founds(Luna,2009).Howeverinfuturestudiesdifferences
atthebehaviouralandneurallevelcouldbecorrelatedwith
realworldmeasuressuchasdecisionmaking,impulsivity,
andrisktakingasthiswouldprovidegreaterinsightinto
thebreadthofneuro-cognitivechangeduringadolescence
(seeGeierandLuna,2010;Andrews-Hannaetal.,2011).
Forexampleindividualdifferencesinadolescence
perfor-manceandneuralactivitymayhelptoexplaindifferences
inrealworldbehaviourssuchasimpulsivityandlackof
foresight.
4.1. Neuralcorrelatesofresponsepreparation:CNVand
LRP
Wefoundnosignificantconditionorgroupdifferences
inthelatencyandamplitudeofincorrecthandLRP
activ-ity.EventhoughtheLRPisfoundtobeausefulmeasureof
responsepreparationtherearesomedifficulties.One
prob-lemisthattheLRPiscalculatedbyexaminingthesumof
activityoverbothcortices(correctandincorrectactivity)
(Grattonetal.,1988).Thereforeincorrecthandactivityis
undetectableifitoccursatthesametimeascorrecthand
activity.Szucsetal.haveonlybeenabletodetectincorrect
handactivityintheLRPinonepreviousstudy.Inthiscase
incorrecthandactivityonsetveryquicklywhereascorrect
activityoccurredmuchlaterduetothenatureofthetask
(Szucsetal.,2009a).Perhapsthedesignofthiscurrenttask
permittedsimultaneouscorrectandincorrecthandactivity
thereforerenderingdifferencesintheLRPundetectable.
CNV activityconfirms the useof a proactivecontrol
strategyinyoungadults.Youngadultsdisplayedan
aug-mentationinCNVnegativityduringthepreparatoryphase
therebyindicatingincreasedneuralpreparation.Thiswas
notpresentinadolescents.Severalauthorshavefoundthat
duringdevelopmenttheCNViseitherabsent(Perchetand
Garcia-Larrea,2005)orofsignificantlysmalleramplitude
thaninyoungadults(Jonkmanetal.,2003;Jonkman,2006).
extendeddevelopmentofthefrontallobes(Adlemanetal., 2002;Rubiaetal.,2000;Sowelletal.,2003;Velanovaetal., 2009).Jonkman(2006)concludedthatthereducedCNVin
adolescentsisduetoanimmaturefrontalparietalnetwork
involvedintheregulationofmotorcontrol.
AdditionallythelinkbetweentheCNV,working
mem-oryandprefrontalcortexactivityprovidesaninteresting
frameworkforinterpretingthecurrentresults.The
rela-tionshipbetweenCNVactivityandbehaviouralmeasures
of working memory and short term memory was also
examined. Only in adolescents was there a significant
negativecorrelationbetweenworkingmemoryscoreand
CNVmeanamplitude;asworkingmemoryimprovedCNV
preparatory negativityincreased.Asthis wasnotfound
inyoungadults,itappearsthatadolescentsarestillusing
workingmemorytomediateandimprovepreparatoryCNV
activity.Fuster(2002)suggestedthattheprefrontal
cor-texusestwodifferentskillsforthetemporalorganization
of behaviour;workingmemoryand preparatoryset.He
suggeststhatworkingmemoryisa‘retrospectiveaction’
tocollatesensoryinformationwhereaspreparatorysetis
a‘prospectiveaction’whichdependsontherelationship
betweenthecueandtheresponse.Perhapsdelayed
pre-frontaldevelopmentinadolescenceresultsinanincreasein
workingmemoryasaretrospective/reactiveasopposedto
prospective/proactivestrategyasindicatedbylackofCNV
activity.
4.2. EMG:correctandincorrecthandactivity
OveralltheRTconditiondifferencespreviously
men-tionedandEMGactivityvalidatetheparadigm.TheSW/sw
conditionactivatedthecorrecthandtoagreaterdegree
thantheGO/goconditionduringresponseexecution.This
confirmsthatthemoredifficultconditionrequiredgreater
handactivationandresponsecontrol.EMGhasbeenused
toexaminemotorlevelengagementofresponsecontrol
duringconditionsofdifferingdegreesofdifficultyor
con-flict(Burle etal.,2002; Szucsand Soltész,2010a;Szucs etal.,2009b).IncreasedcorrectEMGactivityisoftenfound
duringthemoredifficultcondition(incongruentcondition)
(Szucsetal.,2009b,Fig.8;SzucsandSoltész,2010a,Fig.2).
EMG activityrevealsa performancebenefit inyoung
adultsatthemotorlevelpotentiallyduetoearlier
proac-tive preparation; this is absent in adolescents. First of
allyoungadults had earlierpeak latencyin EMG
activ-ityduringresponseexecutionthanadolescentsacrossall
theconditions.Thispotentiallyindicatesgreatercertainty
inresponding.Subsequentlyduringtheresponse
execu-tionphase youngadultssuccessfully engagedadditional
processingresourcesduringtheSW/swconditionas
indi-catedbyincreasedmeanamplitudecomparedtotheGO/go
condition.Adolescentsdidnotdifferentiallyengagemotor
resourcesduringthesetwoconditions.Additionally
incor-recthandactivitywassignificantlygreaterthanbaseline
inadolescentsindicatingalackofresponsecontrol
dur-ingresponseexecution.Interestinglyinyoungadultsan
initialdip(decreasedactivity)in incorrecthandactivity
between1400and1500msmayindicateinhibitionofboth
respondinghandsbeforethecorrect handwasengaged.
Thiswasnotpresentinadolescents.Overallduetotheir
delayedpeaklatencyandincreasedincorrecthandactivity
thisindicatesaninefficientresponseprocessingstrategy
foradolescents.
OnlytwopreviousstudieshaveexaminedEMGactivity
developmentally(RidderinkhofandvanderMolen,1995;
vande Laar etal., 2012).Thecurrent results confirma
delayeddevelopmentalcourseforresponse controlthat
extendsbeyondchildhood.vandeLaaretal.(2012)
exam-ineddevelopmentalchangesinachoiceRTtaskusinga
similarmethodology(LRPandEMG analysis)and found
changestothecentralcorticalaswellasperipheralmotor
structures underlying response speed. They found that
youngchildren(meanage7.7)experiencedagreaterdelay
during the pre-response selection time period coupled
with‘lesssteepslopeofEMGonsetandvariabilityinthe
motor command’. They conclude that younger children
arelatetoengageacentralmotorcommandduetoslow
stimulusprocessingandthisresultsininefficientresponse
preparation. Older children (mean age 11.9), however,
werefoundtohave anextended intervalbetweenEMG
onsetandresponse.Theysuggestthatinyoungchildhood
stimulusleveldifficultyextendstomotorlevelprocessing
whereas in olderchildhood the locusof developmental
change lies in the continued maturation of peripheral
motor processes. Earlierdevelopment of stimuluslevel
processinginchildhoodfollowedbythelatedevelopment
ofthe motorsystemhasbeen previouslynoted (Hogan
etal.,2005;Shawetal.,2008)howevertheexactfunctional
andstructuralchangeshavenotbeenclearlydocumented.
Thelatedevelopmentofthemotorsystemisan
interest-ingareaofresearchthatrequiresfurtherinvestigationas
ithasimplicationsforbetterunderstandingbehavioural
characteristicssuchasimpulsivity(Aron,2011).
4.3. P3bandP3aeffect
Although we confirm that the main locus of
devel-opmental transformation from adolescence to young
adulthoodliesinresponserelatedaspectsofcontrol,
devel-opmental differences in the P3b during the execution
phaseprovideaninterestingneuro-cognitiveframework
ofproactivecontrol.TheP3bduringtheresponse
execu-tionphasewassignificantlygreaterinadolescentsthanin
youngadults. AdditionallythelackofP3aeffectin
ado-lescentssuggeststhatfastupdatingofstimulusproperties
maybeunderdevelopedinadolescents(Dienetal.,2004).
Overalltheseresultssuggestthatprotractedstimulus
cate-gorizationinadolescentsleadstomoreinefficientresponse
execution.
Jahfari et al.(2010) identified three different
neuro-cognitivemechanisms thatmay underliethe slowerRT
foundinproactivecontrol.Adolescentsandyoungadults
mayusedifferentproactivestrategiesthatdrivethe
dif-ferences in P3b amplitude throughout the preparation
and execution phases. First active braking is described
as the process of proactively suppressing an initiated
response without completely cancelling it. This would
manifest in reduced excitability of neural
representa-tionsassociated withthe response beforethe stimulus
hasbeenpresented;forexamplesuppressed(delayedand
theirresponsesproactively.Second,theprolongeddecision
stagehypothesissuggeststhattheincreasedcognitiveload
requiredduringhighconflicttrialsmayaffectinformation
processing. This suggests that delay rests at the
deci-sionmakingstageofprocessing;forexampledelayedP3b
latency.Thirdlytheslowerresponsefacilitationhypothesis
suggeststhatdelayedRTresultsfromprolongedhesitancy
or cautionat the response level. This doesnot suggest
inhibition(astheactivebrakinghypothesissuggests)but
insteada delayedprocessingbetweentheinitiationofa
response and button press. In this case the P3b would
reflect normal stimulus categorization processing
how-everadelayormodificationinresponselevelprocessing
wouldbeexpected.In termsof youngadults itappears
thatthecurrentdatafitsthe‘slowerresponsefacilitation’
hypothesis.TheearlyandeffectiveP3bactivityfollowed
byincreasedamplitudeEMG activityfortheSW/sw
tri-alssuggestssuccessfulstimuluslevelprocessingfacilitates
response related processing. Conversely the adolescent
patternsuggestsaprolongeddecisionstage.Theincrease
P3bactivityafterthetoneisheardcouldberepresentative
ofdelayedstimuluscategorization.It is likely that
ado-lescentsuseareactivecontrolstrategytorapidlyupdate
stimuluscategorizationafterthetoneduringresponse
exe-cution.
Inconclusionweconfirmthatadolescentsuseareactive
controlstrategy.Thisismarkedbysignificantneuraland
physiological differencesin how adolescentsand young
adultsprepareandexecutearesponseduringacuedtask
switchingparadigm.InadolescentslackofCNV,andP3a
preparatory activity followed by delayed and incorrect
EMGactivityandincreasedP3bactivityduringresponse
executionrevealsamoretransient,reactiveandless
effi-cientcognitivestrategy.Furtherresearchintotheprecise
natureofthetransitionfromimpulsiveandinefficient
ado-lescentbehaviourtogoal-directedyoungadultbehaviouris
importantforadvancingdevelopmentaltheoryand
estab-lishingmodelsofneuralchange.
Conflictofinterest
Weconfirmthatthismanuscripthasnotbeenpublished
elsewhereandisnotunderconsiderationbyanother
jour-nal.Allauthorshaveapprovedthemanuscriptandagree
withsubmissiontotheJournalofDevelopmental
Cogni-tiveNeuroscience.Wehavereadandhaveabidedbythe
statementofethicalstandardsformanuscripts.Theauthors
havenoconflictsofinteresttodeclare.
Acknowledgements
Thisresearchwassupportedbygrantsfromthe
Cana-dianCentennialScholarshipfundandtheFundsforWomen
GraduatestoC.Killikelly.TheauthorsthankLauraVuillier
andHannahPinchamfortheirassistanceindesigningthe
taskandtheirusefulfeedback.
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