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Weaknesses in executive functioning predict the initiating of adolescents’
alcohol use
Peeters, M.; Janssen, T.; Monshouwer, K.; Boendermaker, W.J.; Pronk, T.; Wiers, R.;
Vollebergh, W.
DOI
10.1016/j.dcn.2015.04.003
Publication date
2015
Document Version
Final published version
Published in
Developmental Cognitive Neuroscience
License
CC BY-NC-ND
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Citation for published version (APA):
Peeters, M., Janssen, T., Monshouwer, K., Boendermaker, W. J., Pronk, T., Wiers, R., &
Vollebergh, W. (2015). Weaknesses in executive functioning predict the initiating of
adolescents’ alcohol use. Developmental Cognitive Neuroscience, 16, 139-146.
https://doi.org/10.1016/j.dcn.2015.04.003
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ContentslistsavailableatScienceDirect
Developmental
Cognitive
Neuroscience
jou rn a l h om ep ag e : h t t p : / / w w w . e l s e v i e r . c o m / l o c a t e / d c n
Weaknesses
in
executive
functioning
predict
the
initiating
of
adolescents’
alcohol
use
Margot
Peeters
a,∗,
Tim
Janssen
b,
Karin
Monshouwer
a,c,
Wouter
Boendermaker
b,
Thomas
Pronk
b,
Reinout
Wiers
b,
Wilma
Vollebergh
aaUtrechtUniversity,Utrecht,TheNetherlands bUniversityofAmsterdam,TheNetherlands cTrimbosInstitute,TheNetherlands
a
r
t
i
c
l
e
i
n
f
o
Articlehistory:
Received25September2014 Receivedinrevisedform8April2015 Accepted9April2015
Availableonline17April2015
Keywords: Executivefunctioning Alcoholuse Bingedrinking Adolescents Survivalanalyses Cognition
a
b
s
t
r
a
c
t
Recently,ithasbeensuggestedthatimpairmentsinexecutivefunctioningmightberiskfactorsfor theonsetofalcoholuseratherthanaresultofheavyalcoholuse.Inthepresentstudy,weexamined whethertwoaspectsofexecutivefunctioning,workingmemoryandresponseinhibition,predictedthe firstalcoholicdrinkandfirstbingedrinkingepisodeinyoungadolescentsusingdiscretesurvival anal-yses.AdolescentswereselectedfromseveralDutchsecondaryschoolsincludingbothmainstreamand specialeducation(externalizingbehavioralproblems).Participantswere534adolescentsbetween12 and14yearsatbaseline.Executivefunctioningandalcoholusewereassessedfourtimesoveraperiod oftwoyears.Workingmemoryuniquelypredictedtheonsetoffirstdrink(p=.01)andfirstbinge drink-ingepisode(p=.04)whileresponseinhibitiononlyuniquelypredictedtheinitiatingofthefirstdrink (p=.01).Theseresultssuggestthattheassociationofexecutivefunctioningandalcoholconsumption foundinformerstudiescannotsimplybeinterpretedasaneffectofalcoholconsumption,asweaknesses inexecutivefunctioning,foundinalcoholnaïveadolescents,predicttheinitiatingof(binge)drinking. Though,prolongedandheavyalcoholusemightfurtherweakenalreadyexistingdeficiencies.
©2015TheAuthors.PublishedbyElsevierLtd.ThisisanopenaccessarticleundertheCCBY-NC-ND license(http://creativecommons.org/licenses/by-nc-nd/4.0/).
1. Introduction
Recentstudieshavedemonstratedassociationsbetween cog-nitivedeficitsand(heavy)drinkinginadolescents(Fernieetal., 2013;Hansonetal.,2011;Khuranaetal.,2012;Niggetal.,2006; Squegliaetal.,2009;Tapertetal.,2002).Especiallybinge drink-ingseemstobeassociatedwithcognitivedeficitsinadolescents andyoungadults(Hermensetal.,2013;Peetersetal.,2014).An importantquestionthatarisesfromthesefindingsiswhetherthese deficitsarepresentpriortoandpredicttheonsetofdrinkingor whetherthe(heavy)useofalcoholinducesthesedeficits.Although thisrelationshiphasbeeninvestigatedinseveralstudies(Fernie etal.,2013;Hansonetal.,2011;Khuranaetal.,2012;Niggetal., 2006;Squegliaetal.,2009;Tapertetal.,2002),noneofthesestudies haveincludedalcohol-naïveadolescentsatbaseline,whichclearly limitstheinterpretationoftheassociationsfound.Inthepresent studywethereforeexaminedwhethertherelativeweaknessesin
∗ Correspondingauthorat:UtrechtUniversity,Heidelberglaan1,3584CSUtrecht, TheNetherlands.Tel.:+31302533056.
E-mailaddress:m.peeters1@uu.nl(M.Peeters).
executivefunctions(i.e.,workingmemoryandresponseinhibition) predicttheinitiationofthefirstalcoholicdrinkandthefirstbinge drinkingepisodeinyoungadolescents.
1.1. Cognitivedevelopmentinadolescence
During adolescence several important cognitive functions matureanddevelop.Executivefunctionssuchasworking mem-ory,attentionandresponseinhibition,continuetomatureuntillate adolescence(BlakemoreandChoudhury,2006;Caseyetal.,2008). Thesefunctionsareimportantfortheplanning,organizationand coordinationofothercognitiveprocesses(Baddeley,1983;Miyake etal.,2000),andinvolveneuralnetworksincludingdifferentareas intheprefrontalcortex.Incontrasttootherbrainregions(e.g.,the visualcortex),theprefrontalcortexundergoeschangesuntillate adolescence(BlakemoreandChoudhury,2006).Workingmemory, inparticular,continuestomatureuntillate adolescence(18–21 years;Lunaetal.,2004).Inaddition,basiclevelsofresponse inhibi-tionarealreadypresentinearlychildhood;youngchildrenalready abletoinhibitresponses,however,improvementofthisfunction continuesintoadolescence(Lunaetal.,2004).Bothworking mem-oryandresponseinhibitionareimportantforcognitivecontrol;the
http://dx.doi.org/10.1016/j.dcn.2015.04.003
140 M.Peetersetal./DevelopmentalCognitiveNeuroscience16(2015)139–146
abilitytosuppressthoughtsandimpulsesinordertoachieve long-termgoals(BungeandWright,2007;Lunaetal.,2004;Steinberg, 2007).Cognitivecontrolhasoftenbeenrelated torisk behavior (Caseyetal.,2008;Steinberg,2007).Ithasbeenarguedthatthe slowermaturationoftheprefrontalcortex,andtheaccompanying gradualdevelopmentofcognitivecontrol,mightunderlietheoften observedincreasesinriskybehaviorsduringadolescence,including bingedrinking(Caseyetal.,2008;Steinberg,2007).Adifferentline ofresearchhassuggestedthattheincreaseinrisk-takingbehavior isamotivationalissue(CroneandDahl,2012).Itismore reward-ing,andthusmoremotivating,foradolescentsthanitisforadults toengageinriskybehaviorsbecauseoffactorssuchaspeer accep-tanceorpopularity,whichmightexplaintheincreasedrisk-taking behaviorduringadolescence(CroneandDahl,2012).Thedelayed developmentoftheprefrontalcortexandassociatedcognitive con-trolskillsinadolescentsmightthereforenotrepresenta“deficit” orimmaturefunctioning,butratherahighlyflexibleandadaptive development,tunedtothesocialdemandsadolescentsencounter (foradetaileddescriptionseeCroneandDahl,2012).Nevertheless, inbothlinesofresearch,thedevelopmentofcognitivecontrolin lateadolescenceplaysanimportantroleinexplainingrisk-taking behaviorsinadolescents.
1.2. Executivefunctioningandalcoholuse
Working memory (i.e., keeping information active) and responseinhibitionaretwoimportantexecutivefunctionsoften examinedin relationtoalcoholuse(Khuranaetal.,2012; Nigg etal.,2006;Verdejo-Garciaetal.,2008;Wiersetal.,2007).Deficits inresponse inhibitionand workingmemoryappear toincrease automaticandimpulsiveresponseinsuchawaythatbehavioral responsesinrelationtoalcoholstimuliaremorelikelydirectedby immediatesatisfactionofneedsthanpursuanceoflong-termgoals (Grenardetal.,2008;Thushetal.,2008;Peetersetal.,2012,2013; Wiersetal.,2007).Inotherwords,deficitsinexecutivefunctioning limitindividualstorespondinacontrolledandplannedmannerto alcoholstimuli,leadingtomoreimpulsiveandautomaticresponses whichhavebeenassociatedwithincreasedalcoholuse(Grenard etal.,2008;Thushetal.,2008;Peetersetal.,2012).
Severallongitudinalstudies haveexamined thedirect effect ofrelativelypoorexecutivefunctioningondrinkingbehavior in adolescence.Niggandcolleagues(2006),forinstance,foundthat poorinhibitionskillsinearlyadolescents(12–14years,N=498) predictedlater (15–17years)problematicalcohol use.Likewise, Khuranaandcolleagues(2012)foundthatrelativelypoor work-ing memorypredicted growth in the frequency of alcohol use ina community sample ofadolescents (N=358).Moreover,the authorsfoundthattheeffectofworkingmemoryonalcoholusewas mediatedbyimpulsivity suggestingthat poorworkingmemory functioningmightincreaseimpulsivebehaviorwhichsubsequently increasesalcoholuseamongadolescents.Inaddition,Fernieand colleagues(2013)foundthatseveralmeasuresofimpulsivity(i.e., delaydiscounting,risktakingandresponseinhibition)predicted increasein alcoholuseamong youngadolescents(12–13years, N=287).Thequestionremains,however,whetherthesedeficits precedeandpredicttheonsetofadolescents’drinking,sincethese studies have examined executive functioning after adolescents alreadyconsumedtheirfirstdrink,thusleavingopenthe possibil-itythattheimpairedexecutivefunctioningwasalreadytheresult ofearlierdrinking.
1.3. Currentstudy
In the present study we examined the predictive effect of workingmemoryandresponseinhibition,twoexecutivefunctions undertheheadingofcognitivecontrol,andfrequentlyassociated
withriskbehavior,ontheinitiatingofthefirstalcoholicdrinkina sampleofyoungadolescents(12–15years,beforethelegalalcohol buyingageof16–intheNetherlandsatthetimeofthestudy). Althoughcognitioninvolvesmany moreaspects thanexecutive functions,wedecidedtofocusonthesetwocognitions,since partic-ularlythesefunctionsareassumedtoplayavitalroleinadolescent alcoholuseastheycontinuetomatureinadolescence( Verdejo-Garciaetal.,2008).Bingedrinkingisacommondrinkingpattern amongyoungadolescents,andithasbeenlinkedtoseveral(health) riskbehaviors(Milleretal.,2007).Wethereforealsoexaminedthe predictiveeffectofexecutivefunctioningontheinitiatingofthe firstbingedrinkingepisode(i.e.,fiveormoreglassesonaday). Bothadolescentsform mainstreamas wellasadolescentsfrom specialeducation(SE)wereincludedinthestudytoascertain vari-ationindrinkingbehavior.Adolescentsin SEschoolshavebeen foundtodrinkmoreheavily(Kepperetal.,2011)comparedto ado-lescentsfrommainstreameducation.AdolescentsattendtheseSE schoolswhentheyhavebehavioralproblems(e.g.,conduct prob-lems,hyperactivity,attentionproblems),althoughtheymaynot necessarilybediagnosedwithabehavioraldisorder.These exter-nalizingbehavioralproblemsareassociatedwithrelativelyweak WMfunctioning(Barkley,1997;Pihletal.,1990),andmightplace adolescentsatriskforproblematicalcoholuseandlateralcohol dependence.
We hypothesizedthat relativelyweakworkingmemoryand responseinhibitionwouldpredicttheinitiatingofthefirstalcoholic drinkandthefirstbingedrinkingepisodeinthissample. Discrete-timesurvivalanalyseswasusedtodeterminetheinitiatingofthe firstdrinkandbingedrinkepisodeduringthetwo-yearfollow-up ofthestudyandtoevaluatethepredictiveeffectofexecutive func-tioning.Moreover,bothfunctionshavepreviouslybeenassociated withadolescentalcoholuseandproblemdrinking(Khuranaetal., 2012;Niggetal.,2006),althoughtheiruniquecontributiontothe initiatingofdrinkinghasnotyetbeenexaminedsimultaneously.
2. Materialsandmethod
2.1. Participants
Thisstudywaspartofalargerstudyinwhichweassessed self-reportedandbehavioralcognitions,andpersonalitystylesrelated toalcoholuseandotherriskbehaviors.Participantswererecruited fromseveralmainstreamand 17SEschoolsintheNetherlands. Maleswereslightlyoverrepresented(69%boysversus31%girls) becausemoreboysthangirlsattendSEschools(Oswaldetal.,2003). Forbothsamples,informedconsentofthechildaswellas pas-siveparentalconsentwasrequested.Inthemainstreamsample, 37parentsdeclinedparticipationoftheirchild.FortheSEsample, 15parentsand7studentsdeclinedparticipationinthisstudy.The mainstreamsampleincluded250adolescents(69%girls),selected fromanationalsurveystudy,whichwaspartoftheInternational Health Behavior of School-aged Children-survey (HBSC, Zanotti etal.,2012).AdolescentswhoparticipatedintheDutchnational studywerecontactedforadditionalassessmentsafterthe comple-tionofthemainsurvey.TheSEsampleincluded374adolescents (12%girls).Forthepurposeofthisstudy,adolescentsbetween12 and15yearswereselected,resultinginasampleof534(371boys, 163girls)adolescents.
Data were collected at intervals of 6–8 months acrossfour waves.Atbaseline,525adolescentsparticipatedinthestudy(98% of534,notethatsomeadolescentswereabsentduringthefirst wavebutparticipatedinthefollowingwaves).Overall,415(78%) adolescentsparticipatedinwave2,399(75%)adolescents partici-patedinwave3,and425(80%)adolescentsparticipatedinwave4. Missingcaseswereimputedusingamultipleimputationprogram
(i.e.,multipleimputationbychainedequations(MICE),whichis explainedbelow).Thedataoverfourwaveswerecollectedeither viatheInternet (inthecase of mainstreameducation) orvia a trainedresearchassistant(inthecaseofSEeducation).Adolescents fromSEcompletedthequestionnairewithpenandpaperfollowed byacomputersessiontoassessthecomputertasks.FiveoftheSE studentscompletedonlythecomputertasksatbaselineanddidnot completethequestionnaire.Sinceweusedmultipleimputationto handlemissingcases,weincludedtheseadolescentsinthestudy forfurtheranalysis.
2.2. Measures
2.2.1. Demographicalmeasures
Sex,ageandexternalizingbehavioralproblemswereassessed usingaquestionnaire.TheStrengthandDifficultiesQuestionnaire (Goodman,1997)wasusedtoassessexternalizingbehavior prob-lems(hyperactivityandconductproblems).Thescaleincludes25 items,withthreeansweringcategories(i.e.,nottrue,somewhat trueorcertainlytrue).Forthepurposeofthisstudyweusedthe externalizingsubscaleofthisquestionnaire,whichincludesitems suchas“Iamrestless,overactiveandcannotstaystillforlong”or “Ioftenloosetemper”.
2.2.2. Alcoholuse
Todeterminetheinitiatingofdrinkingandbingedrinking(five ormoreglassesonaday),weaskedparticipantstoindicate,for weekendand weekdays separately,the numberof glasses they consumedonanaveragesingleday(e.g.,“Whenyouconsume alco-holonaweek/weekenddayhowmanyglassesdoyoudrink).For thepurposeofthesurvivalanalysis,thiscontinuousmeasurewas recodedasdichotomousvariable.Theinitiatingoffirstalcoholic drinkwasdefinedasdrinkingatleastonestandardglassof alco-hol(containing12.5mlofpurealcohol)onaweekorweekendday. Participantsreceivedeithera“one”ora“zero”onbothvariables, whichservedasanindicatoroftheoccurrenceoftheevent(i.e., ini-tiatingofdrinkingorbingedrinking;“one”indicatedthattheevent occurred).
2.2.3. Workingmemory
Working memory performance was assessed with the Self OrderedPointingTask(SOPT;PetridesandMilner,1982). Partic-ipantscompleteda concreteversion oftheSOPT.Pictureswere simultaneouslyplaced at different positions onscreen, starting withapracticetrialof4picturesfollowedbyfourtrialswith6, 8,10, and12 pictures, respectively.Thepositionof pictures on screenwasrandomlyshuffledinanumberofvariationsequaltothe amountofpictures.Participantswereaskedtoselecteachpicture oncethroughoutthevariations,butnottoselectthesame posi-tiontwiceinarow.Participantswereencouragedtocompletethe taskwithoutanyerrors.Irrespectiveoftheerrorsmade,all par-ticipantsreceivedthefeedback“welldone”aftereachtrial.With respecttothesecondinstruction,thetaskwasprogrammednotto allowselectingthesamelocationtwiceinarow.Foreachtesttrial, aproportionalerrorscorewascomputedbydividingthenumberof correctresponsesbythenumberoftotalpictureswithineachtrial toaccountfortaskdifficulty(CraggandNation,2007).Thetotal SOPTscorewascalculatedbytakingthemeanoftheproportion ofcorrectscoresofthefourtrials.Higherscoresindicatedbetter workingmemoryfunctioning.
2.2.4. Responseinhibition
ResponseinhibitionwasassessedusingtheStrooptask(Stroop, 1935).TheStrooptask,asameasureofresponseinhibition,has beenusedsuccessfullyasamoderatorinpreviousstudies(Houben andWiers,2009;Peetersetal.,2012).Participantswereinstructed
toindicatethecoloroftheword(i.e.,red,green,blue,oryellow) thatappearedonthescreenbypressingthecorrespondingkeyon thekeyboardwhileignoringthemeaningoftheword.Participants startedwithapracticeblock,whichconsistedof40trialswith sym-bols(e.g.,@@@@or&&&&).Thepracticeblockwasfollowedbya testblockwith28trials.Trialscouldbecongruent(i.e.,meaningof thewordmatchesthecolor),neutral(i.e.,coloredsymbolsinstead ofwords),orincongruent(i.e.,meaningoftheworddiffersfromthe color),andtheywerepresentedinrandomorderbetween partici-pants.Eachtrialwasrepeateduntilacorrectanswerwasgiven.An errormessage,includingadescriptionofthekeysusedandtheir correspondingcolor,followedanincorrectresponse.Aresponse inhibitionscorewascalculatedbysubtractingtheRTsonneutral trialsfromtheRTsonincongruenttrials,withhigherRTs indicat-ingmoreproblemswithcontrol.Foranalyticalpurposes,RTswere dividedby1000.
2.3. Missingdata
Becausewe wanted todeterminewhethera participant ini-tiateddrinkingand/orbingedrinkingduringstudyfollow-up,it wasnecessarytohaveadatasetthatwasascompleteas possi-ble.Missingdata,especiallywhenitinvolvesariskfactororevent, isparticularlyproblematicinsurvivalanalyses(vanBuurenetal., 1999).Multipleimputation(MI)isa commonlyusedmethodto handlemissingdata.PreviousresultsindicatedthatMIisareliable andvalidmethod(Sterneetal.,2009).However,tocheckwhether thiswasalsothecaseforthepresentsample,asimulationstudy wasperformed(performedonthehigh-risksample,whichhadthe largestnumberofmissingdata).Todeterminethebestmethodto handlethemissingdata,severaloptionswerecompared,including listwisedeletion,manualfillinmethods(e.g.,lookingatpreviousor subsequentwave/lookingatmajority/fillinginzerosateach miss-ing),andMI.Wecomparedthefivemethodsontwocriteriathat wererelevantforourstudy:(1)percentageofonsettersthatwould beidentifiedbyeachmethodand(2)thepredictiveeffectoftwo variablescommonlyassociatedwithalcoholuse,namelysensation seekingandimpulsivity.Theresultsrevealedthatmultiple impu-tationwastheoptimalmethodtohandlethemissingdatainthe currentstudy(papersubmittedforpublication,detailed descrip-tionofthesimulationstudycanberequestedfromthefirstauthor). We usedtheprogram MICE(R-packageinR)tocreate five dif-ferentimputationfiles,whichweretransportedtoMplusversion 7(MuthénandMuthén,1998–2010)forsurvivalanalyses.MICE replaces themissing information withplausible values byboth minimizingtheuncertaintyandthebiasofthemodel(vanBuuren etal.,1999).Plausiblevaluesareimputedbasedoncarefully cho-senconfoundingvariablesthatserveaspredictorsofthemissing values.Forthepresentstudy,wecheckedcorrelationmatricesto determinethevariablesthatshouldbeusedtopredictmissingdata. Bothcovariatesandtheoutcomemeasurewereincludedin the imputationmodel,asrecommendedbythedevelopers(vanBuuren andOudshoorn,2000).Forthebinaryvariables,wechosethe logis-ticregressionmethod.Forallothercontinuescovariates,weused thepredictivemeanmatchingmethod.Lifetimealcoholuse,daily smoking,druguse(cannabis,ecstasy,cocaine,hallucinogens), gen-der,age,andpersonality(impulsivity,sensationseeking,anxiety, andhopelessness)wereselectedaspredictorsofmissingness.
2.4. Analyticalprocedure
First,descriptivesfordemographicalinformation,alcoholuse andexecutivefunctioningwerepresentedforthetwosamples sep-arately(mainstreamversusSE,Table1)andfortheonsetandbinge sampleseparately (Table2).Second,thefiveimputeddatafiles werepreparedfor discrete-timesurvival analysis.Sincetheaim
142 M.Peetersetal./DevelopmentalCognitiveNeuroscience16(2015)139–146
Fig.1. Structuralsurvivalmodelwithageindicators(12–17years)andpredictors(i.e.,responseinhibitionandworkingmemory)oftheinitiatingof(binge)drinking.
Table1
Descriptivesforthetwosamples(mainstreamversusspecialeducation)separately.
Mainstream education Special education t-Test Age 13.84(.82) 13.70(.73) t(532)=−1.93 Sex(%boys) 39 88 Hyperactivityproblems(SDQ) 1.62(.46) 1.93(.48) t(501)=10.94* Conductproblems(SDQ) 1.26(.23) 1.60(.38) t(501)=6.72*
Alcoholquantitybaseline .28(1.52) 3.13(7.66) t(503)=4.81*
Workingmemory .80(.09) .73(.10) t(493)=−7.51*
Responseinhibition .07(.22) .21(.35) t(492)=4.89*
SDQ=StrengthandDifficultiesQuestionnaire.
* p<.05.
Table2
Descriptivestatisticsforthetotalsample,theonsetsampleandthebingedrinking sample.
Total(N=534) Onset(N=336) Binge(N=458)
M SD M SD M SD
Agebaseline 13.75 .76 13.69 .77 13.73 .78
Alcoholuse 2.19 6.45 0 0 .35 .83
Responseinhibition .16 .32 .13 .30 .14 .30
Workingmemory .75 .11 .76 .10 .76 .11
Note:Thetotalsamplecontainsallparticipantsfrombothsampleorigins (main-streamandspecialeducation).Theonsetsamplecontainsonlythepartofthetotal samplethatdidnotdrinkatbaseline.Thebingesamplecontainsonlythepartofthe totalsamplethatdidnotbingeatbaseline.
ofthestudywastoexamineexecutivefunctioningasriskfactorfor
initiatingafirstalcoholicdrink,weexcludedalladolescentswho
alreadyconsumedalcoholatbaseline(fortheonsetsample)andall
adolescentswhoalreadyengagedinbingedrinking(drinkingfive
ormoreglasses)atbaseline(forthebingesample).Foreach
ado-lescent,theageoftheonsetandtheageofthefirstbingedrinking
episodewereassessedforeveryhalfayear(e.g.,12,12.5,13,...,17),
resultingin11possibletimepointsatwhichtheeventcouldhave
occurred(seeFig.1).UsingMplusforthediscrete-survivalanalysis,
alatentfactoroftheprobabilitythatanindividualwould experi-encetheeventatacertaintimepoint(i.e.,age)wasestimated.
Survival analyses were conducted using Mplus version 7 (MuthénandMuthén,1998–2010).Thefactorloadingsassessing theprobabilityoftheeventoccurrence(seeFig.1onset/binge)were fixedatone(seeFig.1ageindicators)toascertainthattheeffect ofexecutivefunctioningontheonsetofalcoholuse/bingedrinking wasthesameforeachage.Residualvarianceswerefixedatzero. Wetestedforpossiblesexdifferencesusingmultigroupanalyses. WeusedtheclusteringoptioninMplustoaccountfortheeffectof setting(homeversusschoolassessment).
3. Results
3.1. Descriptivesforseparategroups(specialeducationversus mainstream)
Table1representsthedescriptivestatisticsforadolescentsfrom mainstreamandspecialeducationseparately.Ascanbeseenin Table 1, students in SE education significantly differed onsex, hyperactivity and conduct problems,executive functioning and alcoholusefrommainstreamstudents.Effectsizesfordifference inworkingmemoryandresponseinhibitionwereofmediumsize (Cohen’sdworkingmemory=.53,responseinhibition=.46).
3.2. Descriptivestotalgroup
Table 1 includes descriptive statistics of age and executive functioning at baseline for the total sample and the two ana-lyticalsamples(i.e.,onset andbingedrinking)separately.Small differencesforsumscoresonthetwoexecutivefunctioningtask emerged. We used t-tests to examine whetherpossible differ-ences in executive functioning were found between thegroup whoalreadyengagedindrinkingatbaseline(excludedfromthe study)comparedtoalcoholnaiveadolescentsatbaseline(included inthestudy).Significantdifferencesonexecutivefunctioningat baselineemergedbetweenthetwogroupswithlowerscoresfor workingmemory(M=.72fordrinkersandM=.76foralcoholnaïve adolescents)andhigherscoresforresponseinhibition(indicating relativelyweakerexecutivefunctioningforthedrinkers(working memory:t=3.26,p=.01;responseinhibition:t=−2.36,p=.02).
Figs.2and3representthecummulativeincidenceratesofthe initiating offirst drink(Fig.2)and first bingedrinkingepisode (Fig.3)forthetotalgroupandthenon-(binge)drinkinggroupat baseline.
3.3. Predictionoffirstdrinkandfirstbingedrinkingepisode
Table3showstheresultsofthesurvivalanalysiswithworking memoryandresponse inhibition aspredictors ofthe first alco-holicdrinkandbingedrinkingepisode.Multigroupanalysisfavored themodelin whichwe constrainedsex differencestobeequal
Table3
Oddsratio’sandstandardizedregressioncoefficientsforresponseinhibitionand workingmemorypredictingonsetofdrinkingandbingedrinking.
Onset(N=336) Binge(N=458)
Odds ˇ p Odds ˇ p
Responseinhibition 2.20 .80 .01 1.45 .37 .57
Fig.2. Cumulativeincidenceratesoftheageofonsetforthetotalsampleandtheonsetsampleseparately.
(BICconstrained onset=1338, BIC unconstrained onset=1347;
BICconstrained binge=1645, BICunconstrained binge=1696),
suggesting no significantdifferences in thepredictive effect of
working memory and response inhibition on the initiating of
(binge)drinking.Bothexecutivefunctionswereanalyzedina
mul-tivariatemodeltoexaminetheuniqueinfluenceofeachfunction.
Bothworkingmemoryandresponseinhibitionpredictedthe
initi-atingofthefirstalcoholicdrink.Weakerworkingmemory(ˇ=−.51,
OR=.15,p=.01)andpoorerresponseinhibition(ˇ=.80,OR=3.12,
p=.01,higherscoresindicatepoorerresponseinhibition)increased
thelikelihoodthatadolescentswouldinitiatedrinkingduringstudy
follow-up,indicating anearlier initiating offirstdrinkand first
bingedrinkingepisodeforthoseadolescentswithrelativelyweaker
executivefunctions.
Workingmemory,butnotresponseinhibitionpredictedthe
ini-tiatingofafirstbingedrinkingepisode.Lowerscoresonworking
memory(ˇ=−.08,OR=.33,p=.04)increasedthelikelihoodthat
adolescentswouldinitiatebingedrinkingduringstudyfollow-up.
4. Discussion
Thepresentstudywasoneofthefirsttoexaminethepredictive
effectofexecutivefunctioningontheinitiatingofthefirstalcoholic
drinkandbingedrinkingepisodeamongyoungadolescents,and
thefirsttoexamineadolescentswhowerealcohol-naïveat
base-line.Theresultsindicatedthatrelativelyweakworkingmemory
predictedboththeinitiatingofthefirstalcoholicdrinkandthefirst
bingedrinkingepisode,beyondtheeffectofresponseinhibition.In
addition,relativelypoorresponseinhibitionpredictedthe
initiat-ingofdrinkingbeyondtheeffectofworkingmemory,however,no
effectwasfoundforthepredictionoffirstbingedrinkingepisode.
ParticularlyadolescentsfromSEeducationrevealedrelativelypoor
workingmemoryfunctioningandresponse inhibition,a finding
supportedbypreviousstudies (Barkley, 1997;Pihlet al.,1990;
Niggetal.,2006).Itseemslikelythattheapoorerlevelof exec-utivefunctioning,observedintheseadolescents,placethematrisk foranearlyinitiatingof(binge)drinkingwhicheventuallymight increasetheriskforproblematicalcoholuse,laterinadolescence (KingandChassin,2007).
The findings of this study are in agreement with those of Khuranaand colleagues(2012)whofoundthat executive func-tioning,andmorespecificallyworkingmemory,predictedincrease in frequency of drinkingamong young adolescents.Fernie and colleagues(2013)foundsimilarresults, revealing thatresponse inhibition(andtwoothermeasuresofimpulsivity)predicted alco-holusesixmonthslater.Niggand colleagues(2006)foundthat executivefunctioningpredictedproblemdrinkingbehaviorinhigh risk adolescents (adolescents from alcoholic families). In their study,poorresponseinhibitionatage12–14predictedtheonsetof alcoholrelatedproblemsatage15–17.However,unlikeNiggetal. (2006),wedidnotfindapredictiveeffectofresponseinhibition onbingedrinking.Adifferentsample,adifferenttask,adifferent outcomevariableanddifferentanalyzingtechniqueswereusedin thecurrentstudy,whichmightexplainthedivergentresults.Itis possiblethattheStrooptask,usedinthisstudytoassessresponse inhibition, wasless sensitiveindetectingdifferences compared
144 M.Peetersetal./DevelopmentalCognitiveNeuroscience16(2015)139–146
totheworkingmemorytask,perhapsexplainingwhywedidnot findauniqueeffectofresponseinhibitionontheinitiatingofthe firstbingedrinkingepisode.Inaddition,resultsindicatethat deci-sionmakingisimpairedafteralcoholconsumption.Goodworking memoryfunctioning allowsbetterdecisionmaking.It therefore mightbepossiblethatpoorerworkingmemoryfunctioningimpairs decisionmakingresultinginmoredrinking/bingedrinking(George etal.,2005).
Khuranaand colleagues (2012) found that impulsivity fully mediatedtheeffectofworkingmemoryonthedrinkingbehaviorof adolescents,suggestingthatweaknessesinworkingmemoryaffect behaviorthroughdisinhibitionandimpulsivity.Contrarytowhat Khuranaandcolleagues(2012)found,theresultsofthepresent studyindicatedthatatleasttwoexecutivefunctionsuniquely con-tributedtothepredictionoftheinitiatingofdrinkingbehavior.In addition,inthepresentstudy,workingmemorywasaunique pre-dictorofbingedrinkinginadolescentswhiledisinhibitionwasnot. Thelatterfindingisinagreementwithseveralstudiesthathave foundassociationsbetweenbingedrinkingandworkingmemory functioning(StephensandDuka,2008a;Cregoetal.,2009;Squeglia etal.,2011).However,thesecross-sectionalstudies(Cregoetal., 2009;Squegliaetal.,2011)donotshedlightonthedirectionofthe relation.Althoughtheresultsofthepresentstudydonotruleout areverseeffectofalcoholuseoncognitivefunctioning(e.g., bidi-rectionaleffectcf.Peetersetal.,2014),theresultsdorevealthat someweaknessesinexecutivefunctioningprecedetheinitiating ofdrinkingbehavior.Thecontinueduseofalcoholmayaggravate thepre-existingdeficits(Khuranaetal.,2012;Peetersetal.,2014), causingdelayindevelopmentorevendeclineintheperformance onexecutivefunctioningtasks.
4.1. Limitations
Besidesthestrengthsofthestudy,suchasthelargesample sizeofyoungadolescentsandtheinclusionof ahigh-risk sam-ple,somelimitations shouldbeconsidered.Althoughtheexact samemeasureswiththesameinstructionswereusedinthetwo differentsamples(mainstreamandSEeducation),theassessment procedurewasslightlydifferent.Adolescentsinthehigh-risk sam-plecompletedtasksunder theguidanceof a researchassistant whileadolescentsin themainstreamsample completed assess-mentathome(i.e.,onlineassessment).Forthatreasonweadjusted for clustering effects due to differences in assessment setting. Furthermore,itis possiblethattheexclusion ofdrinkersatthe studybaselinelimitstherepresentativenessofthecurrent sam-plecomparedtonationalaverages.Though,adolescentswhowere excluded fromthe analysis revealed significantworse working memoryfunctioningandpoorerresponseinhibition,whichisin linewithourfindings(anearlyinitiatingofalcoholuseispredicted byrelativelyweakexecutivefunctioning).Thegeneralizabilityof theseresultsis restricteddue tothespecificcharacteristicsthe specialeducationsample(e.g.,externalizingbehavioralproblems). Unfortunately,we couldnot controlfor behavioral disorders in ouranalysisbecauseinformationaboutDSMIVbehavioral disor-derswasnotcollected(onlygeneralandlimitedinformationon externalizingbehaviorwasavailablebymeansoftheSDQ). Nev-ertheless,intheDutcheducationalsetting,approximately5%of thestudentsin secondaryeducationattenda schoolfor special education.Therefore,thesestudentsreflectanimportantpartof theDutchstudentpopulation.Furthermore,multipleimputation hasbeencriticizedasmethodofhandlingmissingdatabecauseit couldaddnoisetothedata(Rubin,1996).Thiscriticismappears toloseitsvaluebecauserecentsophisticatedimputationmethods areabletohandlemissingdatabettercomparedtoolder meth-ods,suchaslistwisedeletion(Rubin,1996;Sterneetal.,2009).In addition,thesimulationstudyinthepresentstudysupportedthis
critique.Moreover,inthepresentstudybingedrinkingwasdefined asdrinkingfiveormoreglassesonaday.Generally,bingedrinking referstodrinkingfiveormoreglassesatoneoccasion(Wechsler andNelson,2001).However,itseemsunlikelythatadolescentsof thisage(12–16years)regularlyhavetheopportunitytodrinkin theafternoonaswellasintheeveningonweekenddays. More-over,bingedrinkersconsumedonaveragealmostnineglasseson abingedrinkingday,whichcanbeinterpretedasheavydrinking forsuchyoungadolescents.Nevertheless,itispossiblethatsome oftheadolescentbingedrinkersinthisstudydidnotconsumeall fiveglassesinaroworatoneoccasion.Arelatedpossiblelimitation ofthestudyisthatalcoholusewasassessedbasedonthe partici-pants’ownindication,withnoexternalcorroborationfromparents orfriends.Thispotentiallyallowedparticipantstooverreportor underreporttheiralcoholuse.Nevertheless,astudybyKoningand colleagues(2010)revealedthatself-reportofalcoholuseisa reli-ablemethodtoassessalcoholconsumptionofadolescents.Lastly, recentstudiessuggestthatrepeatedcyclesofbingedrinkingare associatedwithexecutivedysfunction,andpoorworkingmemory performanceinparticular(Dukaetal.,2004;StephensandDuka, 2008b).Sinceweonlyexaminedthefirstepisodeofbinge drink-ingwewerenotabletolookatthisrelation.Futureresearchcould includenumberofbingeepisodesasimportantcovariateinrelation toexecutivefunctioning.
4.2. Implicationsandconclusion
Thefindingsofthecurrentstudyhaveimplicationsfortheory andforprevention.First,tothebestofourknowledgethisstudyis oneofthefirsttodemonstratethatdeficitsinexecutive function-ingprecedetheinitiatingofdrinkingamongadolescents.Previous studieshave foundstrongindications for executivefunctioning beingariskfactor foralcoholuseamongadolescents,however, thedesignofthesestudiespreventedtoderivestronginferences aboutdeficitsinexecutivefunctioningprecedingtheactualonsetof drinkingbehavior(seePeetersetal.,2014,foranoverview).Second, severalclinicalstudieshavefoundcognitivedeficitsafterheavyand prolongedalcoholuse(Hansonetal.,2011;Tapertetal.,2002).It ispossiblethatsomeofthesefounddeficitswerealreadypresent beforedrinkingbehaviorwasinitiated,andamagnifiedandbiased effectofalcoholonadolescents’cognitivefunctioningmayarise. Itshouldbenoted,however,thatthesestudiesexcluded adoles-centswithanexternalizingbehavioraldisorder(conductdisorder, ADHD),whilethecurrentstudyincludedadolescentswith exter-nalizingbehavioralproblems.Inaddition,deficitshavebeenfound forawiderangeofcognitivefunctions(e.g.,attention,visuospatial functioning),andalcoholmightaffectspecificpartsofthe adoles-centbraindifferently.Furtherresearchisneededtospecifywhich cognitivefunctionsaresusceptibletoheavydrinkingandwhich functionsaremainlyofinterestinpredictingthedrinkingonsetof adolescents.
Withrespecttoprevention,thefindingsofthepresentstudy confirmtheimportanceofearlyinterventions.Ithasbeen demon-strated thatexecutive functionsmoderate theeffectof implicit cognitivemotivationalprocessesonalcoholandsubstanceusein adolescents(Grenardetal.,2008;Peetersetal.,2012;Thushetal., 2008).Astheseprocesses getstronger withincreaseddrinking, delayoftheonsetofdrinkingappearstobeagoodgeneralstrategy topreventproblematicalcoholuseinadolescents(Koningetal., 2009,2011).Assomeadolescentsappeartobeatagreaterriskfor anearlyonsetofdrinking,additionaltargetedpreventionmight bewarrantedas well(cf.Conrodet al.,2008).Recently several promisinginterventionshavebeenintroducedtoincreaseresponse inhibition(Houbenetal.,2011)andworkingmemory(Klingberg etal.,2005;Dovisetal.,2012)inadolescentsandyoungadults.
Thesetrainingmethodscontributetoanincreaseinexecutive con-trol,andtheymighteventuallypostponetheageoftheonset.
Thefindingsofthisstudydemonstratethatpre-existingdeficits inexecutivefunctioningpredicttheinitiatingofthefirstalcoholic drinkandfirstbingedrinkingepisodeamongyoungadolescents. The results suggest that relatively weakworking memory and disinhibitionarerisk factorsfor theearlyinitiating of drinking. Moreover,weakworkingmemoryfunctioningisariskfactorfor bingedrinking.Acontinuedheavydrinkingpatternmightfurther worsenexecutivefunctioning(Squegliaetal.,2009;Tapertetal., 2002), beyondthese pre-existingeffects. Futureresearch could benefitfromdisentanglingcognitivedeficitsinducedbyalcoholuse fromcognitivedeficitsthatpredictalcoholuse,withthecurrent findingsprovidingafirstmodeststep.
Conflictofinterest
Theauthorsdeclarenoconflictofinterest.
Acknowledgements
ThisstudywassupportedbytheDutchHealthCareResearch Organization(ZON-Mw;60-600-97-172)andaVicigrant 453-08-001fromtheDutchNationalScienceFoundation(N.W.O.)awarded toprof.Dr.ReinoutW.Wiers.
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