Visual working memory continues to develop through ...
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The capacity of visual working memory (VWM) refers to the amount of visual information that can be maintained in mind at once, ... DownloadArticle DownloadPDF ReadCube EPUB XML(NLM) totalviews ViewArticleImpact SHAREON Abstract Introduction Experiment1 Experiment2 GeneralDiscussion ConflictofInterestStatement Acknowledgments References Peoplealsolookedat ORIGINALRESEARCHarticle Front.Psychol.,27May2015Sec.DevelopmentalPsychology https://doi.org/10.3389/fpsyg.2015.00696 Visualworkingmemorycontinuestodevelopthroughadolescence ElifIsbell1*,KeisukeFukuda2,HelenJ.Neville1andEdwardK.Vogel1 1DepartmentofPsychology,UniversityofOregon,Eugene,OR,USA 2DepartmentofPsychology,VanderbiltUniversity,Nashville,TN,USA Thecapacityofvisualworkingmemory(VWM)referstotheamountofvisualinformationthatcanbemaintainedinmindatonce,readilyaccessibleforongoingtasks.Inhealthyyoungadults,thecapacitylimitofVWMcorrespondstoaboutthreesimpleobjects.WhilesomeresearchersarguedthatVWMcapacitybecomesadult-likeinearlyyearsoflife,othersclaimedthatthecapacityofVWMcontinuestodevelopbeyondmiddlechildhood.HereweassessedwhetherVWMcapacityreachesadultlevelsinadolescence.Usinganadaptationofthevisualchangedetectiontask,wemeasuredVWMcapacityestimatesin13-year-olds,16-year-olds,andyoungadults.Wetestedwhetherthecapacityestimatesobservedinearlyorlateryearsofadolescencewerecomparabletotheestimatesobtainedfromadults.OurresultsdemonstratedthatthecapacityofVWMcontinuestodevelopthroughoutadolescence,notreachingadultlevelsevenin16-year-olds.ThesefindingssuggestthatVWMcapacitydisplaysaprolongeddevelopment,similartotheprotractedtrajectoriesobservedinvariousotheraspectsofcognition. Introduction Thecapacityofvisualworkingmemory(VWM)referstotheamountofvisualinformationthatcanbemaintainedinthemindatonce,readilyavailableforrapidaccess(LuckandVogel,2013).IthasbeendemonstratedthatthecapacityofVWMishighlylimited(LuckandVogel,1997;VogelandMachizawa,2004;XuandChun,2006;Awhetal.,2007;ZhangandLuck,2008).Whenprocessingstrategiesarepreventedorcontrolledinyoungadults,thecapacitylimitofVWMcorrespondstoaboutthreesimpleobjects(Pashler,1988;LuckandVogel,1997;Cowan,2001).ElectrophysiologicalandfunctionalmagneticresonanceimagingstudiesprovidefurtherevidenceforsuchlimitedcapacityinVWM(ToddandMarois,2004;VogelandMachizawa,2004).Theestimatesofsuchdiscretecapacitylimitsdiffermarkedlyacrossindividuals(VogelandMachizawa,2004;Rouderetal.,2008).Thesecapacityestimatesstronglypredictfluidintelligenceinadults(Cowanetal.,2005,2006;Fukudaetal.,2010;Unsworthetal.,2014).Furthermore,theVWMcapacityyieldshighcorrelationswithbothintelligenceandaptitudemeasuresinchildren(Cowanetal.,2005,2006).Understandingthedevelopmentofthiscognitiveassetcanshedlightonbothhowsuchcapacitylimitsemergeandhowindividualdifferencesincrucialaspectsofcognitionunfold. WhilesuperiorperformanceinVWMtaskshasbeenassociatedwithfavorablecognitiveandeducationaloutcomes,deficitsinVWMhavebeenobservedinlearningdisabilitiesinreading(Reiteretal.,2005;Gathercoleetal.,2006;WangandGathercole,2013)andmathematics(McLeanandHitch,1999;Ashkenazietal.,2013;Szucsetal.,2013).Inaddition,VWMdeficitshavebeendocumentedinawidespectrumofdisorders,suchasattentiondeficitandhyperactivitydisorders(Martinussenetal.,2005;Lenartowiczetal.,2014)andschizophrenia(Goldman-Rakic,1994;Silveretal.,2003;LeeandPark,2005).CharacterizingthetypicaldevelopmentaltrajectoryofVWMcapacitylimitscanguidetrainingandinterventioneffortsthattargetatypicalpopulationsinwhichVWMdeficitsarecommon.ProfilingwhenandhowVWMcapacitymaturescaninformusaboutwhentheplasticityofVWMislesslikelytobeconstrainedduetomaturationandthesensitiveperiodsduringwhichtrainingandinterventioneffortsaremorelikelytobeeffective. SeveralstudiesfocusedoninvestigatingthetypicaldevelopmentaltrajectoryofVWMcapacity.Oneofthecommonparadigmsusedinthesedevelopmentalstudiesisthevisualchangedetectiontask(LuckandVogel,1997).Inthistask,participantsarebrieflypresentedwithasamplearrayofobjectsoneachtrial.Followingashortretentionperiod,atestarrayispresentedandparticipantsareaskedtojudgewhetherthesamplearrayandthetestarrayareidenticalordifferinonesingleitem.Theperformanceonthesechange-detectionjudgmentsisthenusedtodeterminethenumberofitemsthatcanbeheldinVWM,orinotherwords,anindividual’sVWMcapacity. VariantsofthisparadigmwereemployedininfantstudiestoinvestigatethedevelopmentofVWMduringthefirstyearoflife(Ross-Sheehyetal.,2003,2011;Oakesetal.,2006).Forinstance,Ross-Sheehyetal.(2003)usedalookingpreferenceparadigmtoexploreVWMcapacityininfants.Infantswerepresentedwithtwosimultaneousdisplaysofitems,onewiththesameitemsstreaming,andtheotherwithonerandomitemchangingateachdisplay.LookingpreferencesofinfantsweremeasuredwiththeassumptionthatinfantswouldshowpreferencesforthechangingdisplaysaslongasthenumberofitemsonthedisplayswaswithinornearthecapacityoftheirVWM.Four-and6.5-month-oldinfantswerereportedtodetectchangesonlyatdisplayswithoneitem,whileinfantsasyoungas10monthsofagewerefoundtopreferlookingatchangingdisplaysthatcontaineduptofouritems,butnotsixitems.Basedonthisfinding,itwasconcludedthatinfantsreachedalmostanadult-likeVWMcapacitybytheendofthefirstyear.Employingsimilartasks,Oakesetal.(2006)reportedthateven7.5-month-oldswereabletodetectchangesofcolor-locationcombinationsinarraysofthreeobjects.TogethertheseresultsimplyarapiddevelopmentinstoringmultipleobjectsinVWMduringthefirstyearoflife. However,contrarytotheassertionsthatVWMcapacitydevelopsrapidlytotheextentthatitreachesalmostadultlevelsininfancy,severalstudiesarguedamoreprotracteddevelopment,continuingatleastthroughchildhood.Forinstance,inastudywithanadaptationofthechangedetectiontaskforyoungchildren,3-and4-year-oldchildrenhadlowerVWMcapacityestimatescomparedto5-and7-year-oldchildren,and5-year-oldsperformedsignificantlyworsethan7-year-olds(Simmering,2012).Inasimilarlineofwork,5-year-oldswerefoundtodisplaylowercapacityestimatesthan10-year-oldsacrossvarioussetsizes(Riggsetal.,2006).TheseresultssuggestthatVWMcapacitycontinuestoexpandatleastduringearlychildhoodandcontradicttheclaimsthatVWMcapacitybecomesadult-likeininfancy. Furthermore,whileRiggsetal.(2006)arguedthatVWMcapacityreachedadultlevelsofthreetofouritemsat10yearsofage,otherstudiesreportedlowercapacityestimatesfor10-year-oldscomparedtoadults(Cowanetal.,2006;Riggsetal.,2011).Similarly,inastudycomparing10-to12-year-oldchildrentoyoungerandolderadults,childrendisplayedhighercapacityestimatesthanolderadultsonlywhentheencodingtimeswereshort,butconsistentlyshowedlowercapacityestimatesthanyoungadults(Sanderetal.,2011).Moreover,inacross-sectionalstudy,Cowanetal.(2005)foundlowerVWMcapacityinsixth-gradechildrencomparedtoadults.Inlinewiththesefindings,12-to16-year-oldsadolescentswereshowntohavelowercapacityestimatesthanadultsinachangedetectiontaskwhenthreetargetitemswerepresent(Spronketal.,2012).Likewise,inastudythatassessedVWMperformanceinalargesampleofindividualsbetweentheagesof8and75,apeakinVWMperformancewasreportedaroundage20(BrockmoleandLogie,2013).SuchconvergingevidencefromindependentstudiessuggeststhatVWMcapacityisnotadult-likeinchildhoodandimpliesongoingdevelopmentatleastduringtheearlyyearsofadolescence. Inthepresentstudy,weinvestigatedwhetherVWMcapacityshowsaprotracteddevelopment,extendingfromadolescenceintoadulthood.Adolescenceisatimeperiodduringwhichthebrainexhibitstremendousstructuralchanges(Raznahanetal.,2011).Thecorticalregionsthatareinvolvedinworkingmemoryprocessessuchastheparietalcortexandprefrontalcortex(CurtisandD’Esposito,2003;ToddandMarois,2004)displaymaturationalchangesacrossadolescence(Gieddetal.,1999;LebelandBeaulieu,2011).Especiallytheprefrontalcortexdisplayschangesinvariousfeatures,suchasthecorticalthickness(Sowelletal.,2004;LenrootandGiedd,2006),graymatterdensity(Sowelletal.,2001),andwhitematteranisotropy(Nagyetal.,2004;Barnea-Goralyetal.,2005;Mabbottetal.,2006)wellintoadulthood.Basedonthesefindingsofprolongedbraindevelopmentinadolescence,weexpectedtoobserveimmatureprofilesofVWMinadolescentsascomparedtoadults.Usinganadaptationofthevisualchangedetectiontask(LuckandVogel,1997),withsetsizes2,4,and6,wetestedwhetherthecapacityestimatesobtainedinearlyorlateryearsofadolescencewerecomparabletotheestimatesattainedfromadults. Experiment1 Introduction ToinvestigatewhetherVWMcapacityreachesadultlevelsinearlyorlateryearsofadolescence,werecruited13-and16-year-oldparticipants.Cowanetal.(2005)demonstratedthatsixthgradechildren,rangingfrom11to13yearsofage,didnothavecapacityestimatesashighasadults.Similarly,comparedtoadults,12-to16-year-oldadolescentshadlowercapacityestimateswhenpresentedwiththreeitems(Spronketal.,2012).Expectingtoreplicatethesefindings,weanticipatedobtaininglowercapacityestimatesfrom13-year-oldscomparedtoadults.Moreover,basedontheongoingbraindevelopmentthroughoutadolescenceinregionsassociatedwithWM,weexpectedtoobservelowercapacityestimatesalsoin16-year-oldscomparedtoadults. Method Participants AdolescentparticipantswererecruitedviathedevelopmentaldatabaseoftheUniversityofOregon.Alladolescentparticipantsweremiddleschoolandhighschoolstudents,attendingavarietyofschoolsinEugene,Oregon.Parentswereinterviewedoverthephonetoensuretheirchildrenhadnormalorcorrected-to-normalvisionandweretypicallydevelopingindividualswithnoneurologicaldisorders,developmentaldelays,ADD/ADHD,learningdisabilities,visualtrackingproblems,colorblindness,depressionoranxiety,andhadneverusedanypsychotropicdrugs. AdultparticipantswererecruitedviaflyersfromtheUniversityofOregon.Alladultparticipantswerestudentsattheuniversity.Priortoparticipation,theywereinterviewedtoensurethattheymetallthecriteriathatwereusedtorecruitadolescentparticipants. Thesampleincludedthreeagegroups:twenty-two13-year-olds(M=13.49years;SD=0.30;13females),twenty-two16-year-olds(M=16.58years,SD=0.34;10females),and23adults(M=20.89years,SD=1.32;14females).One13-year-oldparticipantwasnotincludedinthisfinalsampleforperformingbelowchanceathighersetsizes,suggestingahighlikelihoodthatthisparticipantwasnotfullyengagedinthetask. Maternaleducationlevelswerecomparedasaproxyforsocio-economicstatus(SES).Themeanmaternaleducationlevelcorrespondedto“completedsomecollegeclasses”acrosstheagegroups,whichistheequivalentofsomeeducationbeyond12thgradeandattendancetoanypost-secondaryinstitutionintheUnitedStates.Nodifferencesinmaternaleducationwereobservedbetweengroups[F(2,63)=0.85,p=0.43]. ThestudywasconductedwiththeapprovaloftheUniversityofOregonInstitutionalReviewBoard.Writtenassentwasobtainedfromallparticipantsunder18yearsofage,andtheirparentssignedaconsentformfortheirchildren.Participantsolderthan18yearsofagesignedaconsentformtoparticipate.Allparticipantswerepaidfortheirtime. StimuliandProcedure ThetaskwasamodificationofthechangedetectionparadigmusedinLuckandVogel(1997).Stimuliconsistedofcoloredsquares(0.65°×0.65°)superimposedonstickfigures,introducedtotheparticipantsaschildrenwearingcoloredshirts.Eachcoloredsquarewasselectedatrandomfromasetofninecolors(red,pink,violet,blue,green,yellow,orange,brown,andblack).Agivencolordidnotappearmorethanoncewithinanarray.Thememoryarraysincludedsetsizesof2,4,or6stimuli.Theitemsinagivenarraywereseparatedbyatleast3°fromthecenterofeachsquaretothecenteroftheother.Thepositionsofthestimuliwererandomizedoneachtrialtoappearwithina9.8°×7.3°regiononamonitorwithagraybackground,ataviewingdistanceof75cm.Afixationcrosswaspresentedatthecenterofthescreenthroughoutthestudy. Oneachtrial,thefirstarrayofstimuli(thememoryarray)waspresentedfor150ms,followedbya900msblankretentioninterval.ExamplestimuliareshowninFigure1.Aftertheretentioninterval,onlyoneobjectreappearedonthescreen.Inhalfofthetrials,thisobjectwasidenticaltotheobjectthatappearedinthesamelocationwithinthememoryarray.Intheotherhalfofthetrials,theobjectwasadifferentcolorfromtheobjectthatappearedinthesamelocationbefore.Thiswasalwaysanewcolor,notpresentedelsewhereinthedisplaywithinthememoryarray.Participantswereinformedthatineachtrialagroupofchildrenwearingdifferentcoloredshirtsweregoingtocomeuponthescreen,disappearbriefly,andthenonlyonechildwouldcomebacktothescreen,intheexactlocationhewasbefore.Theywereaskedtoindicatewhetherthechildwaswearingthesameshirtorhadchangedhisshirt.Theparticipantsindicatedtheirresponsesusingtheleftandrighttriggersofavideogamecontroller,whichweremarkedas“same”and“change”respectively.Thetestitemremainedonthescreenuntilaresponsewasmade. FIGURE1 Figure1.Examplestimulusdisplays(notdrawntoscale)fora“changetrial”ofsetsize2. Apracticeblockwasadministeredbeforethemaintasktodemonstratethetasktoparticipantsandallowthemtogetmorecomfortableusingtheinterface.Thepracticeblockconsistedofsixtrialsofsetsize2,followedbysixtrialsofsetsize4.Ifaparticipantperformedbelow66%accuracyforeithersetsize,thepracticeblockwasrepeated.Noparticipanthadtorepeatthepracticeblockmorethantwice.Theexperimentconsistedof80trialsofeachsetsizepresentedrandomly,foratotalof240trials.Participantswereofferedabreakevery80trials.Theexperimenttookapproximately12mintocomplete. DataAnalysis VisualworkingmemorycapacitywascalculatedasK=S(H–F),whereKistheVWMcapacity,Sisthesetsizeofthevisualarray,Histhehitrate,andFisthefalsealarmrate(Cowan,2001).UnivariateANOVAswereusedtoexaminetheomnibuseffectsofage.Plannedcontrastswereemployedtocomparethe13-year-oldsversusadults,and16-year-oldsversusadults.Forallplannedcontrastswithp<0.05,Cohen’sd(Cohen,1977;Rosnowetal.,2000)wasreportedasthemeasureofeffectsize. ResultsandDiscussion Capacityestimatesobtainedfromthesetsize2conditionresultedinapotentialunderestimation(i.e.,K<2.00)ofVWMcapacity(Rouderetal.,2008).Nevertheless,todemonstratethatourresultsdidnotdependontheexclusionofthiscondition,wefirstconductedallanalysesincludingthesetsize2conditioninthegrandaveragesofK.MeansandstandarddeviationsofKestimatesarereportedinTable1. TABLE1 Table1.DescriptivesofVWMcapacity(K)estimatesforthethreeagegroupsinExperiment1. TherewasasignificanteffectofageonKestimatesobtainedasanaveragefromallsetsizes,F(2,64)=11.68,p<0.001,ηp2=0.27.Plannedcontrastsrevealedthatthe13-year-oldshadlowerestimatesthanadults,t(64)=–4.86,p<0.001,d=–1.42.Critically,16-year-oldswerealsofoundtoperformworsethanadults,t(64)=–2.20,p=0.031,d=–0.78.However,sincethesetsize2conditionloweredtheKestimatesforeachgroupandthedirectionoftheresultsdidnotappeartodependontheinclusionofthiscondition,weexcludedthisconditioninasecondanalysisoftheeffectofageonoverallK.TheKestimatesobtainedasanaverageofthesetsize4andsetsize6conditionsforthethreeagegroupsareillustratedinFigure2. FIGURE2 Figure2.MeansandstandarderrorsoftheaverageVWMcapacity(K)estimatescomputedbasedonsetsizes4and6forthethreeagegroupsinExperiment1.*p<0.05;**p<0.001. FortheKestimatesexcludingthesetsize2condition,therewasagainasignificanteffectofageonperformance,F(2,64)=11.41,p<0.001,ηp2=0.26.Consistentwiththepreviousfindings,plannedcontrastsrevealedthatboth13-and16-year-oldshadlowerVWMcapacityestimatesthanadults[t(64)=–4.77,p<0.001,d=–1.40,andt(64)=–2.19,p=0.032,d=–0.76,respectively]. Replicatingpreviousfindingswithyoungadolescents(Cowanetal.,2006;Spronketal.,2012),thisexperimentdemonstratedthat13-year-oldsdonothaveadult-likeVWMcapacityestimates.Expandingonthesefindings,thisexperimentalsoshowedthateven16-year-oldshavelowercapacityestimatesthanadults.TheseresultssuggestthatVWMcapacitydoesnotreachadultlevelsinadolescence. Experiment2 Introduction Experiment1providedconfirmatoryevidencethattheestimatesofVWMcapacitydonotreachadultlevelsinearlyadolescence,andthefirstevidencethattheymaynotreachadultlevelseveninlateadolescence.TheseresultscontradicttheclaimsthatVWMcapacityreachesadult-levelsduringearlyyearsoflife.However,itispossiblethatthediscrepancyoffindingsbetweenthesestudiesisatleastpartiallydrivenbydifferencesinthedurationofmemoryarrays.InthestudiesthatclaimedtheVWMcapacityreachedadultlevelsinearlyyearsoflife(Ross-Sheehyetal.,2003;Riggsetal.,2006),thememoryarrayswerepresentedfor500ms.However,wepresentedthememoryarraysfor150msinExperiment1.Toruleoutthepossibilitythatthepoorerperformanceoftheadolescentswasmainlydrivenbyalackofsufficientexposuretothememoryarray,inExperiment2,wepresentedthememoryarraysforbothshortandlongerdurations. TherearecontradictoryfindingsontheeffectsofincreasedpresentationtimeonVWMperformance.Inastudywithyoungadults,increasingthedurationofthememoryarrayfrom100to500mswasnotfoundtoimproveVWMperformance(Vogeletal.,2001).Onthecontrary,inastudythatcomparedtheVWMperformanceinchildren,youngeradults,andolderadults,performancewasfoundtoincreasefrom100to500ms(butnotfrom500to1000ms)forallagegroups(Sanderetal.,2011). Inthisexperiment,weexploredtheeffectsofthedurationofthememoryarrayonVWMinadolescentsandadults.WeaimedtoreplicatethefindingsofExperiment1andalsodetermine(a)whethertheadolescentsbenefitedmorethanadultsfromlongerexposuretimes;and(b)whethertheincreaseinexposuretothememoryarraywassufficienttoeliminatetheagedifferencesinperformanceobservedinthefirstexperiment.InordertoexaminetheeffectsofexposuretimeontheVWMperformanceofadolescentsandadults,wepresentedtheparticipantswithmemoryarraydurationsof150,500,and1000ms,randomlypresentedacrosstrials.Wedidnotuseapresentationtimelongerthan1000mstopreventtheuseofverbalencodingduringmemoryarrays. AnadditionalstrengthofExperiment2,relativetoExperiment1,istheuseofamorepowerfulstatisticaltechnique,multilevelmodeling(MLM),toanalyzethedata.Multilevelmodelingisappropriateinthiscasebecauseourdataarestructuredasresponseswithinindividuals,withdurationasawithin-personindependentvariableandageasabetween-personindependentvariable.Typicallytheclusteringofresponseswithindividualsinrepeated-measuresdesignisaddressedbyaveragingtheresponsesbutthisapproachdiscardspotentiallymeaningfulvariabilityatthewithin-personlevel.Here,MLMallowsustoanalyzeallresponsesforalldurationsandallparticipantsinasingle,powerfulmodel. Method Participants Thefinalsampleincludedtwenty-nine13-year-olds(M=13.41years,SD=0.25;14females),twenty-eight16-year-olds(M=16.48years,SD=0.29;15females),and32adults(M=20.58years,SD=2.09;15females).Allparticipantshadnormalorcorrected-to-normalvisionandweretypicallydevelopingindividualswithnoneurologicaldisorders,ADD/ADHD,learningdisabilities,colorblindness,orvisualtrackingproblems.Alladolescentparticipantsweremiddleschoolandhighschoolstudents,attendingavarietyofschoolsinEugene,Oregon.AlladultparticipantswereUniversityofOregonundergraduates.One13-year-oldparticipantandone16-year-oldparticipantwerenotincludedinthisfinalsampleforperformingbelowchanceathighersetsizes,suggestingthattheseparticipantswerenotfullyengagedinthetask. MaternaleducationlevelswerecomparedasaproxyforSESandnodifferenceswereobservedbetweengroups[F(2,78)=0.52,p=0.60].Theaveragematernaleducationlevelcorrespondedto“completedsomecollegeclasses”acrossagegroups. ThestudywasconductedwiththeapprovaloftheUniversityofOregonInstitutionalReviewBoard.Writtenassentwasobtainedfromallparticipantsunder18yearsofage,andtheirparentssignedaconsentformfortheirchildren.Participantsolderthan18yearsofagesignedaconsentformtoparticipate.Allparticipantswerepaidfortheirtime. StimuliandProcedure TheparadigmdescribedinExperiment1wasmodifiedtoinvestigatetheeffectsofmemoryarraydurationonperformance.Asinthefirstexperiment,thememoryarraysconsistedof2,4,or6itemsondisplay.InExperiment1,Kestimatesfromthesetsize2conditionwasfoundtolowertheoverallcapacityestimatesbutthedirectionoftheresultsdidnotappeartodependontheinclusionofthiscondition.Wekeptthesetsize2conditionintheexperimenttoparallelthedesignfromExperiment1ascloselyaspossible.Thememoryarrayswerepresentedfor150,500,or1000ms.Theexperimentconsistedof120trialsofeachpresentationtime,withboththesetsizesandmemoryarraydurationsrandomizedacrosstrials.Therewereatotalof360trials.Participantswereofferedabreakevery90trials,withapotentialoftakingthreebreaksduringthestudy.Theexperimenttookapproximately20mintocomplete. DataAnalysis Responsetimedataareclusteredwithinsubjectsinthesensethatobservationsfromthesameparticipantaremorehighlycorrelatedwitheachotherthanobservationsfromdifferentparticipants.Thisviolatesthegenerallinearmodelassumptionofindependenceoferrorsattheresponselevel.MLMexplicitlyaddressesthisissuebyseparatelyestimatingthewithin-andbetween-subjecterrorundertheassumptionthatwithin-subjectobservationsarenotindependent(Garson,2013).Accordingly,weusedMLMwithVWMcapacityestimatesnestedinindividualsforthisrepeatedmeasuresdesign.ThemultilevelmodelwasanalyzedwithHierarchicalLinearModeling(HLM)software(RaudenbushandBryk,2002).Thewithin-personpredictor,whichwasduration,wasenteredatLevel1,andthebetween-personpredictor,agegroup,wasenteredatLevel2.Weusedanunstructuredvariance/covariancematrixtoallowforheterogeneouserrorsacrossagegroups.Exposuretimewascenteredat150ms,anddummycodeswereusedtocompare13-year-oldstoadultsaswellas16-year-oldstoadults.Thefollowingmodelwasusedwheretheinterceptandtheslopeswereallowedtovaryrandomly. Level 1:Reponseij=β0i+β1i TIMEij+eijLevel 2:β0i=γ00+γ01*(Early Adolescence)+γ02*(Late Adolescence)+u0iβ1i=γ10+γ11*(Early Adolescence)+γ12*(Late Adolescence)+u1i Inthismodel,Responseijispredictedbyalinearfunctionofexposuretime(TIMEij)fortheVWMcapacityestimateofindividualiatoccasionj.Theintercept(β0i)representstheindividuali’sVWMcapacityestimateat150ms.Theslope(β1i)representstheeffectofexposuretimeonanindividual’sVWMcapacityestimate.ThismultilevelmodelallowedustotestforreplicationofthefindingsfromExperiment1at150ms(theparametersintheβ0equation),andadditionally,whethertherewasamaineffectofexposuretime(γ10)andiftheagegroupsdifferentiallybenefitedfromlongerexposuretothememoryarrays(γ11andγ12).Cohen’sd(Cohen,1977;Rosnowetal.,2000)isreportedforthecomparisonofthedummy-codedgroupsattheintercept(150ms). ResultsandDiscussion MeansandstandarddeviationsofKestimatesarereportedinTable2,separatelyforsetsize4,setsize6,andtheaverageoftheKestimatesfromsetsize4andsetsize6.TheaverageKestimatesforthethreeagegroupsacrossexposureconditionsareillustratedinFigure3. TABLE2 Table2.DescriptivesofVWMcapacity(K)estimatesacrossexposureconditionsinExperiment2. FIGURE3 Figure3.MeansandstandarderrorsoftheVWMcapacity(K)estimatescomputedbasedonsetsizes4and6forthethreeagegroupsacrossexposureconditionsinExperiment2. Althoughthecapacityestimatesobtainedfromthesetsize2conditionresultsinunderestimationofVWMcapacity,todemonstratethatourresultsdidnotdependontheexclusionofthiscondition,onceagainwefirstconductedallanalysesincludingthesetsize2conditioninthegrandaveragesofK. ReplicatingtheresultsfromExperiment1,at150msexposuretimethe13-year-oldsperformedworsethanadults,t(86)=–3.92,p<0.001,d=–1.15.Similarly,inthisshortestdurationcondition,16-year-oldsalsoperformedworsethanadults,t(86)=–2.31,p=0.023,d=–0.57.DurationofthememoryarraydidnothaveasignificanteffectontheincreaseinVWMcapacityinadults,t(86)=1.54,p=0.12.TherewasasignificantdifferenceintherateofincreaseinVWMcapacitybetween13-year-oldsandadults,t(86)=2.31,p=0.023.Therateofincreaseincapacityoverexposuretimedidnotdifferbetween16-year-oldsandadults,t(86)=1.13,p=0.26. Similarly,fortheKestimatesexcludingthesetsize2condition,at150msexposuretimeadultshadhighercapacityestimatesthanboththe13-year-olds[t(86)=3.86,p<0.001,d=1.14]andthe16-year-olds[t(86)=2.50,p=0.015,d=0.56]. AlsofortheKestimatesexcludingthesetsize2condition,durationofthememoryarraydidnothaveasignificanteffectontheincreaseinVWMcapacityinadults,t(86)=1.71,p=0.090.Unliketheanalysesthatincludedsetsize2condition,thedifferenceintherateofincreaseinVWMcapacitybetween13-year-oldsandadultsdidnotreachsignificanceatthep<0.05level,butwasveryclosetothisalphacut-off,t(86)=1.97,p=0.051.Therateofincreaseincapacityoverpresentationtimedidnotdifferbetween16-year-oldsandadults,t(86)=1.31,p=0.19. Totestwhether16-year-oldsperformedworsethanadultsevenatthelongestpresentationcondition,fortheKestimatesexcludingthesetsize2conditionwhichresultsinunderestimationofcapacity,asubsequentmodelwasrun,onceagainwithheterogeneouserrorterms.Tohaveaparsimoniousmodel,astherateofincreaseinVWMoverpresentationtimedidnotdiffersignificantlybetweenthe16-year-oldsandadults,agegroupwasincludedonlyasapredictorofthecapacityestimatesat1000ms,butnotasapredictoroftherateofdecreaseincapacity.Thismodelrevealedthatevenat1000ms,16-year-oldsperformedworsethanadults,t(58)=–2.20,p=0.032,d=–0.41. WhileVogeletal.(2001)reportednoimprovementincapacityfrom100to500msinyoungadults,Sanderetal.(2011)foundanincreaseincapacityfor10-year-olds,youngadults,andolderadultsfrom100to500ms,butnotfrom500to1000ms.Inthisexperiment,wedidnotfindasignificanteffectofexposuretimeforyoungadults.However,aninterestingpatternfortheslopeofincreaseincapacitywasobservedwhentheyoungerandolderadolescentswerecomparedtotheadults.AsshowninFigure3,13-year-oldsshowedthegreatestrateofimprovementincapacitywithlongerexposuretothememoryarray.Youngeradolescentsappearedtobenefitdifferentiallyfromlongerexposuretimethanolderparticipants,whodidnotseemtobenefitmuchfromanincreaseinthedurationofthememoryarray.Thesefindingsimplythatdifferentfactorsaccountforwhyyoungeradolescentsdonotperformatadultlevelsascomparedtoolderadolescents.ItispossiblethatanimmatureprofileinidentifyingandtransferringperceptualrepresentationsintoVWMpartiallyaccountsforthepoorerperformanceofyoungeradolescents,whileolderadolescentsdonotdisplaysuchanimmaturityinencodingprocesses.Inaddition,thematurationlevelsofcorticalstructuresthatshowatemporalactivationprofilenotaccountedforbyperceptualorgeneralattentioneffects,suchastheinferiorfrontaljunctioninthelateralprefrontalcortex(Toddetal.,2011),mayaccountforwhyyoungeradolescentsdifferentiallybenefitfromlongerexposuretothememoryarrays. Despitedifferentiallybenefitingfromlongerexposuretothememoryarray,bothyoungerandolderadolescentsstillperformedworsethanyoungadults.LongerexposuretothememoryarraydiminishedbutdidnoteliminatetheagedifferencesinVWMcapacityobservedinExperiment1.ThesefindingssuggestthatthecapacitydifferencesobservedbetweenadolescentsandadultsinExperiment1werenotdrivensolelybyshortpresentationtimesandsupportthehypothesisthatVWMcapacityhasaprolongeddevelopmentaltrajectory. GeneralDiscussion ThepresentstudyinvestigatedwhetherVWMcapacitycontinuestodevelopthroughadolescenceintoadulthood.Overall,ourresultsdemonstratedthatthecapacityofVWMdoesnotreachadultlevelseitherinearlierorlateryearsofadolescence.Regardlessofwhetherthememoryarraywaspresentedbrieflyorforlongerdurations,neitheryoungernorolderadolescentsdisplayedadult-likecapacityestimates.Ourfindingsareconsistentwithpreviousstudiesthatdemonstratedlowercapacityestimatesinearlyyearsofadolescencecomparedtoadulthood(Cowanetal.,2005;Spronketal.,2012).Hereweextendthesefindingstolateryearsofadolescence,inlinewiththeclaimthatVWMperformanceimprovesthroughoutadolescence(BrockmoleandLogie,2013). OurresultscontradicttheassertionsthatvisualWMcapacityreachesadultlevelsininfancy(Ross-Sheehyetal.,2003;OakesandLuck,2014)ormiddlechildhood(Riggsetal.,2006).ItispossiblethatVWMcapacitydoesnotdevelopinalinearfashion,butratherfollowsaU-shapeddevelopmentaltrajectory,reachinghigherlevelsofperformanceearlierinlifefollowedbyadipinperformanceduringadolescence,andresurgenceintoadulthood.Indeed,thereareexamplesofsuchnon-lineardevelopmentaltrajectoriesinotheraspectsofcognition(Uhlhaasetal.,2009;Dumontheiletal.,2010). However,itisalsolikelythatthediscrepancyoffindingsbetweentheseinfantstudiesandtheotherdevelopmentalstudiesofVWMcapacitystemsfromparadigmdifferences.Instudiesthatemployedavariationofthechangedetectiontask(LuckandVogel,1997)withchildren,adolescents,andadults,participantshavebeenaskedtoverballyormanuallyrespondtoindicatewhetherachangeoccurredinthedisplay(Cowanetal.,2005,2006;Sanderetal.,2011;Spronketal.,2012).However,ininfantstudies,VWMcapacityhasbeenassessedpredominantlywithgazebehaviorofinfants(Ross-Sheehyetal.,2003;Oakesetal.,2013;Kwonetal.,2014).WecannotruleoutthepossibilitythattheresponsecharacteristicsofparadigmsplayaroleinVWMcapacityestimatesobtainedineachstudy.Ithasbeenarguedthatlookingtimeparadigmsmaytapintodifferentcognitiveprocessescomparedtotaskswithovertresponsedemands,yieldingdifferentialperformanceprofiles(Karmiloff-Smith,1992;Hoodetal.,2000;Keen,2003;LeeandKuhlmeier,2013).ItisplausiblethatvariationsofVWMparadigms,regardlessofhowsimilartheyappear,mayhaveinherentdifferencesinwhataspectsofVWMtheymeasure.Infact,studiesthattestedchildren,adolescents,andadultswithsimilartasksandsimilarmethodsofresponseacquisitionconsistentlydemonstratedlowerVWMcapacityestimatesinchildrenandyoungadolescentsascomparedtoadults(Cowanetal.,2005,2006;Sanderetal.,2011;Spronketal.,2012).OurresultsexpandthefindingsofthesestudiesandsuggestthatVWMperformancedevelopsthroughlateryearsofadolescenceintoadulthood. Severalstudiesreporteddevelopmentalchangesforverbalandspatialworkingmemoryspantasksthroughoutadolescence(Kwonetal.,2002;Gathercoleetal.,2004;Lunaetal.,2004;Lucianaetal.,2005;Johnsonetal.,2014).Furthermore,developmentalchangesinadolescencewereobservedforvariousotheraspectsofcognition,suchasdecision-making(CroneandvanderMolen,2004),speedofprocessing(Kail,1991;Ferreretal.,2013),creativethinking(Kleibeukeretal.,2013),andreasoning(Huizengaetal.,2007;Ferreretal.,2013).OurresultssuggestthattheVWMcapacityshowsaprolongeddevelopmentinadolescence,similartothetrajectoriesobservedinotheraspectsofworkingmemory,aswellasvariousothercognitiveabilities. AlthoughourstudyprovidesevidenceforagerelateddifferencesinVWMcapacitybetweenadolescentsandadults,themechanismsunderlyingsuchdifferencesrequirefurtherinvestigation.Adolescenceisapivotalperiodforbraindevelopmentduringwhichsubstantialchangesareobserved(LebelandBeaulieu,2011;Raznahanetal.,2011;Blakemore,2012;Kleinetal.,2014).Previousresearchassociatedchangesinbrainfunctioningfromadolescencetoadulthoodwithdevelopmentalchangesinvisuospatialworkingmemoryperformance(Kwonetal.,2002;Scherfetal.,2006;BungeandWright,2007).ItisplausiblethatchangesinVWMcapacityestimatesfromadolescencetoadulthoodaredrivenbyfunctionalalterationsinthecorticalregionsthatareinvolvedinworkingmemoryprocessessuchastheparietalcortexandprefrontalcortex(CurtisandD’Esposito,2003;ToddandMarois,2004).Inaddition,thesizeanddensityofwhitemattertractsconnectingprefrontal,occipital,parietal,andtemporallobeshavebeenlinkedtoVWMcapacity(Golestanietal.,2014).Aswhitemattermicrostructuresdrasticallytransformthroughoutadolescence(Nagyetal.,2004;Barnea-Goralyetal.,2005;Mabbottetal.,2006),alterationsinwhitematterfromadolescencethroughadulthoodmayalsoaccountfordevelopmentalchangesinVWMcapacity. Potentially,theagerelateddifferencesinVWMcapacityestimatesmaystemfromdisparitiesinattentionskillsratherthangenuinedifferencesinthenumberofslotsavailableinVWM.Attentionalcontrolhasbeenpostulatedasacriticalcomponentofworkingmemory(EngleandKane,2004).Insupportofthisview,poorerattentionalcontrolhasbeenlinkedtolowerVWMcapacityestimates(Vogeletal.,2005;FukudaandVogel,2009,2011;UnsworthandRobison,2014).Inthisregard,havinglowercapacityestimatesonaverage,adolescentsmayactuallyresemblelowcapacityadults.Researchwithadultsdemonstratedthatlow-capacityadultshavepoorerfilteringskills,whichpreventsthemfromexcludingirrelevantitemsfromVWM(Vogeletal.,2005).Furthermore,low-capacityadultsarefoundtorecoverfromattentionalcapturemoreslowlythanhigh-capacityadults(FukudaandVogel,2011).Ifadolescentsaremorelikelowcapacityadultsinperformance,thepoorerperformancetheyexhibitmaybearesultoftheirinefficiencyinusingtheavailableslotsforVWM.Inlinewiththisclaim,inanevent-relatedpotentials(ERP)studywithadolescentsandadults,contralateraldelayactivity(CDA)wasfoundtobelargerinadolescentsthanadultswhentherewereonetargetandtwodistractoritems,asopposedtothesimilarCDAobservedwhentherewasonlyatargetitemondisplay(Spronketal.,2012). However,themechanismsresponsibleforthepoorerperformanceofadolescentsandlowcapacityadultsmayalsobedistinctfromeachother.Forinstance,inastudycomparingolderadultstoyoungeradults,olderadultswerenotsimplylikelowcapacityyoungadults,despiteperformingworsethanyoungeradultsonaverage(Jostetal.,2011).Similarly,inspiteofthesimilaritiesincapacityestimatesbetweenadolescentsandlowercapacityadults,theremaybedifferentialmechanismsdrivingsuchpoorperformance. Alternatively,theobserveddifferencesinperformancemaystemfromagerelateddisparitiesinthenumberofslotsavailableinVWM.Arecentstudywithchildreninvestigatedwhethersuchdisparitiesinavailableslotsaccountfordifferencesinperformancebetweenchildrenandadults(Cowanetal.,2010).Itwasarguedthatinefficiencyofattentioncannotfullyexplaintheobservedagedifferencesinperformanceandthatthereweregenuinestoragedifferencesbetweenchildrenandadults.Accordingly,theremaybedifferencesinhowmanyslotsareavailableinVWMforadolescentsascomparedtoadults.Moreover,theremaybedifferentunderlyingmechanismsthatresultinimmatureprofilesofVWMinyoungerandolderadolescents.Ourresultssuggestedthatyoungeradolescentsbenefitedmorefromlongerexposuretomemorydisplaysthanadults,whileolderadolescentsdidnotshowsuchbenefits.Theseresultsimplydifferentlimitingfactorsforperformanceinearlierandlateryearsofadolescence. InadditiontodifferinginVWMcapacityestimates,adolescentsmaydifferfromadultsintheresolutionofVWMrepresentations.IthasbeendemonstratedthatthenumberofitemsheldinmindforimmediateaccessandtheresolutionoftheserepresentationsaredistinctaspectsofVWM(XuandChun,2006;Awhetal.,2007;Fukudaetal.,2010).Therefore,theremaybedistinctdevelopmentaltrajectoriesforhowmanyitemscanbeheldinworkingmemoryversushowprecisetheserepresentationsare.Whilethenumberofitemsheldinmemoryincreasewithage,theprecisionoftheserepresentationsmayreachadultlevelsearlierduringdevelopment.Onthecontrary,regardlessofdifferentunderlyingneuralmechanisms(XuandChun,2006),bothsystemsthatsupportVWMmayappearimmatureinadolescence. Itisimportanttonotethatinbothstudieswecomparedadolescentstoyoungadults,whowereonaverage20yearsofage.AlthoughithasbeenarguedthatVWMperformancepeaksatage20(BrockmoleandLogie,2013),wecannotascertainthattheyoungadultsinourstudyreflectthepeakVWMperformanceinadulthood.ItispossiblethatVWMcontinuestodevelopintothethirddecadeoflife,reflectingstructuralchangesinbrainmaturationinadulthood(Sowelletal.,2001,2003;LebelandBeaulieu,2011).Inaddition,alloftheadultparticipantsinourexperimentswerecollegestudents.Wematchedtheadolescentsandadultsinourstudybasedonmaternaleducationlevels.However,itshouldbenotedthatthematernaleducationlevelsinoursampleswererelativelyhigh,correspondingtoatleastsomepost-secondaryeducation.Therefore,itremainstobeassessedhowourresultswouldgeneralizetobothyouthandadultsfromdiverseSESbackgrounds.Moreover,amorecomprehensivebatteryofcognitivemeasureswouldberequiredtoruleoutanyconfoundingcognitivedifferencesbetweenadolescentsandadults.FuturestudiesthatincludeawiderrangeofageandSESandmoredetailedcognitiveassessmentscangreatlybenefittheinvestigationoftypicalVWMdevelopmentfromadolescenceintoadulthood.Furthermore,incorporatingneuroimagingmethodscanassistindeterminingthefactorsthataccountforagerelateddifferencesinVWMcapacityestimates. Althoughmuchremainstobeinvestigated,ourstudyprovidesevidenceforaprotracteddevelopmentalprofileofVWMcapacity.Asalatedevelopingsystemthatdoesnotappeartoreachadultlevelseveninlateadolescence,VWMcapacitybearsthepotentialtobearatherplasticsystemindevelopment,malleabletotheeffectsoftheenvironment.Studiesonneuroplasticityacrossdevelopmenthaverepeatedlydemonstratedthatplasticsystemscanbothbecompromisedandenhanceddependingonexperience(StevensandNeville,2009).Therefore,deficienciesinVWMmaybefoundinadolescentswhohaveexperiencedadversitythroughdevelopment.Forinstance,lowermaternaleducationhasbeenassociatedwithpoorerWMperformanceinadolescentsandtheseassociationsappeartobestablethroughadolescence(Hackmanetal.,2014).Targetedscreeningsandinterventionstofollowmaybehelpfulinmitigatingsuchdisparities.DrawingparallelsfromstudiesthatshowchildrenwithpoorWMskillsespeciallybenefitfromadaptiveWMtraining(Holmesetal.,2009),targetedtrainingsmaybeparticularlyeffectiveforadolescentswithlowerVWMcapacity.SinceVWMcapacityisapredictorofacademicachievementinchildren,interventionsthataimtoimproveVWMskillsmayeventuallybecomehelpfultoolsinimprovingtheacademicoutcomesofadolescentswhoareatriskforschoolfailure. ConflictofInterestStatement Theauthorsdeclarethattheresearchwasconductedintheabsenceofanycommercialorfinancialrelationshipsthatcouldbeconstruedasapotentialconflictofinterest. Acknowledgments ThisworkwassupportedthroughNIH/NIDCDR01-000481toHN,andONRN000141210972andNIMHR01-MH087214toEV.WethankthemembersoftheBrainDevelopmentLabfortheirsupportandassistanceindatacollection,ElliotBerkman,TheodoreBellandJasonIsbellforhelpfulcommentsonanearlierversionofthemanuscript. 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Editedby:YusukeMoriguchi,JoetsuUniversityofEducation,Japan Reviewedby:RichardAllen,UniversityofLeeds,UKHeatherM.Conklin,St.JudeChildren’sResearchHospital,USA Copyright©2015Isbell,Fukuda,NevilleandVogel.Thisisanopen-accessarticledistributedunderthetermsoftheCreativeCommonsAttributionLicense(CCBY).Theuse,distributionorreproductioninotherforumsispermitted,providedtheoriginalauthor(s)orlicensorarecreditedandthattheoriginalpublicationinthisjournaliscited,inaccordancewithacceptedacademicpractice.Nouse,distributionorreproductionispermittedwhichdoesnotcomplywiththeseterms. *Correspondence:ElifIsbell,DepartmentofPsychology,UniversityofOregon,1227UniversityofOregon,Eugene,OR97403,USA,[email protected] Peoplealsolookedat Download
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