Longitudinal development of visual working memory precision in childhood and early adolescence

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ContentslistsavailableatScienceDirect

Cognitive

Development

Longitudinal

development

of

visual

working

memory

precision

in

childhood

and

early

adolescence

S. Burnett

Heyes

a,b,∗,1

_,

_N.

_Zokaei

b,c,1

_,

_M.

_Husain

b

a_School_of_Psychology,_University_of_Birmingham,_United_Kingdom

b_Department_of_Experimental_Psychology,_University_of_Oxford,_United_Kingdom c_Department_of_Psychiatry,_University_of_Oxford,_United_Kingdom

a

r

t

i

c

l

e

i

n

f

o

Articlehistory: Received10March2015

Receivedinrevisedform3March2016 Accepted30March2016

Availableonline9April2016 Keywords: Workingmemory Precision Development Adolescence Childhood

a

b

s

t

r

a

c

t

Visualworkingmemory(VWM)istheabilitytoholdinmindvisualinformationforbrief periodsoftime.ThecurrentstudyinvestigatedVWMprecisiondevelopmentlongitudinally. Participants(N=40,aged7–11years)completeddelayedreproductionsequentialVWM tasksatbaselineandtwoyearslater.Resultsshowage-relatedimprovementinrecall pre-cisiononboth1-itemand3-itemVWMtasks,suggestingdevelopmentduringchildhood andearlyadolescenceintheresolutionwithwhichbothsingleandmultipleitemsare storedinVWM.Probabilisticmodellingofresponsedistributiondatasuggestsage-related improvementinprecisionisattributabletoaspeciﬁcdecreaseinthevariability(noisiness) ofstoredfeaturerepresentations.Thishighlightsanoveldevelopmentalmechanismwhich mayunderlielongitudinalimprovementinVWMperformance,cruciallywithoutinvoking improvementinthenumberofitemsthatcanbestored.VWMprecisionprovidesa sen-sitivemetricwithwhichtotrackdevelopmentalchangeslongitudinally,sheddinglighton underlyingcognitivemechanisms.

1. Introduction

Visualworkingmemory(VWM)providesatemporarystoragemechanismfortheretentionandmanipulationofvisual

informationtosupportothercognitiveprocesses(Luck&Vogel,1997).Thisabilityisconsideredtobeacriticalcontributorto

manyessentialcognitivefunctionssuchasdecision-making,complexreasoningandgoal-directedaction(Baddeley,2003).

NumerousdevelopmentalstudieshaveshownthatperformanceonestablishedneuropsychologicaltestsofVWMimproves

duringchildhood(Alloway,Gathercole,&Pickering,2006;Gathercole,Pickering,Ambridge,&Wearing,2004).Typicallyin

thesetests,participantsviewastaticvisualarray(e.g.colouredshapes)orspatiotemporalsequenceofvisualevents(e.g.

blocktapping)whichareheldinmemoryandthenreproducedfollowingadelay.Thesestudieshavedemonstrated,within

largecross-sectionaldatasets,robustagetrajectoriesandevidencefordevelopmentalstabilityintherelationshipofVWM

toothercognitivecomponents(Gathercoleetal.,2004).

ThemechanismsunderlyingVWMdevelopmentanditsrelationshipwithothercognitivemeasuresremaindebated

(Astle&Scerif,2011).Thatis,whatarethefundamentalcognitivemechanismsunderlyingdevelopmentalimprovementsin

VWM?MosttraditionalmeasuresofVWMrelyonindicesofthenumberofitemsthatcanberemembered,e.g.usingtasks

∗ Correspondingauthorat:SchoolofPsychology,UniversityofBirmingham,Birmingham,B152TT,UnitedKingdom. E-mailaddress:[email protected](S.BurnettHeyes).

1 _Denotes_equal_{contribution.}

http://dx.doi.org/10.1016/j.cogdev.2016.03.004

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andchangedetectiontasksprovidingadiscreteestimateofthenumberofitemsthatcanberetainedinVWM.

Recently,aninnovativeempiricalapproachhasshownpotentialtoaccuratelyandsensitivelycharacteriseVWM

perfor-manceinacompletelydifferentway.Unlikespanorchangedetectiontasks,thisapproachreliesonparticipantsreproducing

theexactqualitiesoftheretainedinformationonacontinuousresponsescale,e.g.theorientationofabarstimulus.Such

analogueresponsesprovideameasureofworkingmemoryprecision,whereprecisionreﬂectstheresolutionwithwhich

itemsareheldinVWM(Bays,Catalao,&Husain,2009;Fougnie,Asplund,&Marois,2010;Wilken&Ma,2004;Zhang&Luck,

2008).RecentinvestigationssuggestthatcontinuousrecallmeasuresmaybemoresensitiveindicesofchangesinVWM

thandiscretecapacitymeasures,e.g.inadultneuropsychologicalpopulations(Zokaei,BurnettHeyes,Gorgoraptis,Budhdeo,

&Husain,2014).

Findingsfromsuchdelayedreproductiontaskshavealsochallengedthe‘quantal’viewofVWM.Resultsfromsuchstudies

arenotconsistentwiththeviewthatthereisaﬁxedupperlimittothenumberofitemsthatcanbestoredinVWM(Baysetal.,

2009;Gorgoraptis,Catalao,Bays,&Husain,2011;Ma,Husain,&Bays,2014;Zokaei,Gorgoraptis,Bahrami,Bays,&Husain,

2011).Instead,theseinvestigationshaveshownthatresponsedatacanbemodelledbyconsideringVWMtoconsistofa

limitedcognitiveresource(Bays&Husain,2008),withrecallerrorarisingduetonoiseintunedpopulationsofneurons(Bays,

2014,2015;Maetal.,2014).Asthenumberofitemsstoredincreases,theprecisionwithwhicheachitemcanberetained

decreases,purportedlybecausethesamepooloftunedneuronsmustrepresentmoreitems,andthustherepresentationof

eachitembecomesnoisier(Bays,2014;Bays,2015;Maetal.,2014).

Usingthestatisticalprocedureofmixturemodellingofresponsedata,continuousVWMtasksalsoprovideameansto

dissectoutsourcesoferrorcontributingtothepatternofoverallVWMperformance(Baysetal.,2009).Inotherwords,

whatbasic,fundamentalcognitiveprocessescontributetoworkingmemoryfailureandsuccess?Firstly,responseerrorcan

theoreticallyariseduetovariabilityinmemory–‘noise’–associatedwiththerememberedfeature;thatis,howaccurately

information(e.g.orientation)isstored.Alternatively,errorcanariseduetorandomguessing,forexample,duetofailuresat

encodingoratretrievalleadingtoacompletelyrandomresponse.Lastly,errormayariseduetosystematicinterferenceor

corruptionofinformationbytheotheritemsencodedintoVWM.Theselattermisbindingresponsesoccurwhenonefeature

ofanobject(e.g.colour)iserroneouslylinkedwiththefeature(e.g.orientation)ofadifferentobjectstoredinmemory(Bays

etal.,2009).Crucially,characterisingVWMdevelopmentintermsofthesedistinctsourcesoferrormayprovidefurther

insightsintounderlyingdevelopmentalcognitivemechanisms.

ThecurrentstudyinvestigateddevelopmentofVWMprecisionlongitudinallybetweenage7and13years.Forty

partic-ipantscompletedanidenticaltaskbatterytwice,twoyearsapart.Tasksconsistedof1-itemand3-itemsequentialVWM

precisiontasksandasensorimotorcontroltask.Precisionwascalculatedas1/SDoferror(reciprocalofvariability)inresponse.

Aftercontrollingfordevelopmentalchangesinsensorimotorperformance,wepredictedlongitudinalincreasesinrecall

pre-cisiononboththe1-itemand3-itemVWMtasks.Inaddition,wepredictedmixturemodellingofrecalldatafromthe3-item

VWMtaskwouldprovideevidencethateffectsofageareattributablespeciﬁcallytoadecreaseinvariabilityinthe

rep-resentationoftargetstimuli,andnottoanychangesinrandomguessingormisbinding.Thatis,themixturemodelling

wouldshedfurtherlightonmorefundamentalcognitivemechanismsunderlyingmemorydevelopment—whetherchanges

inVWMperformanceareduetodevelopmentalincreasesincontinuousmemoryresource,ortosomeotherprocesssuch

asreducedfrequencyofmisbindingorguessing.

2. Methods

2.1. Participants

40participantswererecruitedfromasingle-sex(male)preparatoryschoolinOxfordshireandtestedonthesameprotocol

twice,twoyearsapart(t1andt2).Participantageatt1rangedfrom7.9to11.7years,withmean10.2andstandarddeviation

(SD)1.02(seeTable1).Participantswerefromalarger(N=90)cross-sectionalcohort(BurnettHeyes,Zokaei,vanderStaaij, Bays,&Husain,2012).Thecurrentlongitudinalcohortof40participantsconsistedofallt1participantswhowerestill

attendingtheschoolatt2forwhomparent/guardianconsentcouldbeobtainedatt2andforwhomtimetablingconstraints

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Fig.1.Schematicpresentationoftasks.

(A)Sensorimotorcontroltask.Participantsusedadialtoadjusttheorientationoftheprobebar(above,incircle)tothatofthetargetbar(below). (B)1-itemvisualworkingmemorytask.Participantshadtokeepinmindtheorientationofthetargetbar,andfollowingadelay,usedadialtoadjustthe orientationoftheprobebar(incircle)tothatofthetargetbarheldinmemory.

(C)3-itemvisualworkingmemorytask.Participantswerepresentedwithasequenceof3colouredbars.Followingadelay,aprobebarappeared(incircle). Participantsusedthedialtoadjusttheorientationoftheprobebartomatchthebarofthesamecolourfromtheprevioussequence.

2.2. FSIQe

Standardizedyearlytestscores(CAT-3;www.gl-assessment.co.uk)wereprovidedbytheschoolforeachparticipantat

t1andtransformedintoestimatedfull-scaleIQ(FSIQe_;_see_Table₁_),_as_per_Wright,_Strand_and_Wonders₍₂₀₀₅₎_:

FSIQe= 1.1×CAT-Av−12.0

whereFSIQe_is_estimated_FSIQ_and_CAT-Av_is_average_CAT-3_score_calculated_by_combining_standardised_scores_on_verbal,

non-verbalandquantitativereasoningsubtests(Wrightetal.,2005).

2.3. Tasks

2.3.1. Colour-namingtask

Atthestartoftheexperiment,eachparticipantcompletedacolour-namingtaskinwhichtheywereshownﬁve

screen-shotsfromtheVWMtask,eachcontainingabarinoneofthefollowingstimuluscolours:red,yellow,green,blueand

purple/pink.Participantswereaskedtonamealoudeachoftheseﬁvecolours.Allparticipantssuccessfullycompletedthis

task.

2.3.2. Sensorimotorcontroltask

Directlyaftercompletionofthecolour-namingtask,participantscompleted25 trialsofa sensorimotorcontroltask

(Fig.1A).Stimuliwerepresentedonalaptopmonitor(32◦×19◦)ataviewingdistanceof∼52cm.

Oneachtrialacolouredorientedbar(2×0.2◦ofvisualangle)waspresentedagainstagreybackground.After500ms

followingthepresentationofthebar,aprobebarofthesamecoloursurroundedbyablackcircleappearedbelowthetarget.

Participantswereaskedtoadjusttheorientationoftheprobebarusingarotatingdialtomatchtheorientationofthetarget

whichremainedonscreenuntilresponse.Theblackcirclesurroundingtheprobeitemdisappeareduponrotatingthedial.

Barcolourwasselectedsoastobeeasilydistinguishable—asinthecolour-namingtask.Theorientationofthetargetand

probewereindependentlyrandomized.Theinter-trialinterval(ITI)was500ms.

2.3.3. Visualworkingmemorytask:1-item

Directlyaftercompletionofthesensorimotorcontroltask,participantscompleted30trialsofa1-itemVWMtask.On

eachtrial,participantswerepresentedwithasinglecolouredorientedbaratthecentreofthescreenfor500ms.Following

ablank500msdelay,aprobebarofthesamecolourappearedatthecentreofthescreensurroundedbyablackcircle.

Participantswereaskedtoadjusttheprobebar’sorientationtomatchtheorientationoftheprobed(‘target’)barusingthe

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positionsinthesequencewereprobedwithequalprobability.Participantscompleted90trialsofthistask,withabreak

every15trials.TheITIwas500ms.

2.4. Analysis

2.4.1. Developmentalchangesinprecision

Wecalculatedrecallprecisionasthereciprocalofthecircularstandarddeviationofresponseerror(whereresponse

erroristhedifferencebetweenresponseandtargetangles)(Fisher,1993).Precisionisameasureofresponsevariability:

lessvariabilitycorrespondstomorepreciserecall.Recallprecisionwascalculatedforthesensorimotor,1-itemand3-item

VWMtasks.ToevaluatetheeffectofageonVWMprecisioncontrollingforanychangesinsensorimotorperformance,

wecorrectedperformanceontheVWMtaskbysubtractingsensorimotorerrorfromVWMrecallerrorandrecalculating

precisionaccordingly(i.e.1/sqrt(differenceinerrorvariance)).

Toevaluatedevelopmentalchangesinprecision,Wilcoxonsigned-ranktests(thenon-parametricequivalentofpaired

samplest-tests)wereconductedcomparingt1vs.t2corrected1-and3-itemVWMprecisionvalues(overallandateach

serialposition)aswellassensorimotorprecision.Statisticalsigniﬁcancewasp<0.05.Non-parametricstatisticswereused

sinceinourdataprecisionisnotnormallydistributed.Finally,toinvestigatedifferentialtrajectoriesofdevelopmentfor

3-itemrelativeto1-itemVWMtasks,Wilcoxonsigned-ranktestswereconductedcomparingt1vs.t23-itemVWMprecision

values,correctedfor1-itemVWMperformancebysubtracting1-itemVWMrecallerrorfromoverall3-itemVWMrecall

errorandrecalculatingprecisionaccordingly(i.e.1/sqrt(differenceinerrorvariance)).

2.4.2. Mixturemodellingoferrorinresponse

Inorder toidentifymechanismsunderlyingdevelopmentalchangesin precisiononthe3-itemVWMtask,we ﬁta

probabilisticmodelthatdissociatesdifferentsourcesoferrorinmemorypreviouslyintroducedbyBaysetal.(2009)(see

alsohttp://www.sobell.ion.ucl.ac.uk/pbays/code/JV10/).Thismodelisdescribedbythefollowingequation:

p

ˆ

=˛␬

ˆ␪ −␪

+␤1 m m

i ␬

ˆ −i

+ 1 2

isthetrueorientationofthetargetitem, ˆ istheorientationreportedbytheparticipantandisthevonMisesdistribution

(thecircularanalogueoftheGaussiandistribution)withmeanzeroandconcentrationparameter␬(kappa).Theprobability

ofreportingthetargetitemisgivenby␣.

SeveralsourcesoferrorcouldcontributetodevelopmentalchangesinperformanceonVWMtaskssuchasthoseemployed

inthepresentstudy.Firstly,changesinVWMperformancecouldresultfromachangeinvariabilityinmemoryfortarget

features–hereorientation–capturedbythemodelconcentrationparameter(␬).␬isameasureofvariability,wherehigher

␬correspondstolowervariabilityinmemoryrepresentations(Fig.2A).Successfulperformanceofthe3-itemVWMtaskalso

requiresmemoryforthecorrectcombinationoforientationandcolour.Therefore,changesinperformanceonthe3-item

VWMtaskcouldariseasaresultofchangesintheproportionofresponsesarisingasaresultofanincorrectconjunction

ofcolourandorientation(misbindingerrors).Insuchtrialsparticipantsmakeanerrorcentredontheorientationofother

(non-probed)itemsinthesequence(Fig.2B).Inclearerterms:iftheprobeditemisredbutparticipantsrespondwiththe

orientationofoneoftheothercolouredbarsinthesequence,thiswouldbeclassiﬁedbythemodelasamisbindingerror.

Inthemodel,theprobabilityofreportinganon-targetitemisgivenby␤,with{␾1,␾2...␾m}theorientationsofthem

non-targetitems.Alternatively,changeinrecallprecisioncouldoccurduetochangesinthenumberofguesses/random

responses—capturedinthemodelby␥(Fig.2C),where␥=1-␣-␤.

Maximumlikelihoodparametersof␬,␣,␤and␥wereobtainedforeachtaskusinganexpectationmaximization

proce-dureforeachparticipant(Myung,2003).Usingthisprobabilisticmodel,wewereabletodeterminetheunderlyingsources

ofdevelopmentalchangeinVWM.Similartoouranalysisofrecallprecision,weusedpairedt-teststocomparet1vs.t2

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Fig.2.Threesourcesoferrorinmemoryusedformodellingperformance.

(A)AVonMises(circularGaussian)distributionwithconcentrationparameter␬,centredontheprobedortargetvalue,capturingvariabilityinmemoryfor theprobedorientation,withtheareaunderthedistribution(shaded)beingproportionaltotheprobabilityofrespondingtothetarget.

(B)VonMisesdistributionwithconcentrationparameter␬,centredononeofthenon-probedornon-targetvalues,resultingfromerrorsinmisidentifying theorientationwhichbelongedtotheprobedcolour(misbinding).Theareaunderthedistributioncorrespondstotheproportionofnon-targetresponses. (C)Uniformdistributionoferrorcorrespondingtorandomerror,withtheareaunderthisdistributioncorrespondingtotheproportionofrandomresponses.

Table2

Mean(SD)precisionvalues(rad−1₎_in_each_task_by_time-point_and_condition._All_VWM_precision_values_are_corrected_for_sensorimotor_precision._One

outlyingdatapointwasexcluded(seetext).

Sensorimotor 1-itemVWM 3-itemVWM

Total SP1 SP2 SP3

t1(N=40) 8.74(2.73) 3.33(1.43) 2.33(1.08) 1.90(1.15) 1.83(.496) 3.26(2.29)

t2(N=40) 10.30(2.42) 4.25(1.69) 2.80(1.19) 2.24(1.31) 2.16(0.63) 4.01(2.67)

3. Results

3.1. Sensorimotorprecisionduringdevelopment

Sensorimotorprecisionimprovedsigniﬁcantlybetweent1andt2(Z=3.19,p=0.01;Table2).Therefore,intheremaining

analysesofperformanceinthe1-itemand3-itemsVWMtasks,wecorrectedperformanceforchangesinsensorimotor

precision(fordetails,seeSection3).

3.2. Workingmemoryprecisionimproveswithageonthe1-and3-itemVWMtasks

Meanprecisiononthe1-itemVWMtaskimprovedsigniﬁcantlyafter2yearsaftercorrectingfordevelopmentalchange

insensorimotorprecision(Z=2.87,p=0.004;oneoutlier>2.5SD>meanexcluded).Thus,precisionofrecallforevenasingle

itemmaintainedinmemoryincreasedafter2yearsinchildhoodandearlyadolescence.

Recallprecisiononthe3-itemVWMtaskalsoimprovedsigniﬁcantlywithage.Participantsperformedsigniﬁcantlybetter

att2comparedtot1(Z=2.39,p=0.017;Fig.3A).Wilcoxonsigned-ranktestscomparingt1vs.t2correctedprecisionateach

serialpositionofthetargetdemonstratedasigniﬁcantimprovementinWMprecisionforitemspresentedﬁrstandsecondin

thesequence(Z=2.05,p=0.04andZ=3.06,p=0.002respectively)withnosigniﬁcantdifferenceforthethirditem(Z=1.57

p=0.12;Fig.3A).

3.3. Improvementon3-itemWMtaskgreaterthanimprovementon1-itemVWMtask

Comparisonoft1vs.t23-itemVWMprecisioncorrected for1-itemVWMprecisionshowedevidencefora steeper

developmentaltrajectoryofprecisioninthe3-itemVWMtaskrelativetothe1-itemVWMtask(Z=2.79,p=0.005;seeFig.4

forindividualparticipants’changeinprecision).

3.4. Mixturemodellingoferrorinresponse

Tovisualizethedistributionofresponsesinthe3-itemVWMtask,weplottedthedistributionofresponsesaroundthe

target(i.e.probed)orientation.AsshowninFig.3B,theproportionofresponsesfallingclosetothetargetorientationincreased

fromt1tot2.Thisisspeciﬁcallyillustratedinthepeakofresponsedistributionaroundzero,i.e.thegreaterproportionof

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Fig.3.Performanceon3-itemvisualworkingmemorytask.

(A)Meanrecallprecisionimprovedovertwoyearsoverallandatdifferentserialpositions.

(B)Distributionofresponseswithrespecttotheorientationofthetargetstimulinarrowswithincreasingage.Aftertwoyears,therewasadecreasein variabilityinresponsearoundthetargetorientation.

(C)Modelestimatesdemonstratethatwithagethereisachangeonlyintheconcentrationparameter,␬,i.e.,variabilityinmemoryfortargetorientation.

Fig.4.Performanceonthe3-itemvisualworkingmemorytaskforeachparticipantatt1andt2. Trajectoryofchange,correctedforchangeinperformanceonthe1-itemvisualworkingmemorytask.

However,overallperformancedoesnotinformusasofthesourcesoferror,andhowthesealterwithage.Thatis,overall

performancedoesnotshedlightonwhetherimprovedVWMperformanceisduetodecreasedvariabilityinresponseforthe

targetfeature(kappa),changesinproportionoftarget(p(T))ornon-targetresponses(p(NT)),orincreasedrandomresponses

(p(U)).Wethereforeﬁtaprobabilisticmodel(Fig.2;Baysetal.,2009)toeachparticipant’s3-itemVWMdatasetateachtime

pointtoexaminetheeffectofageoneachofthepossiblesourcesoferror.

Resultsshowthatkappa(inverseofvariabilityinresponsearoundprobedortargetorientation)increasedsigniﬁcantly

withage(t(39)=3.3,p=0.002),cruciallywithnochangeinothermodelparameters:t(39)=1.6,p=0.12forp(T),t(39)=1.4,

p=0.18forp(NTandt(39)=0.3,p=0.73forp(U)(Fig.3C).Thusvariabilityaroundtheprobedtargetorientationimproved

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4. Discussion

ThecurrentstudyinvestigatedlongitudinaldevelopmentofVWMprecisionduringchildhoodandearlyadolescence.

Fortyparticipantsaged7–11yearsatt1completedaVWMprecisiontaskbatterytwice,twoyearsapart.Resultsdemonstrate

ﬁrstlythatrecallprecisionincreasedwithageonboth1-itemand3-itemsequentialVWMprecisiontasks.Theseincreases

remainedsigniﬁcantaftercontrollingforage-relatedimprovementinperformanceonasensorimotorcontroltask.Second,

thelongitudinaleffectsofagewereattributabletoaspeciﬁcdecreaseinvariabilityintherepresentationoftargetstimuli,

andnotduetochangesinrandomrespondingortomisbinding,i.e.corruptionbyfeaturesofotheritemsretainedinmemory.

WediscussimplicationsintermsofdevelopmentalmechanismsunderlyingobservedimprovementsinVWMperformance

withage.

4.1. Developmentofworkingmemoryprecision

AnumberofstudieshaveshownimprovementacrosschildhoodinperformanceonstandardtestsofVWM(Alloway

etal.,2006;Gathercoleetal.,2004).Inthecurrentstudy,wecontributetounderstandingthemechanisticunderpinningsof

VWMdevelopment.WeshowthattheprecisionwithwhichitemsarerecalledfromVWM,whetherpresentedindividually

orinsequencesofthree,increasedafteratimeintervaloftwoyearsinparticipantsaged7–11yearsatstudyentry.Because

participantsweresampledlongitudinally,wecanruleoutinterpretationsbasedwhollyorpartiallyoninter-individual

variabilityandcohorteffects,enablingconclusionstobedrawnregardingthedevelopmentaltrajectoryofVWMprecision.

Importantly,longitudinalincreasesinprecisionwithstoodcorrectionforimprovementsinperformanceonacontroltask

requiringﬁnehand-eyeco-ordination,andhencearenotreadilyexplicableonthebasisofimprovementinsensorimotor

factors.Instead,theresultssuggestthattheresolutionofitemsrecalledfromVWMincreasesduringmiddlechildhoodand

earlyadolescence.

Theseconclusionsalignwiththosefromcross-sectionalstudiesshowingage-associateddevelopmentduringchildhood

andadolescenceinVWMperformance(BurnettHeyesetal.,2012;DeLucaetal.,2003;Luciana,Conklin,Hooper,&Yarger,

2005;Swanson,1999;Zald&Iacono,1998).Thecurrentresultsarealsoconsistentwithstudiesshowingdevelopmental

improvementsinperformanceonexecutivetasksthathaveaVWMcomponent(Brocki&Bohlin,2004;Lucianaetal.,2005;

Luna,Garver,Urban,Lazar,&Sweeney,2004).Usingcontinuousrecallmeasures,ratherthandiscretemeasuresofcapacity,

mayofferenhancedsensitivityfortrackingbehaviouralchangesinVWM,ashasrecentlybeendemonstratedusingeven

relativelysmallsamples(N=12)ofadultpatientswithneurodegenerativeconditions(Zokaeietal.,2014).Importantly,the

approachtakenherealsoenablesinvestigationoftheunderlyingcognitivemechanismsassociatedwiththesedevelopmental

changes.

4.2. Modellingthedistributionofresponses

ContinuousVWMtasksprovideameanstoexaminethesourcesoferrorinrecall.Weappliedaprobabilisticmodel

(Baysetal.,2009)toresponsedatafromthe3-itemVWMtasktodecomposethecontributionsofdifferentsourcesoferror.

Withinthismodel,errorinmemorycanarisefromthreesources.Firstly,itcanbeduetovariability–‘noise’–inmemory

fortherememberedfeature.Alternatively,errorcanariseduetorandomguessing,forexampleduetofailuresatencoding

orretrieval.Lastly,responseerrorinthe3-itemVWMtaskmayalsotheoreticallyariseduetosystematicinterferenceor

biasingofinformationbyfeaturesbelongingtootheritemsencodedintoVWM(i.e.misbindingornon-targetresponses).

Here,weshowthatimprovementwithageinthe3-itemVWMtaskwasattributabletoaspeciﬁcdecreaseinvariabilityinthe

representationoftargetstimuli,andcouldnotbeattributedtoanychangesinthefrequencyofguessesormisbindingerrors.

Assuch,ourmodellinganalysisshedsnewlightonpotentialspeciﬁcmechanismsunderlyinglongitudinaldevelopmentin

VWMperformance.

Infuture,delayedreproductionVWMtasksaccompaniedbyprobabilisticmodellingofresponsedatacouldalsoprovidea

usefultoolforcharacterisingmorefullyneuralchangesassociatedwithVWMacrossthelifespan.Severalstudieshaveshown

thatitispossibletotrackdevelopmentofthefunctionalneuralsubstratesofVWMduringchildhoodandadolescence(Bunge

&Wright,2007;Dumontheil&Klingberg,2012;Geier,Garver,Terwilliger,&Luna,2009;Klingberg,Forssberg,&Westerberg,

2002).Usingprecision,ratherthantraditionalmeasuresofcapacity,mayofferenhancedsensitivityfordetectingvariance

associatedwithage.

4.3. Differentialdevelopmenton1-itemand3-itemVWMtasks

Thecurrentstudyshowedeffectsofageonthedifferenceinrecallprecisionbetween1-itemand3-itemtasks,conceptually

equivalenttoanagebytaskinteraction.Thatis,whereaswedemonstratesigniﬁcantimprovementwithageonbothVWM

tasks,improvementontheharder3-itemtaskwasmoresubstantial.Furtherempiricalstudiesareneededtoexplorethe

developmentalcognitivemechanismsunderlyingthisresult.Possibilitiesincludedevelopmentofattention(Astle,Nobre,&

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Acknowledgments

ThisresearchwasfundedbytheWellcomeTrustandtheMedicalResearchCouncil.

References

Alloway,T.P.,Gathercole,S.E.,&Pickering,S.J.(2006).Verbalandvisuospatialshort-termandworkingmemoryinchildren:aretheyseparable?Child Development,77(6),1698–1716.http://dx.doi.org/10.1111/j.1467–8624.2006.00968.x

Astle,D.E.,Nobre,A.C.,&Scerif,G.(2012).Attentionalcontrolconstrainsvisualshort-termmemory:insightsfromdevelopmentalandindividual differences.TheQuarterlyJournalofExperimentalPsychology,65(2),277–294.

Astle,D.E.,&Scerif,G.(2011).Interactionsbetweenattentionandvisualshort-termmemory(VSTM):whatcanbelearntfromindividualand developmentaldifferences?Neuropsychologia,49(6),1435–1445.http://dx.doi.org/10.1016/j.neuropsychologia.2010.12.001

Baddeley,A.(2003).Workingmemory:lookingbackandlookingforward.NatureReviewsNeuroscience,4(10),829–839.

http://dx.doi.org/10.1038/nrn1201

Bays,P.M.(2014).Noiseinneuralpopulationsaccountsforerrorsinworkingmemory.TheJournalofNeuroscience:TheOfﬁcialJournaloftheSocietyfor Neuroscience,34(10),3632–3645.http://dx.doi.org/10.1523/JNEUROSCI.3204-13.2014

Bays,P.M.(2015).Spikesnotslots:noiseinneuralpopulationslimitsworkingmemory.TrendsinCognitiveSciences,19(8),431–438.

http://dx.doi.org/10.1016/j.tics.2015.06.004

Bays,P.M.,Catalao,R.F.G.,&Husain,M.(2009).Theprecisionofvisualworkingmemoryissetbyallocationofasharedresource.JournalofVision,9(10)

http://dx.doi.org/10.1167/9.10.7

Bays,P.M.,&Husain,M.(2008).Dynamicshiftsoflimitedworkingmemoryresourcesinhumanvision?Science,321(5890),851–854.

Brocki,K.C.,&Bohlin,G.(2004).Executivefunctionsinchildrenaged6–13:adimensionalanddevelopmentalstudy.DevelopmentalNeuropsychology, 26(2),571–593.http://dx.doi.org/10.1207/s15326942dn26023

Bunge,S.A.,&Wright,S.B.(2007).Neurodevelopmentalchangesinworkingmemoryandcognitivecontrol.CurrentOpinioninNeurobiology,17(2), 243–250.http://dx.doi.org/10.1016/j.conb.2007.02.005

BurnettHeyes,S.,Zokaei,N.,vanderStaaij,I.,Bays,P.M.,&Husain,M.(2012).Developmentofvisualworkingmemoryprecisioninchildhood. DevelopmentalScience,15(4),528–539.http://dx.doi.org/10.1111/j.1467-7687.2012.01148.x

DeLuca,C.R.,Wood,S.J.,Anderson,V.,Buchanan,J.-A.,Profﬁtt,T.M.,Mahony,K.,&Pantelis,C.(2003).NormativedatafromtheCANTAB.I:development ofexecutivefunctionoverthelifespan.JournalofClinicalandExperimentalNeuropsychology,25(2),242–254.

http://dx.doi.org/10.1076/jcen.25.2.242.13639

Dumontheil,I.,&Klingberg,T.(2012).Brainactivityduringavisuospatialworkingmemorytaskpredictsarithmeticalperformance2yearslater.Cerebral Cortex,22(5),1078–1085.http://dx.doi.org/10.1093/cercor/bhr175

Fisher,N.I.(1993).Statisticalanalysisofcirculardata.CambridgeUniversityPress.

Fougnie,D.,Asplund,C.L.,&Marois,R.(2010).Whataretheunitsofstorageinvisualworkingmemory?JournalofVision,10(12),27.

http://dx.doi.org/10.1167/10.12.27

Gathercole,S.E.,Pickering,S.J.,Ambridge,B.,&Wearing,H.(2004).Thestructureofworkingmemoryfrom4to15yearsofage.DevelopmentalPsychology, 40(2),177–190.http://dx.doi.org/10.1037/0012-1649.40.2.177

Geier,C.F.,Garver,K.,Terwilliger,R.,&Luna,B.(2009).Developmentofworkingmemorymaintenance.JournalofNeurophysiology,101(1),84–99.

http://dx.doi.org/10.1152/jn.90562.2008

Gorgoraptis,N.,Catalao,R.F.G.,Bays,P.M.,&Husain,M.(2011).Dynamicupdatingofworkingmemoryresourcesforvisualobjects.TheJournalof Neuroscience:TheOfﬁcialJournaloftheSocietyforNeuroscience,31(23),8502–8511.http://dx.doi.org/10.1523/jneurosci.0208-11.2011

Klingberg,T.,Fernell,E.,Olesen,P.J.,Johnson,M.,Gustafsson,P.,Dahlström,K.,&Westerberg,H.(2005).Computerizedtrainingofworkingmemoryin childrenwithADHD-arandomized,controlledtrial.JournaloftheAmericanAcademyofChild&AdolescentPsychiatry,44(2),177–186.

http://dx.doi.org/10.1097/00004583-200502000-00010

Klingberg,T.,Forssberg,H.,&Westerberg,H.(2002).Increasedbrainactivityinfrontalandparietalcortexunderliesthedevelopmentofvisuospatial workingmemorycapacityduringchildhood.JournalofCognitiveNeuroscience,14(1),1–10.http://dx.doi.org/10.1162/089892902317205276

Luciana,M.,Conklin,H.M.,Hooper,C.J.,&Yarger,R.S.(2005).Thedevelopmentofnonverbalworkingmemoryandexecutivecontrolprocessesin adolescents.ChildDevelopment,76(3),697–712.http://dx.doi.org/10.1111/j.1467-8624.2005.00872.x

Luck,S.J.,&Vogel,E.K.(1997).Thecapacityofvisualworkingmemoryforfeaturesandconjunctions.Nature,390(6657),279–281.

http://dx.doi.org/10.1038/36846

Luna,B.,Garver,K.E.,Urban,T.A.,Lazar,N.A.,&Sweeney,J.A.(2004).Maturationofcognitiveprocessesfromlatechildhoodtoadulthood.Child Development,75(5),1357–1372.http://dx.doi.org/10.1111/j.1467-8624.2004.00745.x

Ma,W.J.,Husain,M.,&Bays,P.M.(2014).Changingconceptsofworkingmemory.NatureNeuroscience,17(3),347–356.http://dx.doi.org/10.1038/nn.3655

Myung,I.J.(2003).Tutorialonmaximumlikelihoodestimation.JournalofMathematicalPsychology,47(1),90–100.

http://dx.doi.org/10.1016/S0022-2496(02)00028-7

Swanson,H.L.(1999).Whatdevelopsinworkingmemory?Alifespanperspective.DevelopmentalPsychology,35(4),986–1000.

http://dx.doi.org/10.1037/0012-1649.35.4.986

Wass,S.V.,Scerif,G.,&Johnson,M.H.(2012).Trainingattentionalcontrolandworkingmemory—isyounger,better?DevelopmentalReview,32(4), 360–387.http://dx.doi.org/10.1016/j.dr.2012.07.001

Weil,L.G.,Fleming,S.M.,Dumontheil,I.,Kilford,E.J.,Weil,R.S.,Rees,G.,&Blakemore,S.-J.(2013).Thedevelopmentofmetacognitiveabilityin adolescence.ConsciousnessandCognition,22(1),264–271.http://dx.doi.org/10.1016/j.concog.2013.01.004

(9)

Wright,I.,Strand,S.,&Wonders,S.(2005).Estimationofpremorbidintellectualabilitiesinchildren.TheBritishPsychologicalSocietyDivisionofEducational andChildPsychology,22(2).

Zald,D.H.,&Iacono,W.G.(1998).Thedevelopmentofspatialworkingmemoryabilities.DevelopmentalNeuropsychology,14(4),563–578.

http://dx.doi.org/10.1080/87565649809540729

Zhang,W.,&Luck,S.J.(2008).Discreteﬁxed-resolutionrepresentationsinvisualworkingmemory.Nature,453(7192),233–235.

http://dx.doi.org/10.1038/nature06860

Zokaei,N.,BurnettHeyes,S.,Gorgoraptis,N.,Budhdeo,S.,&Husain,M.(2014).Workingmemoryrecallprecisionisamoresensitiveindexthanspan. JournalofNeuropsychology,http://dx.doi.org/10.1111/jnp.12052

Zokaei,N.,Gorgoraptis,N.,Bahrami,B.,Bays,P.M.,&Husain,M.(2011).Visualworkingmemoryformotionsequences.VisionSciencesSociety,11(4)