Longitudinal stability of the folding pattern of the anterior cingulate cortex during development

ContentslistsavailableatScienceDirect

Developmental

Cognitive

Neuroscience

j ou rn a l h om ep a ge :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

Longitudinal

stability

of

the

folding

pattern

of

the

anterior

cingulate

cortex

during

development

A.

Cachia

_,

_G.

_Borst

_,

_C.

_Tissier

_,

_C.

_Fisher

_,

_M.

_Plaze

_,

_O.

_Gay

_,

_D.

_Rivière

_,

N.

Gogtay

_,

_J.

_Giedd

_,

_J.-F.

_Mangin

_,

_O.

_Houdé

_,

_A.

_Raznahan

b_{UniversityParisDescartes,SorbonneParisCité,Paris,France}

c_{INSERMUMR894,CenterofPsychiatryandNeurosciences,Paris,France} d_{InstitutUniversitairedeFrance,Paris,France}

e_{CATIMulticenterNeuroimagingPlaform,cati-neuroimaging.com,France} f_{UNATI,Neurospin,CEA,Gif-sur-Yvette,France}

g_{NationalInstituteofMentalHealth(NIMH)andtheNationalInstitutesofHealthIntramuralResearchProgram,Bethesda,USA}

a

r

t

i

c

l

e

i

n

f

o

Received8October2015

Receivedinrevisedform19January2016 Accepted28February2016

Availableonline2March2016 Keywords: ACC Fetallife Sulcalpattern Neurodevelopment MRI Executivecontrol

a

b

s

t

r

a

c

t

Prenatalprocessesarelikelycriticalforthedifferencesincognitiveabilityanddiseaseriskthatunfoldin postnatallife.Prenatallyestablishedcorticalfoldingpatternsareincreasinglystudiedasanadultproxy forearlierdevelopmentevents–undertheasyetuntestedassumptionthatanindividual’sfoldingpattern isdevelopmentallyfixed.Here,weprovidethefirstempiricaltestofthisstabilityassumptionusing263 longitudinally-acquiredstructuralMRIbrainscansfrom75typicallydevelopingindividualsspanning ages7to32years.Wefocusontheanteriorcingulatecortex(ACC)–anintenselystudiedcorticalregion thatpresentstwoqualitativelydistinctandreliablyclassifiablesulcalpatternswithlinkstopostnatal behavior.Weshow–withoutexception–thatindividualACCsulcalpatternsarefixedfromchildhoodto adulthood,atthesametimethatquantitativeanatomicalACCmetricsareundergoingprofound devel-opmentalchange.Ourfindingsbuttressuseoffoldingtypologyasapostnatally-stablemarkerforlinking variationsinearlybraindevelopmenttolaterneurocognitiveoutcomesinexuterolife.

©2016TheAuthors.PublishedbyElsevierLtd.ThisisanopenaccessarticleundertheCCBY-NC-ND license(http://creativecommons.org/licenses/by-nc-nd/4.0/).

1. Introduction

Analysisof brain anatomy fromin vivo structural magnetic resonance imaging (sMRI) hasbecomea majortool in biologi-calpsychiatryandpsychology.Disorderslikeschizophrenia and autismspectrumdisorder,aswellastraitslikegeneralcognitive abilities,havebeenlinkedtovariationindiverseneuroanatomical featuresinpostnatal life(GieddandRapoport,2010;Kanai and Rees,2011).However,thereisagrowingawarenessthat prena-talprocessesarelikelytobecriticalforthedifferencesincognitive ability(Raznahanetal.,2012;Shenkinetal.,2004;Walhovdetal., 2012)anddiseaserisk(SchlotzandPhillips,2009)thatunfoldin postnatallife.Recognitionofthishasdriventhesearchfor neu-roimagingfeaturesinlatepostnatallifethatcouldserveasaproxy forearlierdevelopmentalevents.Aleadingcandidateinthiseffort

∗ Correspondingauthorat:LaboratoryforthePsychologyofChildDevelopment andEducation,CNRSUMR8240.Sorbonne,46rueSaint-Jacques,75005Paris,France. Tel./fax:+33140463004/2993.

E-mailaddress:[email protected](A.Cachia).

hasbeentypologiesofcorticalfolding(Manginetal.,2010;Sun etal.,2009).

Unlike quantitative features of the cortical sheet, such as thickness, surface area(Giedd and Rapoport, 2010) and curva-ture/gyrification(Armstrongetal.,1995;Lietal.,2014;Raznahan etal.,2011;Whiteetal.,2010)–whichcantakedecadestoattain thelevelsobservedin adulthood–thequalitativepatternformed bythecharacteristicsetofprimary,secondaryandtertiaryfolds, orsulci,seeninhumanadulthoodisalreadyevidentatbirth(Chi etal.,1977;Manginetal.,2010;Zillesetal.,2013).Inter-individual variationinthisqualitativesulcalpattern–aclassicexamplebeing thepresenceofasingleordoubleparalleltypeoftheACC(Ono etal.,1990),determinedbetween10and15weeksoffetallife(Chi etal.,1977)and presentin76 and24%ofadults respectively– hasthereforebeenusedasamarkerforprenataldifferences.Thus, ACCfoldingpatternhasbeenlinkedtoahostofcognitivedomains includingexecutivecontrol(Cachiaetal.,2014;Fornitoetal.,2004), realitymonitoring(Budaetal.,2011),temperament(Whittleetal., 2009)andsocialcognition(Fujiwaraetal.,2007).Theinferenceof thesestudieshasbeenthatobservedqualitativedifferencesreflect aconstraintimposedbyearlyneurodevelopmentalprocesseson

http://dx.doi.org/10.1016/j.dcn.2016.02.011

1878-9293/©2016TheAuthors.PublishedbyElsevierLtd.ThisisanopenaccessarticleundertheCCBY-NC-NDlicense(http://creativecommons.org/licenses/by-nc-nd/ 4.0/).

thesubsequentabilities.However,acriticalandasyetuntested developmentalassumption–uponwhichexistingandfuture stud-iesofsulcalpatterntypologyasanearlydevelopmentalmarker necessarilyrest–isthatthefoldingtypologiesarestableacross postnatalbraindevelopment.

Here,weprovidethefirstempiricaltestofthisstability assump-tion using 263magnetic resonance imaging (MRI) brain scans, takenfrom75 healthypeoplelongitudinally followedfrom7to 32years.WefocusontheACCbecauseitisacorticalregionthat presentstwoqualitativelydistinctsulcalpatterns(Onoetal.,1990) thatcanbeeasilyandreliablyclassifiedwithstructuralMRIfrom childhood(Cachiaetal.,2014)toadulthood(Pausetal.,1996;Yucel etal.,2001).WeevaluatethelongitudinalstabilityoftheACCsulcal patternfromlatechildhoodtoadulthood,adevelopmentalwindow characterizedbysignificantstructuralremodelingofthebrainas shownbythedrasticACCcorticalthickness,surfaceareaand cur-vaturechangeswithtimeduringthisperiod(Hogstrometal.,2013; Shawetal.,2008).Wecomplementouranalysisofthe longitudi-nalsulcalpatternstabilitybyalsoinvestigatingthelongitudinal changesincorticalthickness.

2. Materialandmethods

2.1. Participants

Seventyfivehealthyparticipants(agerange:7.88–32.8years old; age at first scan: 7.88–25.5 years old; age latest scan: 10.38–32.8yearsold),including26femalesand49 males,were selectedfromalargerprospectivestudy(Gieddetal.,1999)onbrain developmentattheNationalInstituteofMental Health(NIMH) basedonthepresenceofatleasttwolongitudinallyacquiredbrain scanspersubject(Fig.1).Participantswerefreeoflifetimemedical orpsychiatricdisorders,whichweredeterminedthroughclinical examinationandstandardized interview.Psychiatricillnessin a firstdegreerelativewasalsoexclusionary.Furtherdetailsonthis sample hasbeendescribed previously (Gieddet al.,1999).The researchprotocolwasapprovedbytheNIMHinstitutionalreview board.Writteninformedconsentwasobtainedfromparentsand

controlsolder than 18 years, and writteninformed assent was obtainedfromminors.

2.2. MRIacquisition

Allstructuralmagneticresonanceimaging(sMRI)brainscans wereT-1 weightedimageswithcontiguous1.5mmaxialslices, obtainedonthesame1.5-TGeneralElectric(Milwaukee,WI)Signa scannerusinga3Dspoiledgradientrecalledechosequencewiththe followingparameters:Echotime,5ms;Repetitiontime,24ms;flip angle45(DEG);acquisitionmatrix,256×192;numberof excita-tions,1;andfieldofview,24cm.Headplacementwasstandardized aspreviouslydescribed(Castellanosetal.,2001).

2.3. Sulcalsegmentation

Sulcalsegmentation wasperformedwithBrainVISA4.2 soft-ware using theMorphologist toolbox (http://brainvisa.info). An automated pre-processingstep skull-strippedT1 MRIsand seg-mentedthebraintissues.Nospatialnormalizationwasappliedto MRIstoovercomepotentialbiasthatmayresultfromthesulcus shapedeformationsinducedbythewarpingprocess.Thecortical foldswereautomaticallysegmentedthroughoutthecortexfrom theskeletonofthegraymatter/cerebrospinalfluidmask,withthe corticalfoldscorrespondingtothecrevassebottomsofthe ‘land-scape’,thealtitudeofwhichisdefinedbyitsintensityontheMRIs. Thisdefinitionprovidesastableandrobustsulcalsurface defini-tionthatisnotaffectedbyvariationsincorticalthicknessorgray matter/whitemattercontrast(Manginetal.,2004).Foreach par-ticipant,imagesateachprocessingstepwerevisuallychecked.No segmentationerrorwasdetected.

2.4. ACCclassification

AnalysesofACCtypologystabilitywerecarriesoutusingthe first and last scan available for each subject (i.e. total num-ber ofscans=150). Thesulcal pattern of thedorsal partof the ACCwasvisuallyassessedusingthree-dimensional,mesh-based

Fig.2. Thedifferentsulcalpatterntypesoftheanteriorcingulatecortex(ACC)usingOno’snomenclature(twosulcalpatterntypes)andYucel’snomenclature(threesulcal patterntypes).Leftpanel:subjectwithonlyacingulatesulcus(lightblue),labeledas‘single’typeinOno’snomenclatureor‘absent’typeinYucel’snomenclature.Middle panel:subjectwithacingulatesulcusandasmall(<40mm)additionalparacingulatesulcus(inblue),labeledas‘doubleparallel’typeinOno’snomenclatureor‘present’ typeinYucel’snomenclature.Rightpanel:subjectswithacingulatesulcusandalong(>40mm)additionalparacingulatesulcus(inblue),labeledas‘doubleparallel’typein Ono’snomenclatureor‘prominent’typeinYucel’snomenclature.

reconstructionofcorticalfolds (Cachiaet al.,2014)tomeasure the occurrence and extent of local folds (Fornito et al., 2004; Husteretal.,2007;Leonardetal.,2009;Yuceletal.,2001).This three-dimensionalapproachwasusedtoovercome methodologi-calissuesinherenttotheanalysisofthethree-dimensionalsulcal patternoftheACCfromtwo-dimensionalsagittalslices.TheACC sulcalpatternwasassessedbasedontheabsenceorpresenceof aparacingulatesulcus(PCS),avariablesecondarysulcus.ThePCS wasdefinedasthesulcuslocateddorsaltothecingulatesulcuswith acourseclearlyparalleltothecingulatesulcus(Pausetal.,1996; Yuceletal.,2001).Toreducetheambiguityfromtheconfluenceof thePCSandthecingulatesulcuswiththesuperiorrostralsulcus,we determinedtheanteriorlimitofthePCSasthepointatwhichthe sulcusextendsposteriorlyfromanimaginaryverticallinerunning perpendiculartothelinepassingthroughtheanteriorand poste-riorcommissures(AC–PC)andparalleltotheanteriorcommissure; thePCSwasanteriorlylimitedbyanimaginaryverticalline pass-ingthroughtheanteriorcommissure(Yuceletal.,2001).ThePCS wasconsideredabsentiftherewerenoclearlydeveloped horizon-talsulcuselementsparalleltothecingulatesulcusandextending atleast20mm(interruptionsorgapsinthePCScoursewasnot takenintoaccountforthelengthmeasure).Inordertocontrol age-relateddifferencesonbrainsize,allthelengthmeasurementswere performedinMNIspaceafteralinearspatialregistrationusingFSL software(www.fmrib.ox.ac.uk/fsl).

TheindividualACCsulcalpatternswerethenclassifiedwithtwo commonlyusednomenclatures(Fig.2),Ono’snomenclature(e.g.

Cachiaetal.,2014;Fornitoetal.,2006)andYucel’snomenclature (e.g.Budaetal.,2011;Fornitoetal.,2004;Fujiwaraetal.,2007; Whittleetal.,2009).Ono’snomenclature(Onoetal.,1990)provides aclassificationofACCsulcalpatternintwotypes:a‘single’typefor ACCwithoutPCSanda‘doubleparallel’typeforACCwithaPCS. Yucel’snomenclature(Yuceletal.,2001),followingPausworkon thecingulatecortex(Pausetal.,1996),providesaclassificationof ACCsulcalpatterninthreetypes,usingafinerdistinctionbetween ‘present’and‘prominent’PCSbasedonPCSlength(PCSgreaterthan 40mmwerelabelledas‘prominent’).

Theclassification of baseline and follow-up MRIscans were examinedseparatelyandinrandomorder.ACCsulcalpatternwas

doneblindedtopossibleconfoundinginformation,includingthe participant’sageaswellasthelabeloftheACCsulcalpatternin thecontralateralhemisphereandintheothertimepoint. Inter-raterreliability(Cohen’sweightedkappa)wasassessedbyusinga secondrater(O.G.)toevaluate50randomlychosenhemispheres.

Becausequantitativefeaturesofcortexanatomy change dur-ingthedevelopment,includingthePCSlength(Clarketal.,2010), weanticipatedpossiblelongitudinalchangeinACCsulcalpattern labelledwithYucel’snomenclatureandexpectedlongitudinal sta-bilityinACCsulcalpatternlabelledwithOno’snomenclature.

2.4.1. Corticalthickness(CT)analysis

AnalysesofCTchangewerecarriedoutusingallavailablescans fromallparticipants(i.e.totalnumberofscans=263).NativesMRI scansweresubmittedtothewell-validated(Imetal.,2008;Shaw etal.,2008)CIVETpipeline(Ad-Dab’bagh etal.,2006)for auto-matedmodelingofgray/whiteandpialcorticalsurfacesineach scan.Briefly,thisprocessbeginswithlineartransformation, correc-tionofnon-uniformityartifacts,andsegmentationofeachimage intowhitematter,graymatterandCSF(Zijdenbosetal.,2002). Next,eachimageisfittedwithtwodeformablemeshmodelsto extractthewhite/grayandpialsurfaces.Thesesurface representa-tionsarethenusedtocalculateCTatapproximately80,000points (vertices)acrossthecortex(MacDonaldetal.,2000),andaligned witheachotherusinga2-Dsurface-basedregistrationalgorithm toallowcomparisonofequivalentverticesacrossdifferentscans (Lytteltonetal.,2007).

WeexaminedthelineareffectofageonCT,controllingforsex, ateachvertexusingmixed-effectsmodels.Significantvertex-wise maineffectsofagewerevisualizedafterapplyingaFalse Discov-eryRatecorrectionformultiplecomparisonswithq(theexpected proportionoffalselyrejectednullhypotheses)setat5%.

3. Results

3.1. ACCsulcalpattern

ThelongitudinalstabilityoftheACCsulcalpatternwasassessed fromthecomparisonof eachindividualhemisphere atbaseline

Fig.3. Thesulcalpatternoftheanteriorcingulatecortex(ACC)remainsstablefromlatechildhoodtoadulthood.LongitudinalstabilityoftheACCsulcalpatterninasubject witha‘singletype’ACC,withonlythecingulatesulcus(lightblue),andinasubjectwitha‘doubleparalleltypeACC’,withacingulatesulcusandanadditionalparacingulate sulcus(inblue).

Fig.4.Thecorticalthicknessintheanteriorcingulatecortex(ACC)changeswithagefromlatechildhoodtoadulthood.Mapofthelinearageeffect(FDR-correctedT-statistic, q≤0.05)onthecorticalthickness.ThedorsalpartofACCisindicatedwithayellowdashedline.

(mean±sdage:13.7±3.5years;range:7.88–25.5yearsold)and forthelatestscan(20.8±4.9years;range:10.38–32.8yearsold).

Analysis of the individual ACC sulcal patterns using Ono’s nomenclature,withtwoqualitativelydifferenttypes,revealedthat therewere24‘single’typesand51‘doubleparallel’typesinthe lefthemisphereand41‘single’typesand34‘doubleparallel’types intherighthemisphereatthebaseline.Individualqualitative sul-calpatternsofACCwerefoundtoremain-withoutexception -thesamebetweenthebaselineandthefollow-upscans(Fig.3). ThelongitudinalstabilityoftheACCqualitativesulcalpatternwas thereforeof100%intheleftandrighthemispheres.Interrater reli-abilitywas=1.0

Analysisof the individual ACC sulcal patterns using Yucel’s nomenclature(absent, present and prominent), mixing qualita-tive(PCSabsence/presence)andquantitative(PCSlength)features, revealedthattherewere24‘absent’,23‘present’and28 ‘promi-nent’typesinthelefthemisphereand41‘absent’,19‘present’and 15‘prominent’typesintherighthemisphereatthebaseline. Indi-vidualACCsulcalpatternsintheleftandrighthemispherewere foundto slightly changebetween thebaseline and the follow-upscans.Therewere24‘absent’,25‘present’and26‘prominent’ typesinthelefthemisphereand41‘absent’,19‘present’and15 ‘prominent’typesintherighthemisphereatthefollow-up.These longitudinalchangeswerenotrelatedtoqualitativechanges(i.e. switchbetweenthepresenceortheabsenceofaPCS)butwere onlyduetoquantitativechanges(i.e.presentorprominentPCS).In thelefthemisphere,4ACCsulcalpatternsinitiallylabeled ‘promi-nent’werelabeled‘present’atthefollow-upandconversely2ACC sulcalpatternsinitiallylabeled‘present’werelabeled‘prominent’

atthefollow-up;intherighthemisphere,3ACCsulcalpatterns ini-tiallylabeled‘prominent’werelabeled‘present’atthefollow-up andconversely3ACCsulcalpatternsinitiallylabeled‘present’were labeled‘prominent’atthefollow-up.Thelongitudinalstabilityof theACCsulcalpatternusingYucel’snomenclaturethatinvolvesa quantitativecriteria(PCSlength)wasthereforeof80%intheleft andrighthemispheres.Interraterreliabilitywas=0.72.

3.2. ACCcorticalthickness

WealsoassessedthelongitudinalchangeoftheACCcortical thickness(CT)inthesamesample.Deformablemeshmodelswere usedtoextractthewhite/grayandpialsurfacesandcalculatetheCT atapproximately80,000points(vertices)acrossthecortex.Whole brainanalysisrevealedasignificantmaineffectofageonCT, sur-vivingadjustmentformultiplecomparisons,fromlatechildhoodto adulthood,inseveralcorticalareas.Noteworthy,therewasa signif-icantlongitudinalchangeinCTinseveralmedialregions,including thedorsalpartsofACC(Fig.4).

4. Discussion

Ourlargescalelongitudinalstudyprovidesthefirstevidence that the qualitative sulcal pattern of ACC is stable from late childhoodtoadulthood,adevelopmentalwindowofquantitative changesinACCstructure(corticalthicknessandPCSlength).Our findingsupportsuseofsulcalpatterning,basedonqualitativebut notquantitativefeatures,asarelevantmarkertostudylong-term effectsofearlycerebralconstraintsoncognitiveabilities.

Corticalfoldingisahallmarkofmany,butnotall,mammalian brains(Welker,1988).Thedegreeoffoldingincreaseswithbrain sizeacrossmammals,butatdifferentscalesbetweenordersand families(Zillesetal.,2013).Thematuresulcalpatternresultsfrom pre-andperi-natalprocessesthatshapethecortexfromasmooth lissencephalicstructuretoahighlyconvolutedsurface(Chietal., 1977;Haukviketal.,2012).Theprecisemechanismunderlying cor-ticalfoldingisstillunknownbutseveralfactorslikelycontributeto prenatalprocessesthatinfluencetheshapeofthefoldedcerebral cortex,includingcorticalgrowth(ChennandWalsh,2002;Haydar etal.,1999;Kuidaetal.,1996;ToroandBurnod,2005),apoptosis orprogrammedcelldeath(Haydaretal.,1999),differential expan-sionofsuperiorandinferiorcorticallayers(Kriegsteinetal.,2006; Richmannetal.,1975), differentialtangentialexpansion(Ronan etal.,2013)and/orstructuralconnectivitythroughaxonaltension forces(Dehayetal.,1996;HilgetagandBarbas,2006;VanEssen, 1997).Recentprogressincharacterizingbasalprogenitorcellsand thegenesthatregulatetheirproliferationhascontributedtoour understandingofgeneticbasisofcorticalfolding(SunandHevner, 2014,forreview).Thesedifferentearlyprocessesleadtoacompact layoutthatoptimizesthetransmissionofneuronalsignalsbetween brainregions(KlyachkoandStevens,2003)andthustheefficacyof brainnetworkfunctioning.

Thisassociationbetweencorticalfoldingandnetwork function-ingmaymediaterelationshipsbetweenearlysulcalpatternsand laterfunctionaldevelopment(Manginetal.,2010,forreview).For example,werecentlyshowedinalongitudinalstudyin preschool-ers(Borstet al.,2014)thattheACC sulcalpattern, but notthe corticalthicknessorthesurfaceareaoftheACC,atage5predicts theefficiencyincognitivecontrolnotonlyatage5butalsofour yearslater(i.e.,atage9).Ofnote,theefficiencyofcognitivecontrol isonlypartlyexplainedbytheseearlycerebralconstraintsgiven thatitcanbeimprovedbytrainingandpracticeduringchildhood (Diamond,2013forareview)–improvementssustainedby neuro-plasticitymechanisms.Anopenissueisthustodeterminetowhat extentthereceptivitytocognitivetrainingandpracticedepends onearlyneurodevelopmentalconstraintssuchastheACCsulcal pattern.

Thestabilityassumptionofthesulcalpatternwastestedinthis studyfromtheanalysisofACCmorphologyfromlatechildhood toadulthood.Thiscorticalregionandthisdevelopmentalperiod optimizethepossibilitytodetectpossibledevelopmentalchanges insulcalpatterntypes.Indeed,ACCpresentsqualitativelydistinct sulcalpatternsthatcanbereliablyclassifiedwithstructuralMRI fromchildhoodtoadulthood(Cachiaetal.,2014;Pausetal.,1996; Yuceletal.,2001),whichlimitsfalsepositivefindings(i.e.detecting changesinsulcalpatternbecauseofclassificationissuesinstead ofactualmorphologicalchanges).Whileourdataprovidethefirst directevidencethatACCfoldingtypeisadevelopmentallystable traitinhumans,furtherlongitudinalstudieswillberequiredto directlyestablishthatthistraitisalsostableoutsidetheage-range consideredinouranalyses.However,availabledatasuggestthat corticalshapewithintheanteriorcingulateregionismost-likely stableduringthefirstyearsafterbirth,asevidencedbyrecent lon-gitudinalstudiesreportingthatseveralmarkersofcorticalshapeof stablewithintheACCregionduringthefirstyearofpostnatallife, includingcorticalsurfacecurvature(Lietal.,2014),surfacearea(Li etal.,2013)andlocalgyrification(Mutluetal.,2013).Nevertheless, animportantgoalforfuturelongitudinalstudieswillbetestingif ourfindingsregardingthedevelopmentalstabilityoffolding typo-logygeneralizetoothersegmentsofthelifespan,andotherregions ofthecorticalsheet.Testingforgeneralizationtotheentirecortex willraisetheissuesofthedefinitionofthequalitativesulcal pat-ternstobeusedfortheassessmentofeachcorticalarea.Thiswill requirestheestablishmentofadictionaryofhumanbrainfolding patterns(Sunetal.,2009),forinstancebasedonthe‘sulcalroot’

(Regisetal.,2005),namelyindivisibleandstablesulcalunits cor-respondingtothefirstfoldinglocationsduringantenatallifeand thatcanberecoveredafterbirthfromtheanalysisofthelocalcortex curvature(Cachiaetal.,2003)ordepth(Imetal.,2010).

5. Conclusion

Byprovidingdirectevidencethatsulcaltypologyremainsfixed enroutetoadulthood,weprovidefirmergroundforresearchersto harnessthepowerfulopportunityofusingadultfoldingpatternsto retrospectivelystratifycohortsbasedoncategoricaldifferencesin theirearlierbraindevelopment.Thisapproachprovidesameansto assesshowearlylifeinfluencescognitiveabilitiesinlaterlife,which inturnmayilluminatemechanismsoffundamentalimportanceto basicdevelopmentalcognitiveneuroscience.

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