Parentingand HumanBrainDevelopment1

·MichaelI.PosnerMaryK.RothbartUniversityofOregonUSA

Abstract

Thischaptertracesimportantchangesinbrainsystemsbetweeninfancyandadulthood.RestingstateMRIstudieshavetracedchangesinbrainnetworksthatsupporthumanbehaviorthroughoutthelifespan,andtaskrelatedMRIstudies have tracedchangesinnetworksrelatedtoacquiredskills.Weconcentrateonthebrainnetworksinvolvedinlanguageandself-regulationbecausebotharecriticalskillsdevelopingbetweeninfancyandlaterchildhood,

Whileallchildrendevelopsimilarbrainnetworksunderlyinglanguageandself-regulation,theefficiencyofthesenetworksvariesamongpeople.WeexamineevidencefromtemperamentandgeneXenvironmentinteractions to supporttheroleofparentinginthechild’sdevelopment of self-controlandliteracy.Itisimportantforparents,educatorsandthoseinvolvedinshapingpublicpolicytounderstandwhatisknownandtoappreciatewhatremainstobelearned about brain development. While brain development does not in itself dictate the best policies for parenting it may help to inform parents and policy makers on how besttosupport childdevelopment.

Keywords

Attention,EEG,GeneXEnvironment,Language,fMRI, Self-Regulation,State

1TheresearchforthischapterwassupportedinpartbygrantsN00014-15-1-2022,andN00014-15-2148fromtheOfficeofNavalResearchtotheUniversityofOregon.TheauthorsappreciatethehelpofPascaleVoelkerinthisresearch.

Theoreticalbackground

Introduction

Itisincreasinglypossibletoidentifybrainnetworksinvolvedinhumandevelopment,including development of thoseskillsthatallowthechildtobetterunderstandandadapttotheirphysicalandsocialworlds.We have learned a great deal about how the brain changes with development, and we report here on methods and important findings on brain development. Do these advances in brain study have direct implications for what parents should do and how policy makers should be spending their money? In our current state of knowledge we think not.

Advances in the study of the human brain do allow us to better understand the developing child. They even provide support for the proposal by Hebb (1949 ) and others (Posner & Rothbart, 2007) that neural networks may be a key to developing an integrated psychology. However, brain findings at present have only weak connections to behavior, and it is at that level where parenting occurs. To offer advice, wewould need to extrapolate from brain findings to behavioral findings. For example, brain studies may help us identify a very early age at which parents can enrich language experience. However, what the nature of the intervention should be, e.g. whether to increase the number of words the parent directs toward the child, or ask the parent to repeat using a new word in a number of settings, we cannot say.

On the other hand, parents do benefit from learning about brain development .They can take into account such findings as the degree to which children’s self-regulation is generally slow to develop, the early importance of infant orienting, and the importance of individual differences among children, but this does not result in specific advice for parents.

Apreviousreviewof parenting was basedlargelyonstudiesofdevelopmentalpathology, concludedthatparentactionsinfluencebraindevelopment,butcalledformoreresearchlinkingthebehavior oftypicalchildrentothebrain(BelskydeHaan,2011). In this review we concentrate on normal brain development. Thischapterconcentratesontwoareas of brain research, languageandandself-regulation.We dealonlywiththebrainofthedevelopingchild,leavingasidethesubstantialnewresearchon adaptationsofthecaregiver’sbraintoparenthood(forreviewsseeAbraham,Hendler,Zagoory-Sharon,Feldman,2016;Kim,Strathearn,Swain,2016).

Ouremphasisinthischapterisonmethodsthatcanilluminatebrainnetworksinvolvedinlanguageandattention. Theneedtounderstandlanguageanditsdevelopmenthaslongbeenrecognized,andanextensiveliteratureisavailableonchildren'sorderofacquisitionoflanguage-relatedskills.They demonstrate that languagedevelopmentisnotsimplyaprocesstaughtbyparentsortheirsurrogates.Rathertheacquisitionoflanguagedemonstratesaclearinteractionbetweengeneticeffectsandtheenvironmentintowhichtheinfantisborn.Becauseofmore recent studiesinbraindevelopment,we have learned muchmore aboutthedetailsofthisprocess, givingusabetterunderstandingofhowlanguage develops

Wealsoexamineattentionandthechild’sdevelopmentofself-regulation.Asinlanguage, brainnetworksofattentionareduetocommongeneticfactorsininteractionwith experience..SomeoftheindividualdifferencesintheefficiencyofattentionnetworkshavebeentracedtogeneXenvironmentinteractionsthatinvolveparentinginconjunctionwithchildtemperament.Individualdifferencesintheefficiencyofexecutiveattentionarerelatedtoparents’reportsoftheirchildren’sabilitytoregulatetheirbehavior(EffortfulControl;Rothbart,2011;RothbartRueda,2005).EffortfulControl(EC) and self regulation as measuredinchildhoodhasbeenfoundtohaveextensive consequencesforsuccessfuloutcomesofadults(Moffittetal.,2011).

Methods of examining brain changes

Tobeginthischapterwereview methodsforexaminingbrainchangesduringdevelopment.Theseincludeearlystudiesof thebrainsofinfantsandchildrenwhocametobestudiedafterdeath,andnewermethodsforexaminingstructuralandfunctionalchangeusingbrainimaging.

Anatomy

Methodsforexaminingbrainchangesduringdevelopmentbeganwithstudiesofthebrainsofinfantsandchildrenwhodiedearlyinlife,followedbynewermethodsthatexamineimagesofthelivingbrain. Thehumanbrainroughlyquadruplesinweightbetweenbirthandsixyearsofage, by then reaching90%ofitsadultvolume (BrownJernigan,2012).From1939-1967, Conel(1939-1967)examinedinfantandchildbrainsfromautopsies.Overthedecades,hewasabletoexamineunderamicroscopechangesinnumberofsynapses,theirdensityandtheincreasedcomplexityofdendritictrees.Inallareasofthecortex,hefoundthatsynaptic densityincreasedafterbirthandthendeclined,reachingadultlevelsfirstintheprimarysensorycortexandmuchlaterinfrontalareas(HuttenlocherDabholkar,1997).

StructuralImages

Structuralimagingusingmagneticresonanceimaging(MRI)providesfurthersupportfortheincreaseandthendecreaseinneurons(greymatter)with age, ,asmeasuredbybothcorticalthicknessandsurfacearea(Wierenga et al.,2014).However,evenlargerchangesinbrainsizeareduetoincreasesinmyelinatedfibers(whitematter),whichincreaselinearlyfrominfancytoadulthood(Zilles,2005).Theaxonsoflongprojectionsaremyelinatedearlierthatthoseconnectingthetwohemispheres,whilemyelinintheassociationareastakesthelongesttime to developandshowsthelargestindividualdifferencesduringdevelopment(seeBrownJernigan,2012,foradditionalinformationonstructuralchangesindevelopment).

Structuralfindingspointtotheimportanceofconnectivitybetweenneuralareasduringdevelopment.Functionalimagingofadultsusingpositronemissiontomography(PET)andfunctionalmagneticresonanceimaging(fMRI)hasconsistentlyshownthatmostcommonhumantasksinvolveanumberofbrainregions,with these oftenincludingboththecortexandsub-corticalareas(PosnerRothbart,2007).Because widelyseparatedbrainareasare connected incarryingoutevenverysimplecognitivetasks,suchasshiftingattentionbetweenareasofthevisualfield, theroleofwhitematterconnections is criticalintheefficiencyandtimingoftaskperformance.

Taskrelatedfunctionalimaging

Functional MRI cognitive research beganbysubtractingimagesofthebrainobtainedduringanexperimentaltaskfromthoseiinacloselyrelatedcontroltask.Whilesubtractionprovidesevidenceonthebrainareasinvolved in a task,methodssuchasElectricalandMagneticEncephalographyandDynamicCausalModelingcanindicatewhenandinwhatorderthesebrainareasareactivated(Posner,Sheese,Odludas,Tang,2006).Functionalimagingbasedoncorrelations of MRI activation across brain areascanhelpexaminecommunicationbetweenthese areas(Posner et al.,2006).Mosttasksinvolveanetworkofbrainareaswhichmustbeorchestratedduringperformance.Inmanytasks,youngchildrenactivatemorebrainareas during a taskandoftenshowmoreextensiveactivationwithineachareathanyoungadults(BrownJernigan,2012).

WhiletaskrelatedfMRIcantracechangeswithdevelopment,theagesthatcouldbestudiedhavebeenlimitedbytheabilityofchildrentocarryouttaskinstructions. However,itisnowpossibletotracethechangesinbrainconnectivitythatoccurduringearlydevelopmentbyexaminingbrainactivitywhilethepersonisatrest(rsMRI; Raichle,2009).

RestingStateImaging

Restingstatemethodscanbeappliedatanyagebecausetheydonotrequiretheuseofatask.Oneofthebrainnetworksknowntobeactiveduringrestistheexecutiveattentionnetwork(Dosenbachetal.,2007;Fairetal.,2009).Studieshaveshownthat frontalmidlinenodesoftheexecutiveattentionnetworkarepresentduringthefirstmonthsoflife(Gaoetal.,2013),althoughconnectivitywithotherbrainstructuresissparse.Asignificantincreaseinconnectivityisevidentby2yearsofage(Gaoetal.,2009)andcontinuestodevelopslowlyacrossthechildhoodyears(Fairetal.,2009).Duringinfancyandearlychildhood,mostbrainnetworksinvolveshortconnectionsbetweenadjacentbrainareas,butlongconnectionsimportantforself-regulationdevelopslowlyoverchildhood(Fairetal.,2009;Gaoetal.,2009).Althoughsomeofthese results maybeduetomovementofyoungchildrenduringthescan,behavioral data also indicatethat manylongconnectionsdevelopinlaterchildhoodandbeyond. For example, there is a largeimprovementin reaction time(RT)between7yearoldsandadultswhenperformingthe Attention Network Test (ANT), whicinvolveslongconnectionsbetweensensoryandmotorareas(Voelker, Rothbart, & Posner,2016).

Incontrast,theabilitytoresolveconflict,which is necessary in daily life to maintain a coherent behavior designed to reach goals, and whichinvolvesthe executive attention network,showslittleornoimprovementbeyondsevenyears(Ruedaetal.,2004). Thesefindingssuggestthatcontrolstructuresrelatedtoexecutiveattentionmaybepresentininfancy, but they do not have the connectivity required to exertfullcontrolovervoluntary behavior untillater in development.Wediscussexecutivecontrolmorefullyunderthesectionondevelopmentofattention.

IndividualDifferences

Ourunderstandingofbrainnetworkscommontoallhumansmakesitpossibletoviewindividualdifferencesasvariationsintheefficiencyofthesenetworks.Networkefficiencyisinfluencedbyvariationin genesandbythegeneXenvironmentinteractionsthatshapethechild’stemperament.

Temperament

Thedevelopmentoftheindividualchilddependsupontheirtemperamentanditsinfluenceonthechild’sinteractionwiththeirenvironment(Rothbart,2011).Temperamentreferstothebasicdimensionsofreactivitytotheenvironmentandself-regulationthatdifferamongchildren.Parentsoftendonotbecomebelieversintemperamentuntilafterthebirthoftheirsecondchild(Putnam,Sanson,Rothbart,2002).Itthenbecomesclearthatthesametechniquesofchildrearingthatworkedwellwithoneinfantmay not be effectivewiththenewbaby.n.Temperamentinvolvesgeneticfactorsbutisnotlimitedtothem.IntermediatebetweentheDNAinheritedbythechildandtheeffectsofparentingaretheenvironmentaleffectsthatinfluencetheexpressionofDNA,whichiscalledepigenetics.ThereissomeevidencethatmethylationofDNAmayaffectsuchdimensionsoftemperamentasnegativeaffectandsurgency(Fuemmeleretal.,2016),butadditionalstudiesareneededinthisrelativelynewfield.

Dimensionsoftemperamentsuchassurgency(iactivitylevelandpositiveaffect),negativeaffect,(fear,frustrationanddistress),togetherwithorientingandsoothabilitycan be studied in caregiverreports based on observatonoftheirinfants(Putnam,Sanson,Rothbart,2002;Rothbart,2011).Later,effortfulcontrol,whichmeasurestheabilityofchildrentoregulatetheirownbehavior,isreportedbyparents.Effortfulcontrol(EC)hasalsobeenshowntorelatetodevelopmentofthe brain’sexecutiveattentionnetwork.Ininfancy,self-regulationdependsmoreuponalertingandorientingnetworkswhichbythenarewelldeveloped.Thesenetworkssustainthewakingstateandallowtheinfanttobesoothedthroughdistraction.

Wewillbeexamininghowgenesinteractwiththeenvironmentduringinfancyandearlydevelopment.However,earlytemperamentratingsareoftenmorepredictiveoflaterbehaviorthanare directpredictionsofbehaviorfromgenes.Thisisprobablybecausetemperamentsummarizestheinfluenceofalargenumberofgenes,eachonewithasmalleffect,andbecausetemperamentmeasuresincludeeffectsofexperienceaswellasgenes.Moreover, experience cannot be inferred from an environmental stimulus, because the same stimulus can lead to quite different experience depending on the child’s temperament (Rothbart, 2011). However, understandinghowtemperamentandgenesarerelatedtotheenvironmentcanservetoimproveourunderstandingofthemechanismsofdevelopment.

GenesandEnvironment

Imagingstudieshaverevealedtheimportanceofconnectivitybetweenbrainareas.Infact,efficiencyof connectionsbetweenneuralareasinnewborn infantspredictslatercognitivefunction.In a large longitudinal study, Leeand colleagues(2017)foundthatdiffusiontensorimaging(DTI)ofwhitematter connectivityatbirthpredictedbetterperformanceoncognitivetestsatagetwo.Thisfindingemphasizes theimportanceofgeneticandprenatalfactorsinlayingdownthebasicconnectivestructureonwhichmuch ofperformanceisbased.Althoughmanygenesarecommontoeveryone,differencesinattentionand cognitionarepartlydependentuponvariationswithinthegenome.Thishasbeenshownclearlyinstudiesof attentionnetworks(Fan, Fossella, Summer, Wu, & Posner,2003). Ofcourse,whichgeneticvariationsareinheriteddependsupontheparents,butnotupontheactionsofparents.

Intheory,itispossibletomanipulatetheenvironmenttoprovideeitheranenrichedoranimpoverished environment.Ethicalissuesobviouslymakeitdifficulttoconductexperimentalstudieswithhumans, althoughnaturalvariations in environmentscanprovidequasi-experimentalstudies.Animalresearch has providedevidencethatcorticalthicknesscanbechangedbyplacing the mice in environmentsof increased complexity (Diamond,Krech, Rosensweig,1964).Theseare important findings andwediscussthembelowin thesectiononinterventions.

Development of Language and Attenition

In this section we review studies of brain development that can be linked to some of the most important tasks undertaken by parents and children starting in infancy.

Language

Thestudyoflanguageacquisitionmakesmajorcontributionstoourunderstandingofhumanbrain development.Thereareseveralreasonsforthis.Languageisaspeciesspecificcharacteristicofallhuman cultures.wheras the specificlanguagelearnedisaclearcontributionofthecaregivers.Moreover,studiesof adulthumanlanguageusehavebenefittedfromimagingstudiesofthehumanbrain,sothatsomeofthenetworksinvolvedareknown.

Theoveralllevelofachild’s languageskillhasapowerfulimpactontheabilitytoformrelationshipswithothersandtosucceedinawiderangeofcognitivetasks.Improvementinourunderstandingofhowtooptimizelanguagedevelopmentand totreatandrehabilitatedisordersoflanguagedevelopmentwillhaveprofoundconsequencesforbothabasicunderstandingofhumandevelopmentandforhumansociety.

Everyonerecognizestheinfluenceoftheparentsinthespecificlanguagethechilddevelopsbutoftendo notrecognizehowearlythatinfluenceisshown.Ifgivenanopportunity,twomontholdinfantsdisplayaclearpreferenceforthelanguagespokenbytheparentsoverothers(Dehaene-LambertzHouston,1998), andtheyalsopreferthemother’svoicetoothervoicesspeakingthesamelanguage.Anotherclear demonstrationofparentalinfluenceistheimportanceofchild-directedspeechinvocabularydevelopment(Montag,Jones,Smith,2015)

Whathasbecomeclearinthelasttwentyyearsishowparenting helpsshapethebrainsystemtoallowfor specificrecognitionofthephonemesofone’snativelanguage.Thephonemeisthefundamentalconstituentofalltheworld’slanguagesthatallowsdiscriminationamongwordsinthelanguage.Theinfant’sabilityto recognizephonemesisdemonstratedbypresentingasinglephoneme(e.g.,b)severaltimesinarow,untiltheinfantshowsreducedorientingtoitspresentation,andthenchangingtoanothercloselyrelatedphoneme(e.g.,p)toseeiftheinfantshowsanincreasedresponse.Ifthechangedsoundiswithinthesamephonemicboundary(e.g.differentformsofb)thereislittleornoincreaseinorienting,butorientingisclearlyincreased ifaphonemicboundaryiscrossedtop,evenwheninbothcasesthephysicalchangeinthesignalisequal.

Phonemes

Forsometimewehaveunderstoodthatlanguageacquisitionproceeds,roughlyspeaking,throughstages coveringtheperiodfrombirthtoaboutage5.Duringthistimechildrenmovefromperceivingbasicdifferencesinthesoundandrhythmicaspectsofhumanlanguageingeneraltocontrollingthedetailed grammaticalcontrastsintheirnativelanguage.Recentresearchhasprovidedsurprisingandimportantnewinsights,particularlyintowhatyounginfantsbringtothistaskandhowrapidly earlynativelanguagelearningbegins.

INSERT BOX 1 ABOUT HERE

Between6and12monthsinfants’perceptionofthedistinctionbetweennativeandnonnativephonemes increases(WerkerTees,1984). Whilenon-nativeperceptiondeclines,nativespeechperceptionshows asignificantimprovement.Forexample,Japaneseinfants’discriminationoftheEnglishr-ldistinctiondeclines between8and10monthsofage, andatthesametimeAmericaninfants’discriminationofthesamesounds improves.(Kuhletal.,2008). Thesediscriminationspredictlaterlanguageskills,butin oppositedirections.Improvednativephonemediscriminationpredictsbetterlaterlanguageskills,whilerelativelybetternon-nativediscriminationisassociatedwithpoorerlaterlanguage.

OnewayofthinkingaboutthesechangeshasbeendevelopedbyKuhl(2010).Shesees nativelanguageimprovementastheresultofspecificdevelopmentsinthe neuralareasprocessingspeech,whereas non-nativelanguageimprovementreflectsthebasicauditoryabilitytodiscriminatephonemessuchasisfoundin non-humananimals.Duringearlyphoneticdevelopmentthespeechpatternsdirectedtowardinfantsby caregivers tend toexaggeratethefeaturesthatseparatephonemesinthenativelanguage.Ofcourse,non-nativephonemesdonothavetheadvantageofsuchspeech.Thus,speechdirectedtowardtheinfantiscrucialtotheelaborationoftheneuralsystemsrelatedtospeechrecognitionandalsototheinfant’sproductionofspeech duringthelatterpartofthesecondyear.

Theimportanceofsocialinteractioninthelearningofphonemesissupportedbythefindingthatnon-nativephonemes(e.g.,mandarinphonemesfornativeEnglishspeakers)canbemaintainedbyactivetutoring oftheinfant,butthetutoringmustinvolveapersonandnotmerelyacomputerizedimage(Kuhl,Tsao,Liu,2003; See also Box 1).TheextentoflearningofSpanishphonemesforEnglishspeakersexposedtobilingualspeech waspredictedbythedegreeoforientingtowardthetutor,suggestingthatorientingisoneaspectoftheadvantageofactualpeopleoverelectromagneticdisplays(Conboy, Brooks,Meltzoff,Kuhl,2005).Another link to orienting is that infantsoflessthantenmonthsormorethantwoyearsofagelookprimarilyattheeyeswhenviewing pictures offaces.However,duringtheperiodwhenphonemiclearningtakesplacethe infants lookmorefrequentlyatthemouth(LewkowiczHansen-Tift,2012), See also Box 1.

Improvementintheperceptionofnativephonemeshas also been found to betemporallyrelatedtochangesinwhitematter tractsthatconnectnodesofthespeechperceptionnetwork.Betweenthemiddleofthefirstyearoflifeand3 yearsofage,thereismaturationofaxonsenteringthedeepercorticallayersfromthesubcorticalwhitematter.Theseaxonsprovidethefirsthighlyprocessedauditoryinputfromthebrainstemtohigherauditory corticalareas(MooreGuan,2001).Thetemporalcoincidencebetweenthischangeandinfants’phoneticlearningindicatesanimportantbrainpathwaytolanguage.Laterwereviewmorespecificwhitematter changesthatoccurpriortolearningtoread,andshowhowtheypredictlaterperformance.

BuildingWordsandSentences

Studiesoftheneurobiologyoflanguage in speech and in the ability to learn to readhavelongbeendominatedbytheclassicalviewthatemphasized theroleofthreewell-circumscribedcerebralregionswithinthelefthemisphere:Broca'sareaintheinferior frontallobe,forplanningandexecutingspeech,Wernicke'sareaatthejunctionbetweenthesuperior temporalandtheparietallobes,fortheanalysisandidentificationofspeech,andtheangulargyrus,fororthographictophonologicaldecodingduringreading.However,eventheearlieststudiesofimagingfoundactivityinotherareas,bothcorticalandsubcortical.Amongthemistheanteriorcingulate,apartoftheexecutiveattentionnetwork,whichbecomesactivewhenparticipantsobtain auseforanoun(Petersenetal.,1987),andwhich isconsistentlyactivatedbytheresolutionofconflictbetween activateditems.

InfantscanbereadsentenceswhiletheyareatrestinanMRIscanner., sentencesread tonewborninfantsactivatethesameposterior(Wernicke’s)andanterior(Broca’s)brain areasfoundtobeactivewhenadultsprocesslanguage(Dehaene-Lambertz,Hertz-Pannier,Dubois,2006). Ofcourse,theinfantsdonotreallyunderstandthesentences.Thelefthemisphereasymmetryfoundinmostadults, however, doesnotappeartostartuntilthesecondyearoflife(Emerson,Gao,Lin,2016). Overthefirstfiveyearsoflifethereisasteadyimprovementintheabilitytouseandunderstandwords.Parents mayguidethisabilitythroughthevocabularyandspeechpatternstheyusewiththeirchildren. One important example is joint attention in which the child tends to learn the word indicating the object of their parents attention (Baldwin, 1995). While joint attention skill is correlated with vocabulary acquisition it is not a sufficient cause and some children learn vocabulary in spite of having difficulty in joint attention (Akhtar & Gernsbacher, 2007).

IntheacquisitionofEnglishandsimilarlanguages,childrenof18to24monthsbegintoform early sentencesbycombininganounandverb,ortwonouns,usingthebasicwordorderoftheadultlanguage,and omittingfunctionwords(the,is)andinflections(pluralandpasttense)(Brown,1973).Childrencanknow thatsomeunstressedelements,likethefunctionwords,shouldbeincludedinadultsentences,evenwhen theydon’tproducetheseelementsintheirownspeech.

Itisestimatedthatchildrenofprofessionalclassparentsareexposedto26millionwordsbyage3,whilechildrenfromwelfarefamilieshavebarelyhalfthatexposure(HartRisley,2003). There are clear correlations between exposure to words and later fluency in speech and reading, but many other factors may be involved in these correlations. There have also been efforts to use electronic technology to increase word exposure, but judging from the findings with phonemes (see box 1) these may not beeffective.

Bilingualism

Formuchoftheworld’spopulation,knowledgeoftwoormorelanguagesstartsearlyinlife. Incomparisonwithmonolingualpopulations,theuseoftwolanguagesoften leadstoreducedvocabularyandgreatereffortinachievingmasteryoftheprimarylanguage(CostaSebastian-Galles,2017).

However,bilingualismhasalsorelatedtoexecutiveattention. Wehavepreviouslydescribedtheinvolvementoftheexecutiveattentionnetworkinthebrain’sprocessing oflanguage, and there is evidence that thisnetworkshowsgreaterefficiencyinbilingualsthanin monolinguals.Foragivenlevelofperformance,thereisreducedactivationinbilingualswhohavelearned twoormorelanguagesatthesametimeoflife.Reducedactivationindicatesthatforbilingualslesseffortis neededtoresolveconflict.Ithas also been arguedthattheimprovedefficiencyoftheexecutiveattention networkleadstoimprovedgeneralcognitionbybilinguals.According to this view (Bialystak, 2017)bilingualshavemultiplewordmeaningsactivatedfromtheirlanguagesandmustexercisecontroltomaintaintheuseofonelanguage. Switchingbetweenlanguagesalsorequirescontroloperationslikeresolvingconflictthatinvolveexecutiveattention.Theexerciseofthesecontroloperations,particularlyearlyinlife,mayleadtoimprovedabilityforcontrolduring mental arithmetic, problem solving and other forms of thought. .Thereisstillagreatdealofcontroversyaboutwhether bilingualsdodisplaybettercognitiveprocessesintasksinvolvingconflictresolution(Bialystok,Craik,Luk,2012).Nonetheless,CostaandSebastian-Galles(2017)arguethatthebrainnetworkunderlying executiveattentionisimprovedinbilinguals,andBialystok(2017)concludesthatexecutiveattentionisthemostlikelymechanismfortheimprovedabilitytoresolveconflictinbilinguals..

Advances inneuroimagingtechniqueshaveaddedtoourunderstandingoftheadvantagesanddisadvantagesoflearning multiplelanguages.Forbilingualswhostartearlyinchildhood,the two or morelanguagesareactivated and storedtogether in the brain. Thisrequiresthepersontoresolveconflictinunderstandingandusingwordsandtobeadeptinswitching betweenthetwolanguages (Bialystok, 2017). Languages learned later in life, for example in high school, are not stored together and there is less automatic interference when retrieving items.

Reading

Oneofthebestpredictorsofsuccessinacquiringliteracyisthenumberofwordstowhichthechildhas been exposedbythreeyearsofage. Itisalsopossibletolearnmoreaboutthepotentialreadingskillofthechild byrecordingelectricalactivityfromthescalpinresponsetospoken phonemes duringinfancy.Thebetterthe brain’s representation of phonemes,theeasieritwillbetoacquirethewrittenlanguage(Molfese,2000).

Howcouldthisbe?Wehavereviewedabovetheimportanceofexperienceintheveryearlydevelopmentofthephonemesystem.Muchthesameistrueoftheabilitytounderstandindividualwords.Experiencewithauralspeechhelpstheinfantandchildtodevelopastrongrepresentationofaurallanguage.Exposureto highlevelsofbackgroundnoisecaninterferewiththesuccessfulshapingofthephonemicsystem(Cohen, Glass,Singer,1973).Goodrepresentationofphonemesandwordsareimportantbecauseoneaspectof acquiringtheabilitytoread(literacy)isbeingabletoreferwrittenwordstospeechsounds.

Soundingoutindividuallettersandblendingthemintowholewords during reading iscalleddecoding.Ifchildrenhaveawordintheirauralvocabulary,theyare thenabletointerpretthe word meaning justastheywouldforthespokenword.Decodingskillisanimportantstepintheacquisitionofliteracy and imagingstudieshaveshownthatchildren whohavedifficultylearningtoreadshowpooractivationofthephonologicalcodesfromprint.A remediationprogram(McCandliss,Sandak,Beck,Perfetti,2003)thathasbeensuccessfulinimproving children’s decodingusesacomputertointroducewordswithaconsistentsoundpattern.Over20sessions,new phonemesareintroducedandthechildpracticesdecodingthem.Byscanningthebrainsofchildrenbeforeandafterthistrainingithisprogram was found to be successfulinteachingdecodingandalsoinproducingactivationofthephonologicalcodeinpoorreaders,whopreviouslydidnotsuccessfullyactivatethesound basedcodeduringreading.[AM1] This program’s use of words that differed in a single phoneme (e.g. bat vs pat) helped the child learn the importance of individual sounds in creating words. Parents may also use this method for teaching their own children decoding skills and the Dr. Suess books shown one example of the use of phoneme discrimination skills in reading.

Nevertheless,thosewhohavelearnedonlydecodingskillsarenotnecessarilyfluentreadersand often do notchoosetoread.Fluentreadingdependsuponthedevelopmentofavisuallybasedwordformsystem.Thissystemhasbeenlocalizedtothefusiformgyrusoftheleftoccipitallobe (Molko et al 2002).

Evenin 4-6month old ifnatsthereisevidenceofstrongorganizationofafacerecognitionsystemalong with otherhighlevelvisualbrainareassimilarbutnotidenticaltothoseinadults(Deenetal.,2017).Thereisalsoevidencethattheneuralpathwaysintothevisualwordformareaarepresentwellbeforeliteracybegins(Sayginetal.,2016).Moreover,theefficiencyoftheseearlypathways predicthowwellthechildwillbeabletoreadvisualwordsseveralyearslater,afterliteracyisachieved.Theprocessofdevelopingthevisualwordformsystem,inadditiontopromotingfluentreading,alsoallows facerecognitiontobecomemorelateralizedtoareasoftherighthemisphere(Dehaene,Cohen,Morais,Kolinsky,2015).Indeedthehigherthelevelofreadingskill,thestrongeris thelateralizationofthefacesystem.Becauseofthisinfluenceoffluencyonthefacerecognition system,tooearlyacquisitionofliteracy may havehaveadetrimentaleffectofaspectsoffacerecognition.Theacquisitionofliteracy,unlikebilingualism,doesnotappeartoinfluencetheexecutiveattentionsystemdescribedinthenextsectionofthischapter(Dehaene,Cohen,Morais,Kolinsky,2015).

Animportantwaytoimprovechildren’sprintedvocabularyisfortheparenttoengageinreadingwiththechild.Thereissubstantialevidencefrombothhighandlowincomecountriesthatinteractivereadingwith thechildimprovesvocabulary,literacyacquisitionanddirectedattention(Engleetal.,2007,Montagetal.,2015; Vally Murray,Tomlinson,Cooper,2015).

AttentionandSelfRegulation

Theimportanceofparentingindevelopingbrainnetworksrelatedtoattentionandself-regulationis perhapslessobviousthanforlanguage,butattentioniscertainlyofnolessimportancethan,and iscriticalto languageacquisition.Evidencethatself-regulationinvolvesahighlevelexecutiveattentionnetworkhasled ustogrouptheareasofattentionandself-regulationtogether.Adultstudieshaveidentifiedthreebrain networks,whichinvolvedifferentfunctionsofattention.Thesearethealerting,orientingandexecutivecontrolnetworks(PetersenPosner,2012).Inanatomicallyorientedfunctionalimagingstudies,theorientingnetworkisoftencalledthefrontalparietal(FP)network,whiletheexecutivenetworkiscalledin theCingulo-Opercularnetwork(CO; Dosenbachetal.,2007).Thenetworks,theiranatomy,timecourseand neuro-modulatorsinvolvedareillustratedinFigure8.1.Thereareothervaluableframeworksfortheclassificationofattention,forexample,differentiating bottomupfromtopdowncontrol(AmsoScerif,2015). Webelieve,however,thatitisimportanttodistinguishbetweentheorientingandexecutivenetwork,bothof whichcanhavetopdowncomponents,inordertograspthetransformation in attentionthattakesplacebetweeninfancy andearlychildhood.

INSERTFIG1ABOUTHERE

SeveralofthenetworksinvolvedinattentioncanbeexaminedusingtheAttentionNetworkTest(ANT),developedtostudyindividualdifferencesinthe efficiency of the alerting,orientingandexecutivebrain networks(Fan,McCandliss,Sommer,Raz,Posner,2002;Rueda et al.,2004) In addition to adult research theANTcanbeusedtostudyattentioninchildrenofabout4yearsandabove (Posner et al 2014).

TheANTusesdifferencesinreactiontime(RT)betweentaskconditionstomeasuretheefficiencyofeach network.Eachtrialbeginswithacue(orablankinterval,intheno-cuecondition)thatinformstheparticipant thatatargetwillbeoccurringsoon,orwhereitwilloccur,orboth.Thetargetalways occurseitheraboveorbelowfixation,andconsistsofacentralarrow,surroundedbyflankingarrows.Theflankerspointeitherinthesamedirectionasthetargetarrow(congruent)orintheoppositedirection (incongruent).SubtractingRTsofcongruentfromincongruenttargettrialsprovidesameasureofconflictresolutionandassessestheefficiencyoftheexecutiveattentionnetwork.SubtractingRTsobtainedinthedouble-cuecondition(wherethecueservesasawarningbutdoesnotprovideinformationaboutthetargetlocation)fromRTsintheno-cuecondition, givesameasureofalertingduetothepresenceofawarningsignal.SubtractingRTstotargetsatthecuedlocation(spatialcuecondition)fromtrialsusingonlyacentralcue, givesameasureoforienting,becausethespatialcue,butnotthecentralcue,providesvalid informationonwhereatargetwilloccur.TheANTthususesreactiontimedifferencestomeasureindividualefficiencyofthealerting,orientingandexecutivenetworks(Fanetal.,2002).Insubsequentwork, ANTreactiontimeshavebeenshowntobesomewhatreliable(Macleodetal.,2010)andhavebeenused totracethedevelopmentofattentionnetworksfrom4yearstoadulthood.

Belowwediscussthedevelopmentoftheattentionnetworksininfancyandchildhood.Attentionininfancyislessdevelopedthanlaterinlifeandthefunctionsofalerting,orientingandexecutivecontrolarelessindependentduringinfancy.Wefirstexaminealertingandorienting,andthenconsiderexecutiveattentioninrelationtothedevelopmentofself-regulation.Themethodformeasuringthesevariablesmustbedifferentininfancythanlater,whenvoluntary responsescanbedirectedbytheexperimenter.Effortshavealso beenmadetodesigntasksthatcanbeperformed byinfantsthattapintothesamenetworksofbrainareasshowninFigure8.1.

Alerting

Theearlylifeoftheinfantisverymuchconcernedwithchangesinstate.Sleepdominatesatbirthandthewakingstateisrelativelyrare..Thenewborninfantspendsnearly¾ofthetimesleeping(ColomboHorowitz,1987),andmanyofthechangesinthealertstatedependuponexternalinput.Arousalofthecentralnervoussysteminvolvesinputfrombrainstemsystemsthatmodulateactivationofthecortex. Asinadults,primaryamongtheseisthelocuscoeruleus,thesourceofthebrain’sneuromodulator norepinephrine.Ithasbeenshown thattheinfluenceofwarningsignalsoperatesviathisbrainsystem, sincedrugsthatblocknorepinephrinealsopreventthechangesinthealertstatethatleadtofasterreactiontimeafterawarningsignal(MarroccoDavidson,1998).Itislikelythattheendogenouschangesin alertnessduringwakingthattakeplacewithoutexternalinputalsoinvolvethissystem.

Thereisadramaticchangeinthepercentageoftheinfant’stimeinthewakingstateoverthefirst3 monthsoflife.Bythe12thpostnatalweek,theinfanthasbecomeabletomaintainthealertstateduring muchofthedaytimehours.Thisabilitystilldependsheavilyuponexternalstimulation,muchofitprovided bythecaregiver.

Withinthewakingstate,thelevelofalertnessvariesovertime.Theabilityofapersontosustainattention isfrequentlymeasuredbyexaminingvariationsinperformanceonataskoverarelativelyextendedperiodof time,such astheContinuousPerformanceTasks(CPT).IntheCPTapersonmustrespondtooccasionaltargetswhileignoringmorefrequentnon-targets.Variationsinthelevelofalertnesscanbeobservedbyexaminingthepercentageofcorrectand/oromittedresponsestotargetsorthrough measuresofperceptualsensitivity(d’)overtime.Withyoungchildren,thepercentageofchildren abletocompletethetaskcan alsoindicatematurationaldifferencesintheabilitytosustainattention.Inastudyconductedwith preschoolers,only30%to50%of 3to4yearoldswereabletocompletethetask,whereasthepercentageroseto70%for4to4½yearoldsandcloseto100%above age 4 ½ (Levy,1980). Eventhoughthelargestdevelopmentofvigilanceseemstooccurduringthepreschoolperiod,adults continuetoshow greater abilitytosustainperformancethenchildrenthroughmiddleandlatechildhood,especiallyundermoredifficulttaskconditions.Theydonotreachtheadultleveluntilapproximately13yearsofage(Curtindale, Laurie-Rose,Bennett-Murphy,Hull,2007).Thisdevelopmentmay have importantimplicationsfor parentsandotherswhoexpect achildcan payattentionoverextendedperiodsevenwhenthebrain’snetworks donotyetsupportit. The slow development of the alerting and executive network may caution parents about unrealistic expectations for their child’s control of attention.

Preparationobtainedfromwarningcues(phasicalertness)canbemeasuredbycomparingthespeedand accuracyofresponsetotargets withandwithoutwarningsignals(Posner,2008).Presentationof warningcuespriortotargetsallowsthepersontogetreadytorespondbyincreasingtheirstateofalertness. Thiscommonlyresultsinfasterresponses,althoughitmayalsocausedeclinesintheaccuracyoftheresponse,particularlyatshortintervalsbetweenwarningcueandtarget(Posner,1978).Thewarning signalinterruptstherestingstateandimprovesalerting.Thebrainnetworksactiveatrestandduring attentivestatesarequitedifferent(Raichle,2009).

Onewaytoexaminebrain changes following a warning isbyregisteringpatternsof brain-generatedelectricalactivation(EEG)throughelectrodesplacedonthescalpwhilewarningcuesareprocessed.Typically,severalhundredmillisecondsafteracuepredictingtheupcomingoccurrenceofatargetthere is anegativevariationofbrainactivitythat is sustainedupuntilthetargetappears(Walteretal.,1964).ThiselectrophysiologicalindexiscalledtheContingentNegativeVariation(CNV)and itappearstoberelatedtoasourceofactivationintheanteriorcingulatecortexand adjacentmidprefrontalcortex(SegalowitzDavies,2004).TheCNVandotherslowwaveshavebeen relatedtochangesfrom the resting state to the attentive state usingfMRI(Raichle,2009).TheamplitudeoftheCNVincreaseswithage, especiallyduringmiddlechildhood.as observedovertherighthemisphere(Jonkman,Lansbergen,Stauder, 2003)TheearlycomponentsoftheCNVariseinfrontalcortex,suggestingthattheCNV is relatedto maturationofthefrontalaspectsofalertingnetwork.

DeficitsinthealertingnetworkhavebeenidentifiedasacauseofAttentionDeficitDisorder(HalperinSchultz,2006). This is one reason for thefrequentwarningtoparentstoinsuregoodsleeppatternsintheirchildren, sincesleepdeprivationimpairsthemaintenanceofthealertstate.Frequentbreaksduringtasksmayalsobeusefulinhelpingtomaintainthealertstateinyoungchildren.

Orienting

Orientingtosensoryinformationinvolvesabrainnetworkthatincludesthedorsalandventralparietallobe,frontaleyefieldsandsubcorticalareasincludingthepulvinarandsuperiorcolliculus(CorbettaShulman,2002;PetersenPosner,2012).Whileorientingismostoftenstudiedusingvisualevents,thesourceoforientingseemstoinvolvethesamebrainnetworkirrespectiveofsensorymodality.However, thesiteatwhichattentioninfluencesinput dependsupontheinputmodality.

Forvisualevents,themostfrequentmethodofstudyingorientingininfancyinvolvesthe trackingofsaccadiceyemovements.Asinadults,thereisacloserelation,butnotidentity,betweenthedirectionofgazeandthe direction of the infants’covert orienting .Eyemovementscanbedrivenbyexternalinputfrombirth(RichardsHunter,1998);however,thesystemcontinuestoimprove over many years inmakingprecisemovementsdirectlytothetarget. Infanteyemovementsoftenfallshortofthetarget, requiring a series of sort movements beforereachingthefoveawherevisionismostacute(Clohessy,Posner,Rothbart,2001).Althoughnotaseasyto track,ashiftofattentionviatheorientingnetworkwithouteyemovements(covertorienting)likelyfollows asimilartrajectory.Studieshave examinedthecovertsystembyuseofbriefcuesthatdonotproduceaneyemovementfollowedbytargetsthatdo,showingthatthespeedoftheeyemovementtothetargetisenhancedby thecueandthisenhancementbecomesgreateroverthefirstyearoflife(Butcher,2000).Inmorecomplex situations,forexample,whentherearecompetingtargets, improvementmaycontinue for longerperiods.

Fornewborninfants,controloforientingisinitiallylargelyinthehandsofthecaregiver.By4 months,however,infantshavegainedconsiderablecontrolin the ability to disengagetheirgazefromonevisuallocation andmoveittoanother,andgreaterorientingskillinthelaboratoryisassociatedwithlowertemperamentalnegativeemotionandgreatersoothabilityasreportedbyparents(Johnson,Posner,Rothbart,1991).

Orientingtosensoryinputisamajormechanismforregulationofdistress.Infantsoftenhaveahardtimedisengagingfromhighspatialfrequencytargetsand may becomedistressedbeforetheyareabletomoveaway fromthetarget.Caregiversmaythen attempttosoothetheirinfantsbybringingtheirattentiontonovel objects.Asinfantsorient,theyareoftenquieted,andtheirdistressappearstodiminish.Inonestudy (Harman,Rothbart,Posner,1997),infantswerefirstshownasoundandlightdisplayand oftenbecamedistressed, butwhenorientedtoaninteresting competingevent,however, theirsignsofdistressdisappeared. Assoonasorienting to the novel object stopped,however,theinfants’distressreturnedtoalmostexactlythelevelsshownpriorto presentationofthesoothingobject.Aninternalsystem,whichwastermedthedistresskeeper,appearsto holdacomputationoftheinitiallevelofdistress,sothatitreturnsiftheinfant'sorientationtothenoveleventislost.Interestingly,infantswerequietedbydistractionforaslongasoneminute,withoutchangingthelevelofincreased distressreachedonceorienting to the distracting stimulusended(Harman, Rothbart,Posner, 1997).

Infantsdeveloptheabilitytoorientattentiontoexternalstimulationearlyinlife,yet aspectsoftheattentionsystemthatincreasetheprecisionandvoluntarycontroloforienting continuetodevelopthroughoutchildhoodandadolescence (Rueda et al 2004).Mostinfantstudiesexamine control of eyemovements.Bythetimechildrencan followinstructionsandrespondtostimulationbypressingkeys,bothovertand covertorientingcanbemoreeasilymeasured.Thecuingtaskhasbeenwidelyusedtostudythedevelopmentofvisualorientingoverthelifespan,and severalstudieshaveexaminedthedevelopmentoforientingduringchildhood.Despiteaprogressiveincreaseinorientingspeedtovalidcues duringchildhood,datagenerallyshownoagedifferencesto thebenefitinorientingprovidedbythecuebetween5-6yearsofageandadulthood(EnnsBrodeur,1989).There is an age-related decreaseinthetimetodisengagefromafalsecueandshifttothetarget(the costoforienting;EnnsBrodeur, 1989;Schul,Townsend,Stiles,2003;WainwrightBryson,2002).Aspectsof orientingrelatedtocontrolofdisengagementandvoluntaryorientation,whichin adults dependoncorticalregions oftheparietallobe,improvewithageduringchildhood.

Restingstatebrainimagingdatacanbeusedtomeasurefunctionalconnectivitybycalculatingcorrelations betweenareasthat are active duringimaging.Thesestudieshaveindicatedthattheorienting systemshowsgreaterconnectivityduringinfancythandobrainareasassociatedwiththeexecutiveattention network(Gaoetal.,2009).Connectionschangeoverthelifespan.Infantsshowmostlylocalconnectionsand childrenage9alsoshowmanyshorterconnectionsthandoadults. Adultsshowmoresegregationofthe orienting and executive attention networksandlongerconnectionsforboth(Dosenbachetal.,2007;Fairetal.,2007, 2008).Whilethereisevidencethatyoungerparticipantsmovemoreandthiscouldreducetheabilitytoimagelong connections(Power, Barnes, Snyder, Schlaggar, & Petersen,2012),inourviewitseemsunlikelythatthisartifactwillchangetheconclusions discussedabove.

Animportantlandmarkforparentsistheoccurrenceofjointattention(Mundyetal.,2007),whenthedevelopingchildbeginstopayattentiontowhatthecaregiverisattendingto.Usuallyachievedduringthefirsttwoyearsoflife,thisallowstheparenttoprovidelabelsfortheobjecttowhichtheyattend,andcan greatlyexpandthechild’svocabulary.Unliketheacquisitionofphonemesdescribedpreviously,thechild at this age doesnotorienttotheparent’smouth,butrathertheparentandchildorienttoacommonobjectofattention. Thereissomecontroversyoverwhetherjointattentionissufficientto associate awordwith itsobject(SmithYu,2014)orwhethersomeadditionalassociativeprocessisneeded.Inadults,itisclearthatlearningand retrievalofwordmeaningsinvolvestheexecutivesystem(Petersen & Posner, 2012).Sincetheexecutivenetworkisbecoming increasinglyconnectedduringthepreschoolyearsitislikelytobemoreinvolvedinthisformofword learning.

Jointattentionis oneexampleinwhichthepresentationofnovelobjectsaidsthechildinlearningwords.Animagingstudy (Eggebrecht etal.,2017)scanned37childrenatboth12and24monthsduringthechild’sefforttoinitiateactsofjointattention.Theconnectivityfound betweenthevisualsystemandthefronto-parietalorientingsystemduringinitiationofjointattentionincreasedbetween12and24months.Therewasnosignificantinvolvementofthecingulo-parietal(executiveattention)network.However,iflearninganewassociation between a visualobjectanditsnameisanoutcomeofjointattention,assuggestedbySmithandYu (2014),executiveattentionwouldalsobecomeinvolved.(Petersen, Fox, Posner, Mintun, & Raichle,1987).

Wehaveoutlined atransitionbetweenthebrainnetworksresponsibleforcontrolin infancyandthoseat3-4yearsandlater.At7months,control,includingtheregulationofdistress(Rothbart, 2011)mainlyinvolvestheorientingnetwork,butby4years,theexecutivenetwork becomes dominant in self regulation. Wedonotbelievethatcontrolthroughorientingendswiththepreschooltransition.Weviewadultsashavingdualcontrol.Looking awayfromdisturbingorhighlyarousingeventsisclearlyamajorcopingstrategyinadults(RothbartSheese,2007),andorientingisoftenacriticalelementintrainingattentionalcontrolasinmeditation.However,thegrowinginfluenceofexecutivecontrolallowstheperson’sinternallycontrolledgoalsto become increasingly dominant.

ExecutiveAttention

In adults theexecutiveattentionnetworkinvolvestheanteriorcingulategyrusandtheanteriorinsula(also calledthecingulo-opercularnetworkinfMRIstudies (PetersenPosner,2012).Thesetwoareasofthehumanbrainhaveauniqueprojectioncell.Thiscell,theVonEconomoneuron(Allman,Watson,Tetreault, Hakeem,2005),isthoughttobeimportantincommunicationbetweenthecingulateandotherbrainareas.Thisneuronisnotpresentinmacaquemonkeysandexpandsgreatlyin frequencybetweengreatapesandhumans.ThetwobrainareasinwhichVonEconomoneuronsarefound arealsoinclosecommunication,evenduringtherestingstate(Dosenbachetal.,2007). Moreover,thereissomeevidencethatthefrequencyofthe von Economoneuronsincreasesbetweeninfancyandlater childhood(Allmanetal.,2005). There are otherimportantdifferencesin theevolutionofconnectivitybetweennon-humanprimatesandhumans.Anatomicalstudiesshowagreatexpansionofwhitematter,whichhasincreasedmoreinrecentevolutionthanhastheneocortexitself(Zilles,2005).Inourview,theVonEconomoneuronandtherapidandefficientconnectivityitprovides,isamajorreasonwhyself-regulationinadulthumanscanbesomuchstrongerthaninotherorganisms.Wealsothinktherelativelyslowdevelopmentoflong-termconnectionstodistantbrainareasallowstheexecutivenetworktoprovide increasingcontrolatlaterages.

Itisdifficulttoassessexecutiveattentionininfantsbecauseasoutlinedabove,caregiversprovidemostof theregulationofinfantbehavior. Effortfulcontrolisahighlevelfactorderived fromparentreportsonchildren’s temperament(RothbartRueda,2005).Thisfactorisdefinedastheabilitytowithholdadominantresponse inordertocarryoutanon-dominantone.Parentsobservingtheirchildren’sspecificbehaviorin dailylifesituations(forexample,puttingawaytoysoncommand,etc.)canreadilyrespond to questionsthatrelatetothisfactor.Thiscanbedoneforchildrenabout2yearsofageandolder,althoughaspects of orienting and emotion canbemeasuredfromearlyinfancy(Rothbart,2011).Belowtwoyearsofage,temperamentobservations include scales likeorienting, fear, anger, soothability andpositiveaffect(Rothbart,2011).Childrenaboveage3-4canperformtasksthatinvolvevoluntary responding,suchaspressingkeystovisualinput.Inmultiplestudies,higherECinquestionnairemeasuresispositivelycorrelatedwithmoreefficientperformanceinresolvingconflict in laboratory tasks(executiveattention)(RothbartRueda,2005).

Theproblemsinmeasuringcontrolbytheexecutiveattentionnetworkduringinfancyhadledustobelievethattheexecutivenetworkwasnotpresentuntilaboutage3-4.Whileitisclearthatsomevoluntarycontrolisexercisedininfancy,forexample,4montholdinfantscanmakeantisacades(Johnson,Posner,Rothbart, 1994),itispossibletoattributethatcontroltotheorientingnetwork.However,wewereabletoobtaindirectevidenceofexecutiveattentionininfancyfromastudyof7-month-oldinfantsviewingvisualdisplays (Berger,Tzur,Posner,2006;Wynn,1992). Infantsorientlongerwhen a displayisinerror(Wynn, 1992)andthisbehaviorwasassociatedwith activity inasetofEEG electrodesatthefrontalmidlinethat localizetotheanteriorcingulate,animportantnodeoftheexecutivenetwork.Thetypicalregulationof behaviorfoundinadults,thatis,toslowdownfollowinganerror,seemednottoemergeuntilaboutage3years(Jones,Rothbart,Posner,2003).

Wehavefollowedtheemergenceofexecutiveattentionfrominfancytolaterchildhoodbyusing anticipatorylookinginavisualsequencetask(Clohessy,Posner,Rothbart,2001;Haith,Hazen,Goodman,1988).Inthis task ,visual stimuliareplacedinfrontoftheinfantinafixedand predictablesequenceoflocations.Theinfant’seyesaredrawnreflexivelytothestimuli at these locations becausetheyaredesignedtobeattractiveandinteresting.Afterafewtrials,someinfantswillbegintoanticipatethelocation ofthenexttargetbymovingtheireyespriortothetargetpresentation.Anticipatorylookingoccurswith infantsasyoungas3.5to4months(Clohessy,Posner,Rothbart, 2001;Haith, Hazen, & Goodman, 1988).However,a sequence can also involveconflictwhen thecorrectmovedependsonthepresentlocationoffixation. For example, consider the sequence 1,2,1,3. When fixated at position 1 there is a strong conflict between position 2 and 3 requiring a memory of where one was before moving to 1. Theabilityto correctlyanticipateduringconflictdoesnotoccuruntilabout18-24monthsofage(Clohessy,Posner,Rothbart, 2001).

Correctanticipationin conflict trials, however,didnotallowacleardeterminationofwhethertheorientingortheexecutivenetwork was controlling theresponses,evenwhen they involvedanticipations. However,inalaterstudyof18-24montholdstheerrorrelatednegativity(ERN)followinganincorrectresponsewasfoundtoberelatedto childrens’ performanceinthesequencelearningtask,andboththeERN andsequencelearningpredictedchildrens’ performanceonanexecutiveattentiontaskatage2and questionnaire measures of effortfulcontrol atage3(Barbero,2016).

AtthreeyearsofageweusedtheSpatialConflictTask(Gerardi-Caulton,2000)whichinducesconflictbetweentheidentityandthelocationofanobject.Onsometrialsthe responsekeythatmatchedthetargetidentitywas onthesamesideofthescreen(compatible)andsomeontheoppositeside(incompatible).Atthreeyears,theabilitytorespondcorrectlywhentherewasconflictinthesequentiallookingtaskwasrelatedtotheabilitytoresolveconflictintheSpatialConflicttask(Rothbart,Ellis,Rueda,Posner,2003). Recall that we also found at age 3-4 errors made in a conflict task began to produce slowing on the following trial. Thesefindings converge to demonstratethatconflictisresolvedbytheslowdevelopmentoftheexecutiveattentionnetwork during earlylife.

AnimportantfMRIstudy(Fjelletal.,2012)involved750participantsfrom4to21yearsof age andusedatask inwhichavisualtargetissurroundedbyeithercongruentorincongruentflanker stimuli. Theparticipantsneeded to resolveconflictbetweenthetargetandflankersintheincongruentcondition, and theabilitytoresolvesuch conflictisameasureoftheefficiencyofexecutiveattention.Upuntil7yearsofage,thesizeoftherightanteriorcingulatewasthebestpredictorof childrens’abilitytoresolveconflict,asmeasuredbyreactiontimedifferencesbetweencongruentandincongruentflankers.Inthesamestudy,diffusiontensorimaging(DTI) suggestedthatoverallreactiontime (RT) ismostrelatedtotheefficiencyofwhitematterconnections.Thisstudy supportstheanatomyresultsdescribedpreviouslyinillustratingtheimportanceof white matterconnectivity betweentheanteriorcingulateandotherbrainareasasakeycomponentofself-regulation.

Thedevelopmentofexecutiveattentionhasalsobeentracedintotheprimaryschoolperiod(Ruedaetal.,2004),using RTtoincongruentflankers tomeasure children’s abilitytoresolveconflict.Overall,children’s reactiontimesweremuchlongerthanadults,butconsiderabledevelopmentinthespeedofresolvingconflictwasobservedfromage4toabout7yearsofage. Theabilitytoresolveconflictontheflankertask, asmeasuredbyincreasesinRTanderrorswith incongruentcompared tocongruentflankers,remainedaboutthesamefromageseventoadulthood. Whenthedifficultyoftheconflicttaskisincreasedbyotherdemands, however, suchasswitchingrulesorholdingmoreinformationinworkingmemory,furtherdevelopmentofconflictresolutionisfound evenbetweenlatechildhood andadulthood(Davidson,Amso,Anderson,Diamond,2006).

Thefindingstodatesuggestthatorientingisplayingsomeoftheregulatoryrolesinearlyinfancythatwilllaterbeexercisedbytheexecutivenetwork.Parentingmayalsoplayanimportantroleinthe earlydevelopmentoftheexecutiveattentionnetwork,perhapspartlythroughthepresentationofnovelobjectsthathavebeenshowninadultstoactivatetheexecutivenetwork(Shulmanetal.,2009).Parentemotionalavailabilitymay alsobeimportantintheearlydevelopmentofexecutiveattention. Onestudyoffiveyearolds, usingago-nogoRTtask,ameasureofdelayofgratificationandathirdtaskrequiringfollowingcomplex rules,foundthatchildrenwhoseparentsshowedhighemotionalavailabilityhadbetterscoresinthelasttwotasksandmoreefficientnetworksrelatedtothego-nogotask,althoughinthistasktherewasno differenceinperformance(Shneider-Hassloffetal.,2016).

Attentionand the Control of Emotion

Theventralportionofthe anterior cingulate (ACC)andadjacentorbitalfrontalcortexconnectsmainlytolimbicregionsand itsfunction as would be expected from it sconnections is relatedtothecontrolofemotions(Bush,Luu,Posner2000;Etkin,Egner, Peraza,Kandel,Hirsch,2006).Themoredorsalpartofthecingulateconnectsmorestronglytocorticalareasinthefrontalandparietallobes and thus to cognitive control.ThereisevidenceofincreasedconnectivitybetweenthedorsalACCandauditoryareaswhenattendingtospeech,whereasswitchingtovisualinputisreflectedinincreased connectivitybetweentheACCandoccipitallobe(Crottaz-HerbetteMenon,2006).Thedevelopmentaldatacitedinthelastsection(PerlmanPelphrey,2001)andsomenewadultfindings(Jahn,Nee, Alexander,Brown,2016)supportseparatefunctionsfortheventralanddorsalACCandshowthat bothdevelopstronglybetween5and8yearsofage.Thereisfurther evidenceofsomesubstantialoverlapin theventralACCbetweennegativeemotionandcognitivecontrolsuggestingthesetwofunctionsarenotalwaysseparate(Shackmanetal.,2011).

Parentreportsoftheir7montholdinfants’positiveaffect are related to reports of infants’ duration of orienting and predictthelaterto resolveconflictatage7(Posner, Rothbart, Sheese, & Voelker,2014).Researchsuggeststhatevenat9-10months,someaspectsofsustainedorientingcaninvolvetheexecutivesystem.Forexample,Kochanska,MurrayandHarlan(2000) foundthatchildren’sfocusedattention observed inthelaboratoryat9monthspredictedmeasuresoftheir effortfulcontrolinpreschool.

Studiesof restingstateMRIat birthsuggestearlydevelopmentofanodeinthemid-prefrontalcortexadjacentto emotionalcontrolpartsoftheACC(Gaoetal.,2009).Thesefindingsprovidesomesupportfortheideathatemotionalcontroldevelopsmorequicklythancognitivecontrolduringearlylife,althoughthereisstrong overlapintheirlaterdevelopment.Whilethedataarenotcompletelyclearonthispoint,itisofobvious important forparentstofosterthedevelopmentofemotionalcontrolduringinfancythrough soothing and other methods.

ExecutiveControlandAdolescence

Onestrikingfeatureofadolescentbehavioristhetendencytowardhighlevelsofrisktaskingsuchasdrugandalcoholabuse,accidentaldeath,andunprotectedsex (Eatonetal.,2008).Thesebehaviorsappeartodependinpartupontherelativespeedofmaturationoffrontalcontrolsystemsasopposedtostriatalrewardsystems.Accordingtothisview,theactivationofthereward systemscanoverwhelmtheabilityofcognitiveandemotionalcontrolsinthisagegroup.

Oneillustrationofthisideaisfoundinastudyofchildren,teenagersandadultsinago,no-gotask involvingthepresentationofhappy,sadorneutralfaces(Casey,Galvan,Somerville,2016;Somerville, Hare,Casey,2011).Whilethethreeageshadsimilarcorrectresponses,theteenagersmademorefalsealarms,thatis,theymorefrequentlypressedthekeywhenanon-targetwaspresented,thanyoungerorolder ages.Abrainscanconductedduringthistaskshowedgreateractivityinteensthanotheragesintheventralstriatum,anareaofthebrainrelatedtorewardprocessing.Therightventralfrontalareawasmainly activatedinno-gotrials,andwasthoughttobeinvolvedintheactualinhibitionofaresponse;activationin thisareadeclinedlinearlywithageandwaspositivelycorrelatedwithfalsealarms.Theauthorsinterpretthese findingsassuggestingastrongerinfluenceofrewardstimuliontheteenagebrainthanfoundatother ages.However,thereislaterevidencethatduringtheteenageyearsthereisachangefromcontrolbytheventral(emotional)tomoredorsal(cognitive)midlineareas,suggestingan increase incognitivecontrolduringtheteenageyears(Silversetal.,2016).

AdifferentmethodologicalapproachistoexaminerestingstateMRIacrossages.Althoughtherearemanymethodologicalissuesincomparingdifferentages,includingpossiblechangesinamountofmovementinthescanner,itappearsthatventralstriatalrewardareasshowgreateractivityduringtheadolescentyears than for children and adults. Theventralstriatumisoneofthefewbrainareasinwhichthetaskrelatedactivationdiscussedintheprevious paragraphconvergeswiththerestingstatedata(Stevens,2016).