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The role of selective attention on academic foundations: A cognitive neuroscience perspective

STEVENS, Courtney, BAVELIER, Daphné

Abstract

To the extent that selective attention skills are relevant for academic foundations and amenable to training, they represent an important focus for the field of education. Here, drawing on research on the neurobiology of attention, we review hypothesized links between selective attention and processing across three domains important to early academic skills.

First, we provide a brief review of the neural bases of selective attention, emphasizing the effects of selective attention on neural processing, as well as the neural systems important to deploying selective attention and managing response conflict. Second, we examine the developmental time course of selective attention. It is argued that developmental differences in selective attention are related to the neural systems important for deploying selective attention and managing response conflict. In contrast, once effectively deployed, selective attention acts through very similar neural mechanisms across ages. In the third section, we relate the processes of selective attention to three domains important to academic foundations: language, literacy, and mathematics. [...]

STEVENS, Courtney, BAVELIER, Daphné. The role of selective attention on academic

foundations: A cognitive neuroscience perspective. Developmental cognitive neuroscience , 2012, vol. 2S, Suppl.1, p. S30-S48

DOI : 10.1016/j.dcn.2011.11.001 PMID : 22682909

Available at:

http://archive-ouverte.unige.ch/unige:91940

Disclaimer: layout of this document may differ from the published version.

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ContentslistsavailableatSciVerseScienceDirect

Developmental Cognitive Neuroscience

jou rn a l h om epa g e:h t t p : / / w w w . e l s e v i e r . c o m / l o c a te / d c n

The role of selective attention on academic foundations:

A cognitive neuroscience perspective

Courtney Stevens

a,∗

, Daphne Bavelier

b,c

aWillametteUniversity,900StateSt,Salem,OR97301,USA

bUniversityofRochester,Brain&CognitiveSciences,Rochester,NY14627,USA

cUniversityofGeneva,FPSE,CH-1211Geneva4,Switzerland

a rt i c l e i n f o

Articlehistory:

Received19July2011

Receivedinrevisedform28October2011 Accepted1November2011

Keywords:

Selectiveattention Distractorsuppression Development Training

a b s t r a c t

Totheextentthatselectiveattentionskillsarerelevantforacademicfoundationsand amenabletotraining,theyrepresentanimportantfocusforthefieldofeducation.Here, drawingon researchontheneurobiology ofattention, we reviewhypothesized links betweenselectiveattentionandprocessingacrossthreedomainsimportanttoearlyaca- demicskills.First,weprovideabriefreviewoftheneuralbasesofselectiveattention, emphasizingtheeffectsofselectiveattentiononneuralprocessing,aswellastheneural systemsimportanttodeployingselectiveattentionandmanagingresponseconflict.Second, weexaminethedevelopmentaltimecourseofselectiveattention.Itisarguedthatdevel- opmentaldifferencesinselectiveattentionarerelatedtotheneuralsystemsimportantfor deployingselectiveattentionandmanagingresponseconflict.Incontrast,onceeffectively deployed,selectiveattentionactsthroughverysimilarneuralmechanismsacrossages.In thethirdsection,werelatetheprocessesofselectiveattentiontothreedomainsimportant toacademicfoundations:language,literacy,andmathematics.Fourth,drawingonrecent literaturesontheeffectsofvideo-gameplayandmind-braintrainingonselectiveatten- tion,wediscussthepossibilityoftrainingselectiveattention.Thefinalsectionexamines theapplicationoftheseprinciplestoeducationally-focusedattention-trainingprograms forchildren.

© 2011 Elsevier Ltd. All rights reserved.

Academicachievementis determinedbya varietyof factorsincludingeducationalopportunity,socio-economic status(SES),socialaptitudes,personalitytraits,andcog- nitiveskills(see,forexample,Brooks-GunnandDuncan, 1997;Wentzel,1991;WentzelandCaldwell,2006).Among the latter, theability to focus onthe taskat hand and ignoredistraction,alsotermedselectiveattention,appears tohavereverberatingeffectsonseveraldomainsimportant toacademicfoundations,includinglanguage,literacy,and mathematics.Whileitisimportanttorecognizethatmany

Correspondingauthor.Tel.:+15033706470;fax:+15033706512.

E-mail addresses: cstevens@willamette.edu (C. Stevens), daphne@cvs.rochester.edu(D.Bavelier).

factorsdetermineacademicachievement,thefocusofthis paperwillbeexclusivelyonselectiveattention.

Selectiveattentionreferstotheprocessesthatallowan individualtoselectandfocusonparticularinputforfurther processingwhilesimultaneouslysuppressingirrelevantor distracting information. The competinginformation can occurbothexternally,asinextraneousauditoryorvisual stimulationintheenvironment,orinternally,asindistract- ingthoughtsorhabitualresponseswhichgetinthewayof performingthetaskathand.Asmoststudiesinthelitera- turehavefocusedonthefilteringofexternalinformation, thisreviewwillfocusprimarilyontheability,whenpre- sentedwithacomplexenvironment,toselecttherelevant dimensionsfor the taskathand and respondappropri- ately. Furthermore, the focus will be on the preschool andearlyschoolyears,althoughtheconsiderableneural 1878-9293/$seefrontmatter© 2011 Elsevier Ltd. All rights reserved.

doi:10.1016/j.dcn.2011.11.001

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developmentoccurringduringinfancyinthesedomains isacknowledgedanddiscussedelsewhere(e.g.,Dehaene, 1997; Kuhl, 2004; Richards, 2003; Sheese et al., 2008;

XuandSpelke,2000).Drawing onresearchfromcogni- tivescienceandcognitiveneuroscience,weproposearole forselectiveattentioninthreedomainsimportanttoaca- demicfoundations(language,literacy,andmathematics).

Inthesectionsbelow,wepositbothpossibleneuralmecha- nismslinkingselectiveattentiontoeachdomain,aswellas broaderimplicationsforeducationalandremediationpro- gramsbasedonexistingdataontheplasticityofselective attention.

1. Neuralbasesofselectiveattentioninadults

Studies of the neural bases of selective attention in adults provide a useful framework for considering the effectsofselectiveattentiononacademicfoundationsdur- ingdevelopment.Thesestudieshaveoftenbeendivided intothreeseparatesetsofquestions.Onesetofquestions concernshowselectiveattention,oncedeployed,modu- latesinformationprocessing.Asecondsetofquestionsis focusedonthe mechanism(s)by which selectiveatten- tionisdeployed,includingtheneuralnetworksthatorient attentiontoparticularaspectsoftheenvironment.Finally, athirdsetofquestionsrelatestotheneuralmechanisms thatactivelymanagecompetitionfromirrelevantstimuli, particularlywhenthesearemoresalientthanthetarget itself.Thesethreesetsofquestionsareconsideredinturn below.

1.1. Influenceofselectiveattentiononinformation processing

“Everyoneknowswhatattentionis...”wroteWilliam Jamesin1890.“Itisthetakingpossessionbythemind,in clearandvividform,ofoneoutofwhatseemseveralsimul- taneouslypossibleobjectsortrainsofthought...Itimplies withdrawalfromsomethingsinordertodealeffectively withothers...”(James,1890,pp.403–404).Despitethese reassuringwords,ithastakenthelast50yearsofresearch tounderstandhowattentionactstoregulatetheflowof informationmadeavailableinthebrain.Wearepastthe ragingdebateofthe1960soverwhetherattentionoperates byapplyinganearlyversuslatebottleneckoninformation processing(Broadbent,1958;DeutschandDeutsch,1963).

Thishasbeenresolvedbyresearchshowingthattheeffects ofattentioncanbeobservedfromneuralregionssupport- ingearlyperceptualprocessingallthewaytohigher,more integrativedecisionareas(e.g.,ColbyandGoldberg,1999;

Martinezetal.,2001;O’Connoretal.,2002).

Thefirstproperlycontrolledstudytoidentifytheinflu- ences of selective attention on neural processing used a clever experimental paradigm that manipulated the focusofselectiveattentionwhileholdingallelseconstant (Hillyardetal.,1973).Inthispioneeringexperiment,Steven Hillyardusedtheevent-relatedbrainpotential(ERP)tech- nique to examine the temporal dynamics of selective auditoryattention.Adultparticipantswerepresentedwith twosimultaneousstreamsofauditorytonesdeliveredvia headphonesseparatelytoeachear.Participantsattended

selectively toone earand detectedrare high-frequency tonesintheattendedchannel.Standard(non-target)tones presented totheattendedearelicitedlargerN1s(nega- tivitybetween80and120ms)thanthesametoneswhen presentedintheunattendedchannel.Thisindicatedthat selectiveattentionmodulatedearlyneuralprocessing.Fur- ther,assomeportionoftheattentioneffectmirroredthe distributionoftheunderlyingERPcomponents,thismod- ulationappearedtoactatleastinpartasagaincontrol mechanismoninput-drivenneuralactivity.Thisparadigm illustratedwhatbecameknownastheHillyardPrinciple:In ordertoassesstheeffectsofselectiveattention,responses shouldbe comparedto thesamephysical stimuli while holdingoverallarousallevelandtaskdemandsconstant, suchthatallthatdiffersisthefocusofselectiveattention.

Since thisinitialreportin1973,severalstudieshave applied theHillyard Principletoexamine the effects of selectiveattentiononinformationprocessingindifferent modalitiesorwhendirectedtodifferentstimulusattributes (for reviews, seeHillyard et al.,1987; Hopfinger et al., 2004).Forexample,usingpositronemissiontomography (PET)andfunctionalmagneticresonanceimaging(fMRI), severalstudiesreportattentionalmodulationthroughout multiple cortical and even subcortical processing areas (Corbettaetal.,1999; O’Connoret al.,2002;Schoenfeld et al., 2007—but notethat attentioneffects in the ear- liest areasmay reflect feedbackmodulationas opposed to modulations of the initial afferent volley, e.g., see Martinezet al.,2001).Further,whenselectiveattention is directed toparticular stimulusattributes(e.g., shape, color,ormotion)enhancedactivityisobservedincortical areasassociatedwithprocessingthatattribute(Corbetta etal.,1999;Motter,1994;Schoenfeldetal.,2007).Simi- larly,whenattentionisdirectedtowardparticularobject classes associated with specialized cortical areas (e.g., faces,houses),activityismodulatedinthoseobject-specific corticalregions(Wojciuliketal.,1998).

The attentional gating observed with non-invasive neuroimagingtechniquesarisesfromapush–pullmech- anismbywhichthecoding oftask-relevantinformation is enhanced whilethat of task-irrelevantinformation is suppressed.Severalstudiesdocumentthatattentionalters theselectivityofneuronsinthehierarchyofvisualareas, especiallybyimprovingtheencodingoftask-relevantfea- tures (Jehee et al., 2011; Murrayand Wojciulik, 2004;

Reynolds et al., 2000).Neurophysiological studies from awakebehavingmonkeysfurthershowthatattentionacts byallowingneuronstofireasifonlytheattendedobject werepresentintheirreceptivefield,diminishingtheeffect ofdistractorsfallinginthesamereceptivefield(Reynolds and Desimone, 2003; Sundberg et al., 2009; Verghese, 2001).Asreceptive fieldsincrease in sizefromearlyto later corticalprocessingareas,themodulatoryeffects of selectiveattentionbecomemoremarked,especiallyinlater areaswheretargetanddistractorsaremorelikelytofallin thesamereceptivefieldgiventheirlargersize(Lucketal., 1997).Inaddition,severalrecentstudiesmakeclearthat increasinginformationprocessingoftheattendedstimulus requires engaging neurons that have the best discrimi- natorypowerbetweenattendedanddistractingfeatures.

Thiswillnotnecessarilybetheneuronalpopulationsmost

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selectivetotheattendeddimension,butrathermaybeneu- ronalpopulationsthatfallbetweenattendedanddistractor features,asinitiallyexemplifiedbyNavalpakkamandItti (2007) (seealso,Ma etal.,2011; Scolariand Serrences, 2010).Thus,itiscriticaltoalsoconsiderthenatureofdis- tractorsandtheirrelationshiptotheattendedtargetwhen interpretingattentionalmodulations.

1.2. Neuralsystemsusedtodeployselectiveattention

Theabovediscussionfocusedontheeffectsofselective attentiononmodulatingtheflowofinformationprocess- ing.Anadditionalfundamentalissueconcernstheoriginof theseattentionalmodulations,thatis,theneuralsystems engagedtoorientselectiveattentiontothelocation,object, or featureofinterest. Theguiding ofselectiveattention iscommonlyagreedtobecontrolledbybothbottom-up signals,withsalientinformationguidingtheallocationof attention,aswellasinatop-downfashionwherebythe goalsoftheparticipantsalsoshapeattentionalallocation (BuschmanandMiller,2007;CorbettaandShulman,2002;

Desimone and Duncan, 1995; Kastner and Ungerleider, 2000; Yantisand Serences,2003).Such stimulus-driven and goal-directed ways of controlling attentionrely on partiallyoverlappingnetworksofbrainareas,and,while guidedbyseparableoperatingprinciples,interactalmost constantlytoultimatelydetermineattentionallocation.

Afruitfulapproachtocharacterizingtheoperatingprin- ciplesbehindthedeploymentofselectiveattentionisto identifytheneuralresponsetopreparatorycuesthatsig- nalthespatiallocationorstimulusfeaturetobeattended priortotheappearanceoftheactualtargetdisplay.Across severalsingleeventfMRIstudies,preparatorycueshave been found to engage a primarily fronto-parietal net- work(Bressleretal.,2008;Corbettaetal.,2002;Corbetta and Shulman, 2002; Walsh et al., 2011). For example, Hopfingeretal.(2000)examinedresponsetoaninforma- tivecolor-coded cue presented atfixation that directed spatialattention totheleftor rightvisualfield.Several brainareaswereengagedbytheinstructivecue(butnotthe subsequentappearanceoftargets), suggestingtheirrole in top-downattentionalcontrol.These regionsincluded theintraparietalsulcus(IPS),frontaleyefields,andaddi- tionalregionsoftheanteriorfrontalgyrus.Theseregions appearimportanttotheendogenousorientingofselective attention,withsomeevidencethatbrieflypresentedcues thatcaptureattentionexogenouslyrecruitasimilarneu- ralnetwork(Corbettaetal.,2008;Fanetal.,2005;Peelen etal.,2004—butseealsoBuschmanandMiller,2007for differencesbetweentop-downandbottom-upsourcesof attentionalcontrol).

While mostresearchhasfocused oncuesthat direct selectiveattentiontospatiallocations,otherstudieshave investigatedcuesdirectingattentiontoparticularstimu- lusfeatures(e.g.,color,shape,ormotion).Thesestudies have identified similar fronto-parietal networks associ- atedwithorientingselectiveattention,althoughthereis evidencethatthepreciseregionsofthecontrolnetwork mayvarysomewhatbasedonthefeatureortypeofselec- tionbeingmade(CorbettaandShulman,2002;Giesbrecht etal.,2003).Thissuggeststhatwhiletheeffectsofselective

attentionaremostapparentinthecorticalareasassociated withtheattendedstimulusdimension(e.g.,modulation ofmotion-sensitiveMT/MSTwhendirectingattentionto motion),itisafronto-parietalnetworkthatisusedacross dimensionstodeployselectiveattention.

1.3. Monitoringandresolvingresponseconflictfrom competingstimuli

Theearlyattentionalfilteringreviewedabovemodu- latestheamountofprocessinganydistractinginformation may receive. Distractors may be processed to varying degrees asa function oftheirphysical similarity tothe targets,theirlocationinthevisualfield,andtheirintrin- sicsalience,tonameafew(seeMiller,1991forareview).

Thus,attimes,distractingstimulimayreceiveenoughpro- cessingtocompeteforresponseselection,triggeringthe needforresponseconflictresolution.Toassesstheinflu- ences ofsuch competingdistractors, we turnnext toa landmarkparadigminthefield—theflankercompatibility effect.Flankertasksevaluatetheimpactontargetprocess- ingofdistractorsflankingatargetasafunctionofwhether theflankeriscompatibleorincompatiblewiththeresponse associatedwiththetarget(EriksenandEriksen,1974).

For example, in the arrow flanker task, participants indicatethedirectionofacentrallypointingarrowwhile ignoring thedirectionthat nearby flanker arrowspoint (Fan et al., 2002).Behaviorally, reaction time is slowed andaccuracydecreaseswhentheflankerarrowspointin theoppositedirectionofthecentralarrow(incompatible condition)comparedtointhesamedirection(compatible condition).Thisflankereffectisbelievedtoresultfromthe processingoftheperipheral,distractingarrows,suchthat greaterregulationofthecompetinginputisrequiredwhen theflankerarrowspointinanincompatibledirectiondue inlargeparttothecompetitionbetweentheresponseasso- ciatedwiththetargetandthatwiththedistractors.Larger reactiontimeoraccuracydifferencesbetweencompatible andincompatibleconditionsaretypicallytakenasanindex ofpoorerattentionalfilteringability.Othertasksinwhich acompetingdominantresponsemustbeinhibitedarealso takentomeasurefilteringabilityandthemanagementof responseconflict,includingclassicStrooptasks(e.g.,the color-nameStroop,inwhichparticipantsnamethecolor ofinkusedtospellcolorwords,suchasresponding‘blue’

tothewordREDprintedinblueink).

UsingflankerandStrooptasks,neuralnetworksasso- ciatedwiththemanagingofresponseconflicthavebeen identified by subtracting neural activity in response to compatibletrialsfromincompatibletrials.Theseinclude theanteriorcingulatecortex(ACC),thalamus,andbilateral frontalregions,aswellasportionsofthefusiformgyrus (Caseyetal.,2000;Fanetal.,2005;MacDonaldetal.,2000).

SeveralstudiessuggestthattheACCisinvolvedprimarily inthemonitoringofresponseconflict,whichinturnsignals frontalregionstoresolvetheconflict(Botvinicketal.,2004;

Bushetal.,2000;MacDonaldetal.,2000).Interestingly, ACCrecruitmentappearsspecifictosituationsinvolving potentialresponseconflict(asoccursinflankerandStroop tasks),whereasincreasingcompetingstimulithatarenot associatedwithacompetingresponse(asachievedwith

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increasedwhitenoiseor task-irrelevantsignals)instead recruitsposteriorparietalcortex(PPC)andfrontalregions (Listonetal.,2006).Thissuggeststhatthefronto-parietal networkdescribedearliermaybeinvolvedinnarrowing thefocusofselectiveattention,whereastheACC-frontal networkisspecificallyengagedtomanageresponsecon- flict.

Insupportofthekeyroleoffrontalregionsinregulat- ingresponse conflict,greateractivityinDLFPChasbeen specificallyassociatedwithreducedinterferenceonStroop tasks(MacDonaldetal.,2000).Further,transientdisrup- tionofrightinferiorfrontaljunction(IFJ)usingtranscranial magneticstimulationimpairsbothattentionalmodulation andsubsequentmemoryperformanceinselectiveatten- tion/workingmemoryparadigms(Zantoetal.,2011).This findinghighlightsthecausalroleofregionsofthefrontal cortexinselectiveattention,aswellasthecriticalroleof selectiveattentioninsupportingworkingmemoryperfor- mance,atopictowhichwewillreturnlater.

Takentogether,thesedataindicatethatselectiveatten- tion is initially deployedusing a largely fronto-parietal network.Whenthisnetworkiseffectivelydeployed,early modulationofneuralactivityisobservedduringthefirst fewhundredmillisecondsofneuralprocessing,withthe effectsofselectiveattentionpercolatingthroughoutmul- tiplecorticalprocessing areas.Thesemodulations allow afirstfilteringoftask-relevantinformation;in addition, whencompetingsourcesofinformationleadtoresponse conflict, the ACC and associated frontal areas become recruitedtoexertgreaterattentionalcontrol.

2. Developmentofselectiveattention

Theabovesectionfocusedontheneuralsystemsmedi- ating selectiveattention in the matureadult. However, manyoftheneuralstructuresimplicatedaboveineffec- tivelydeployingselectiveattentionandresolvingresponse conflict,including regionsof theprefrontalandparietal cortex,showa protractedperiod of postnatalstructural developmentlastingintoatleastthethirddecadeoflife (Gieddetal.,1999;Gogtayetal.,2004;Sowelletal.,2001;

Tsujimoto,2008—seealsoSowelletal.,2002suggesting thecingulatecortexshowsmorerapidstructuralmatura- tionrelative tofrontalregions).Thisslowmaturationof thebasicneuralarchitectureimportanttoselectiveatten- tionsuggeststhatfunctionalchangesinselectiveattention mayalsooccurthroughoutchildhoodandadolescence.As inthediscussionofselectiveattentioninthematureadult, weconsiderthematurationofboth (1)theinfluencesof selectiveattentiononneuralprocessingand(2)theneural systemsthatdeployandcontrolselectiveattention.

Behaviorally,whilesomeaspectsofattentionareclearly present in some form in infancy (Gomes et al., 2000;

Richards,2004),theabilitytodeployandcontrolselective attentioncontinuestodevelopintoearlyadulthood(for reviews,see:Pludeetal.,1994;Ridderinkhofandvander Stelt,2000).Forexample,backgroundnoisecreatesgreater interferenceeffectsforyoungerchildrenandadolescents (Cherry,1981;Doyle,1973;PearsonandLane,1991;Plude etal.,1994),whoalsoshowlargereffectsofflankerstimuli relativetoadults(Pludeetal.,1994;Ruedaetal.,2004).

Interestingly,despitegenerallypoorerselectiveatten- tionskills,therearesomeconditionsunderwhichchildren can achieve adult-likeperformance. For example, while childrenmaybelessefficientatfilteringinformation,ifa spatial(i.e.,exogenousorienting)pre-cueisusedtofocus children’sattentionbeforeappearanceofthetarget,chil- drenperformlike adults(Akhtarand Enns,1989).Also, whilechildrengenerallyshowlargerflankereffectsthan adults,children andadultscanbemadetoshowequiv- alentflankereffectswhen attentionaldemands arehigh (Huang-Pollacketal.,2002).Thislatterfindinghasbeen interpretedintheframeworkoftheperceptualloadtheory ofattention(Lavie,2005),inwhichtheprocessingofflanker stimuliarisesfromuntappedattentionalresourcesspilling overtodistractinginformation.Asattentionaldemandsare increased(byvaryingperceptualload,forexample),most availableattentionalresourcesaredevotedtothetarget stimulus,leavinglittletonoresourcesfordistractorpro- cessing.Asaresult,thesizeoftheflankereffectdecreases.

Accordingly,Huang-Pollacketal.(2002)foundthatflanker interferencedecreasedforbothchildrenandadultsasper- ceptualloadofthecentraltaskincreased.Thiseffectwas greaterforchildrenthanadultssuchthatunderconditions ofhigherperceptualload,therewerenolongerdifferences inflankereffectsbetweenchildrenandadults.

These findings have important implications for con- ceptualizinghowselectiveattentiondevelops.Inarecent review, RidderinkhofandvanderStelt(2000)proposed thattheabilitiestoselectamongcompetingstimuliand preferentiallyprocessmorerelevantinformationareessen- tiallyavailableinveryyoungchildren,butthatthespeed and efficiency of these behaviors improve as children develop.Reportsofpoorselectiveattentionskillsinolder children maythusbeareflectionofbroad,inflexible,or poorly tuned attention control rather than an inability todifferentiallyprocessattendedandunattendedstimuli afterattentionhasbeendeployed.Theimplicationisthat selectiveattentioncanberecruited,eveninyoungchildren, if sufficient cues are provided todirect selective atten- tion.Withrespecttotheneuralbasesofselectiveattention describedabove,thissuggeststhatattentionalmodulation ofsensoryprocessingmaybepossibleforchildren–includ- ingearlymodulationofsensoryprocessing–butthatthe frontal-parietalstructuresguidingthecontrolofselective attentionandtheresolvingofresponseconflictmayshow amoreprotractedperiodofdevelopment.

Withinthisframework,itwouldbepredictedthatwhen children dodeployselectiveattention,theinfluenceson neuralprocessingwouldbesimilartothoseobservedin adults. Forexample,it mightbeexpectedthat children, likeadultsinthestudiesdescribedabove,canshowatten- tionalmodulationofneuralprocessingthatoccurswithin thefirst100msofstimuluspresentation.Toaddressthis question,werecentlydevelopeda child-friendlyversion of the Hillyard selective auditory attention paradigm describedabove(Cochetal.,2005;Sandersetal.,2006).

Inthismodifiedparadigm,childrenlistenedtooneoftwo narrativesplayedsimultaneouslyfromseparatespeakers locatedtotheleftand rightofthechild. Childrenwere cued to attend to one of the two stories, and ERPs to identicalprobestimuliembeddedintheattendedversus

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unattendedchannelwererecorded(seeFig.1,toppanel).

First,wetestedwhetheradultsshowedtypicalattention effectsinthischild-friendlyparadigm.Remarkably,even though adults were not actually listening to the probe stimuli(they weremerely embeddedinthestory),they showed typical effects of selective attention on ERP responses. Specifically, by 100ms post-stimulus onset, ERPs in response to probe stimuli embedded in the attended channel showed anincreased negativitycom- paredtoresponsestoidenticalprobesembeddedinthe unattendedchannel.Whenthistaskwasusedwithchil- drenasyoungasthreeyearsofage,probestimulielicited abroadpositivityfromabout100–300mspost-stimulus onset,ratherthanthetypicalP1-N1morphologyobserved in adults.However,as inadults, theneuralresponse in children was modulated by selective attention within 100ms,suchthat thebroad positivitywas amplifiedin responsetoprobesembeddedintheattendedascompared tounattendedchannel(seeFig.1,middlepanel).

These findings provide compelling support for the argument that, withsufficient cues, children can show impressiveattentionalmodulations.However,notallchil- dren show this robust effect of selective attention on earlyneuralprocessing.Forexample,childrenfromlower socio-economicbackgroundsshowreducedeffectsofselec- tiveattentiononearlyneuralprocessingrelativetotheir peers from higher socioeconomicbackgrounds (Stevens etal.,2009)(seeFig.1,bottomleftpanel).Similarresults were recently reported using a similar paradigm with adolescents from different socioeconomic backgrounds (D’Angiullietal.,2008).Thissuggeststhatindividualdiffer- encesduringdevelopmentexistinthecapacitytodeploy selectiveattentionand,asa result,modulateearlyneu- ralprocessing.More generally,thefindings suggestthat theabilitytocontrolthedeploymentofattentionisfragile in development, and while essentially available, atten- tional modulation may not be harnessed to the same degreebyallchildren.Atstake,then,istheissueofwhy selectiveattention isnot alwaysdeployedeffectively in children, asproperdeploymenthasacascadeofbenefi- cial consequences onneuralprocessing. It is likely that thesedifferencesreflectlessmaturecontrolstructures,or sourcesofattentionalmodulation,aswellasgreaterdif- ficulty handlingresponseconflict. Asmentioned earlier, some ofthe prefrontaland parietal areas implicated in attentionalcontrolarestructurallythelatestdeveloping neuralstructures,andtheseregionsmayshowsimilarly protractedperiodsoffunctionaldevelopment.

To ourknowledge,no studieshave examineddevel- opmentalchangesintheneuralresponsetoendogenous orientingcues.However,onefMRIstudyexamineddevel- opmentalchanges inan exogenouscueing paradigm,in which a spatialpre-cue exogenously orientedattention toaspatiallocationeithercongruent(valid)orincongru- ent(invalid)withthesubsequentappearanceofatarget (Konradet al., 2005).In comparison to adults,children age8–12 yearsshowed largerreactiontime differences betweenvalidandinvalidcuetrials,aswellaslessrecruit- mentoftherighttemporo-parietaljunction(TPJ)relative toadults.TherightTPJisbelievedtobeparticularlyimpor- tanttodisengagingattentionfromapreviouslyattended

location, suggesting that the ability to dynamically re- allocateattentionastaskdemandschangemayalsobea slowermaturingprocess.

The ability to handle response conflict may also be particularlyslowtodevelop inchildren. Severalstudies haveexamineddevelopmentalchangesintheneuralsys- temsimportantforhandlingresponseconflict,asarisesin Stroopandflankertasks.Usingvariouscolor-wordStroop tasks,age-related increases in prefrontalcortex activity havebeenreportedforincongruentrelativetoneutralor congruenttrials(Adlemanetal.,2002;Marshetal.,2006;

Schroeteretal.,2004),withyoungerchildrenalsoshow- ingadelayinprefrontaldeploymentbyapproximatelytwo secondsrelative toadults(Schroeteret al.,2004).There isalsoevidencetosuggestgreaterrecruitmentofparietal regionswithincreasingageduringStrooptasks,though thesedifferencesmaybepresentonlybetweenchildren andadolescentsandshowlittledevelopmentfromadoles- cencetoadulthood(Adlemanetal.,2002).Lessconsistent havebeenfindingsforage-relatedchangesintheACCdur- ing Stroop interference, withreports of both increased (Adlemanetal.,2002)anddecreased(Marshetal.,2006) activitywithage.Aseparatestudyexaminedneuralactiv- itytocongruentrelativetoneutralconditionsinaflanker arrow task in children and adults (Bunge et al., 2002).

Childrenage8–12yearsshowedatypicalrecruitmentof prefrontalcortex relativetoadults.Specifically,children showedgreaterleftPFCactivitywhereasadults showed greaterright PFC activity.Thesedifferences in laterality weretakentoreflectpossiblechangesinattentionalstrat- egy, with children perhaps more reliant on the verbal codingofarrowdirectionstoperformthetask.

Takentogether,studiesofthedevelopmentofselective attentionsuggestbothsimilaritiesanddifferencesbetween childrenandadults.Clearlyselectiveattentioncaninflu- enceneuralprocessing–anddosoevenatearlystagesof perceptualprocessing–inchildren.Thissuggeststhat,once deployed,comparableneuralmechanismsmediateatten- tionalmodulationsinchildrenandadults.Incontrast,the controlstructuresguidingboththedeploymentofselective attention(i.e.,fronto-parietalnetworks)and theresolv- ing of response conflictarising fromcompeting stimuli (i.e.,ACC-frontal regions)show maturationthat contin- uesthroughadolescence.Next,weconsidertheimpacts ofcompromisedselectiveattentiononfoundationalpro- cessesimportanttothreeacademicdomains.

3. Roleofselectiveattentionondomainsimportant toacademicperformance

The above discussion has highlighted the impact of selectiveattentiononmultiplestages ofneuralprocess- ingand demonstratedthat this mechanismof attention is essentiallyavailableto veryyoungchildren. By what specificmechanismsmightselectiveattentionhavewide- ranging impacts on domains considered essential to academic achievement? Below, we examine three tra- ditional domains relevant to the education literature, including language, literacy, and mathematics, positing possible neurobiological mechanisms linking selective attentiontoperformanceineachdomain.

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Fig.1. Effectsofselectiveauditoryattentiononneuralprocessinginadultsandchildren.Toppanel:Schematicrepresentationoftheexperimentalparadigm.

Childrenwereinstructedtoattendtothestorypresentedfromeithertheleftorrightspeaker.ERPswererecordedtoprobestimulisuperimposedonboth theattendedandignorednarrative.Middlepanel:Bothchildrenandadultsshowedattentionalmodulationofearly(∼100ms)sensoryERPcomponents, thoughthemorphologyoftheunderlyingevokedpotentialdiffered.Bottompanel:Earlyattentionalmodulationofevokedpotentialsisreducedchildren fromlowersocio-economicbackgrounds(leftbox)orwithspecificlanguageimpairment(rightbox).

Datatakenfrom:Sandersetal.(2006),Stevensetal.(2009,2006).

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Fig.2. Effectsoftemporalselectiveattentiononneuralprocessingofcontinuousspeechinadultsandchildren.Toppanel:Schematicrepresentationof experimentalparadigm.Attentionprobes,50msexcerptsofthenarratorsaying“ba”,werepresentedduringacousticallymatchedportionsofcontinuous speech.Theprobeswerepresentedconcurrentlywithwordonsetsandatrandomcontroltimesamongotherconditions.Bottompanel:Probespresented duringtheinitialportionsofwordselicitedalargernegativityby80msafteronsetinbothadultsand3–5-year-oldchildrenoveranteriorandmedial regions.

Datatakenfrom:AstheimerandSanders(2009,2011).

3.1. Selectiveattention&languageprocessing

From the first day of kindergarten, children receive instructionandinteractwithclassmatesviaspokenlan- guage.Thisrendersearlysuccessintheclassroomlargely contingent on entering the school system with a basic facilityinorallanguage.Here,weconsiderhowselective attentionmaybeimplicatedinlanguageprocessing.This considerationbeginswiththeobservationthatwhileaudi- toryspeechisperceivedasaseriesofdiscretewords,the actualacousticsignalisacomplex,rapidlychangingstream ofinformationwithfewobjectiveboundaries.Further,the acoustic boundariesthat do exist seldom coincidewith actualwordboundaries(seeFig.2,toppanel).Fromthis continuousstreamofauditoryinput,then,thelistenerfaces thechallengeofparsingwordboundariesandextracting meaning.Complicatingthistask,manyspeechsoundsare differentiatedbasedonlyonsubtlespectralortemporaldif- ferencesontheorderoftensof milliseconds,and many

morphemeshavelowperceptualsalienceinthecontextof thecontinuousspeechstream.

Given thecomplex natureof the speechsignal,it is reasonable to ask what role selective attention might have in facilitating language processing. Whereas this review hasupuntil now focusedonselectively attend- ing when competing visual or auditory information is presented simultaneously, temporal selective attention involvesidentifyingandselectingparticularpointsintime for furtherprocessing. Several recent ERP studies doc- umentthat humans can allocateattentionto particular pointsintimeandthattheeffectsonneuralprocessingare markedlysimilartothoseobservedwithselectionbased onotherstimulusfeatures,withattentionalenhancement evidencedasanincreasedneuralresponsewithin100ms ofprocessing(Griffinetal.,2002;Langeetal.,2003).

The link between temporal selective attention and speechprocessinghasrecentlybeenexploredinanelegant seriesofERPstudies.Inonestudy,participantslistenedto

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sentences,andERPswererecordedduringword-initialas comparedtoword-medialsyllableswithinthesentences, withthesyllablesequatedforloudness,length,andphone- miccontent(Sanders andNeville,2003).Toensurethat participantswereattendingtothesentences,theywere occasionallyqueriedastowhethertheprecedingsentence containedaparticularword.AdultsshowedalargerN1to word-initialascomparedtoword-medialsyllables, sug- gesting temporal selectiveattention has beenallocated totheinitialportionsof thewords.Similarresultshave beenreportedforword-initialandword-medialsyllables embeddedin continuous strings of novel psuedowords amongparticipantswhoareabletolearnthenovelwords inaseparatetaskpriortoERPtesting(Sandersetal.,2002).

SimilarresultsarealsoreportedwhenERPsarerecorded toidentical probe stimuli superimposed oncontinuous narratives,suchthatprobespresentedatorimmediately followingwordonsetselicitanenhancedN1comparedto probesembeddedinotherlocationsmatchedforacous- ticproperties (Astheimer and Sanders,2009—seeFig.2, bottomleftpanel).Thisearlyenhancementsuggeststhat when processing speech, listenerslearn to identifyand predictwordinitialsegmentsandselectivelydirectatten- tiontothosepointsintimetoaidinprocessing.Although not explored,similar processes mayenable listeners to directattentiontootherpointsintime withhighinfor- mationvalue,e.g.,thepointsin timewhere inflectional morphemesmightappear.Thus,deployingtemporalselec- tiveattentionstrategicallymayallowthelistenertoselect andamplifyprocessingoftheportionsofthespeechsignal mostcriticalforcomprehension.

Iftemporalselectiveattentionwereimportanttolan- guage learning, we would expect to find that young children areabletodeploy this mechanismduring lan- guageacquisition.Inarecentstudy,AstheimerandSanders (2011)examinedwhetherchildren age 3–5years show evidence of temporal selective attention during speech processing,similartothatobservedinadultsinthestudies describedabove.ERPswerecomparedtolinguisticprobe stimuliembeddedinanongoingchildren’snarrative,either concurrent withword onsets or at other control times matchedfor basicacoustic properties.Results indicated thatchildren, like adults,deployed temporallyselective attentiontomodulateearlysensoryprocessingoflinguistic probespresentedcoincidentwithwordonsetsrelativeto controltimes(seeFig.2,bottomrightpanel).Thesefindings indicatethatearlyenhancementofword-initialprocessing isaneuralmechanismavailabletoyoungchildrenandthus acandidatecriticalmechanismforparsingandprocessing thecontinuous speech stream. To theextent that chil- drenhavedifficultyselectivelyattending–orusingcues toidentifywhichregionsshouldbeattended–theymay facedifficultiesparsingandprocessingthespeechstream.

Indeed,other researchindicatesthatselective attention maybeimportanttoshapingauditorysoundprocessing duringdevelopment,includingaspectsofsoundprocess- ing important to language development (Sussman and Steinschneider,2009).

In support of the role of selective attention in lan- guageprocessing,severalstudieshaveexaminedwhether childrenwithSpecificLanguageImpairment(SLI)exhibit

deficitsinselectiveattention.SLIisadevelopmentaldis- order marked by delayed and atypical language ability thatcannotbeexplainedbyachild’sage,generalintelli- gence,oreducationalopportunity(Leonard,1998).Several behavioral studies reportdeficitsin aspectsof selective attention among children with SLI (Noterdaeme et al., 2000;Spauldingetal.,2008;Ziegleretal.,2005).However, asbehavioraltasksrepresentthesummedactivityofmul- tiplestagesofprocessing,itisunclearwhetherthelocus oftheattentiondeficitarisesinattentionalmodulationof earlysensoryprocessing.

Toexaminewhethertheearlyneuraleffectsofselec- tiveattentionarecompromisedinchildrenwithSLI, we recentlycomparedagroupofchildrenwithSLItoacontrol groupmatchedforage,gender,nonverbalIQ,andsocioeco- nomicstatususingthechild-friendlyERPselectiveauditory attentiontaskdescribedabove(Stevensetal.,2006).Inthis task,childrenattendedselectivelytooneoftwonarratives presentedfromseparatespeakers,andERPswererecorded toprobestimulisuperimposedontheattendedandunat- tendedstories.AlthoughthechildrenwithSLIwerewilling andabletoperformtheselectiveattentiontask(asindi- catedbyperformanceoncomprehensionquestionsabout theattendedstory),theydidnotshowearlyeffectsofatten- tiononneuralprocessing(seeFig.1,bottomrightpanel).

Furthermore,theseperformancedeficitswereassociated specificallywithareducedabilitytoenhancetheneural responsetotheattendedstimuli(i.e.,aproblemwithsig- nalenhancement),ratherthandifficultysuppressingthe unattendedresponse. Itisanongoing questionwhether childrenwithSLIshowthesamedeficitsintemporalselec- tiveattentionduringonlinelanguageprocessing.However, the strikingdeficits in selectiveauditory attentionsug- gestthismaybeacriticallinkbetweenselectiveattention andlanguageprocessingdifficultiesinatleastsomechil- drenwithSLI.Itremainsforfutureinvestigationstofurther assessthestrengthofsuchalink.

3.2. Selectiveattention&literacy

Theemergenceofwrittensymbolscriptsduringhuman historyhadtheadvantageoftransformingtheephemeral speechsignalintoadurablevisualform.Thisformiswidely usedinacademiccontextsasthemediumforcommuni- cating information. However,printed textbroughtwith it newdemands onvisuo-spatial attention. Unlike lan- guageprocessing,whereauditoryselectiveattentionmust bedirectedtocriticalpointsintime,readingrequiresthat visualselectiveattentionbefocusedspatially.Withoutthis ability, the printed page would bea sea of visualclut- ter.Forexample,allscriptsrequirethatselectiveattention moveseriallyinsomeorderedfashion(e.g.,fromleftto rightacrossapageand/orfromtoptobottom),andthere is evidencethat learning toread biasesboth thegradi- entofvisualattentionandscanpatternstoalignwiththe demandsofthescriptbeinglearned(Ferrettietal.,2008).

Foralphabeticscripts,attentionmustbefurtherfocused, particularlyduringtheearlylearningstages,onlettersand letterclustersinordertoacquirethemappingsbetween graphemesandspeechsounds,i.e.,knowledgeofthealpha- betic principle.Below,evidence fortherole ofselective

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attention onliteracy developmentis reviewed, withan emphasisontheimpactofattentionalfocusduringalpha- beticscriptlearningonthedevelopmentofneuralsystems importantforfastandaccuratereading.

Asa relativelyrecentculturalinvention,reading isa formofperceptualexpertisethatisunlikelytobeinnately specifiedinthebrain(Cohenand Dehaene,2004).Thus, overthecourseofliteracyacquisition,thebrainmustadapt processingsystemstosupportthefast,accurateidentifi- cationofwrittensymbolstrings.Althoughneuroimaging studies have identified a setof left-hemisphere regions importanttoskilledreading (e.g.,forareview seePugh etal.,2000),wefocushereona regionofleftextrastri- atecortex,oftenreferredtoasthevisualwordformarea (VWFA)(Cohenetal.,2000;McCandlissetal.,2003b).This areaisbelievedtorespondpreferentiallyduringtasksthat involvetheautomaticconversionofavisualformtoalin- guisticform,mosttypicallywithprintedwordsbutalso observedinothertasksincludingnamingvisualpresenta- tionsofobjectsandcolors(e.g.,seePriceandDevlin,2003;

Wrightetal.,2008).IntracranialrecordingsandERPstud- ieslocalizetherapidtimecourseofneuralspecializationin theVWFA,withtheN170largerinamplitudeoverleftpos- teriorregionsinresponsetowordsrelativetootherclasses ofvisualstimuliandlikelyarisingfromtheactivityofneu- ronsintheVWFA(e.g.,Allisonetal.,1994;Bentinetal., 1999;McCandlissetal.,2003b).

Left-lateralization of the N170 is observed not only during explicit reading, but also during implicit pro- cessing tasks that do not require reading, such as one-backrepetitiondetectiontasks.Thisobservationhas ledtothephonologicalmappinghypothesis(Maurerand McCandliss,2007),whichproposesthatleft-lateralization of the N170to wordsreflects automatic links between orthography and left-lateralized phonological systems.

Indeed,thereisevidencefordevelopmentalshiftsinthe lateralizationoftheN170towordsduringreadingacqui- sition. During the initial stages of reading acquisition, children showabilateraloreven right-lateralizedN170 enhancement to words relative to false-font strings in one-backtasks(Maureret al.,2005,2007).Initialright- lateralizationoftheN170ishypothesizedtoreflectavisual expertise effect, similarto that observed for face stim- uli or noveltrained objects (Rossion et al., 2002), that doesnotbecomeleft-lateralizeduntilwordsareautomat- icallymappedtoleft-lateralizedphonologicalsystems.In this context,itisreasonabletoassumethattheseauto- maticmappingsarefacilitatedwhenattentionisdirected tosmallerunitsoforthographicanalysisduringearlyliter- acyacquisition.

Insupportofthishypothesis,arecentstudyexamined whethertheN170lateralizationinresponsetoanovelsym- bolscriptwasinfluencedbyattentionalfocusduringthe learningphase.Inthisstudy,agroupofadultsreceiveda brief,20-mintrainingsessionwithanovelsymbolscriptin whichportionsofholisticwordsymbolsconsistentlycor- respondedtoparticularphonemes(seeFig.3).Attentional focusduringtrainingwasmanipulatedbyinstructinghalf ofparticipantstofocusonthesymbolasaholisticunitand theotherhalftofocusonmappingportionsofthesym- boltoindividualphonemes(i.e.,explicitattentiontothe

alphabeticprinciple),alsoshowninFig.3.Followingthe training,ERPswererecordedwhileparticipantscompleted anexplicitphonology-basedtaskinwhichtheyindicated whetheravisuallypresentedsymbolmatchedanaudito- rilypresentedword(bothtrainedanduntrainedsymbols were used, with similar results across stimulus types).

ResultsindicatedthatN170responsestothevisualsymbols varied as a function of attentional focus during train- ing:adultsinstructedtofocusonthesymbolsholistically showedabilateralN170responsetothesymbolswhereas adultstrainedtomapthesymbolstophonemesshowed a left-lateralized N170response (Yoncheva et al.,2010).

Interestingly,neithergroupshowedaleft-lateralizedN170 tothenewlylearnedsymbolsduringanimplicitprocess- ingone-backtask(Maureretal.,2010).Thedifferentiation acrosstasks ishypothesizedtobea consequenceofthe brief20-mintraining,withleft-lateralizationnotyetappar- entintheimplicitprocessingone-backtask.Longer-term training datawill helpfurtherevaluatethis hypothesis.

However,themoststrikingfindingacrossthesestudieswas thatleft-lateralizationoftheN170towordsonlyoccurred forthegroupofparticipantswhoattendedtotheembed- dedalphabeticprinciple withinthenovelsymbols. This suggeststhatattentionalfocus,andtheabilitytoidentify and process smaller orthographic-to-phonological units of words,mayfacilitate thedevelopmentof rapid,left- lateralizedneuralresponsesimportanttofluentreading.

ArecentfMRIstudyfurthersupportstherelationship betweenselectiveattentionanddevelopmentoftheVWFA (Vogeletal.,2011).Thisstudyusedrestingstatefunctional connectivityMRItoexaminethefunctional relationship betweentheVWFAandotherbrainregions.Thelogicof the analysiswas that brain areas that show correlated slowfluctuationsofBOLDactivityduringrestlikelyshare a history of use-dependent co-activation. Although the VWFAisconsideredakeypartofthereadingnetwork,its slowfluctuationsofBOLDactivityshowedlittlecorrela- tionwithotherregionsofthereadingnetwork(leftSMG, AG,and ITG). Instead,large correlations wereobserved betweenactivityintheVWFAandfronto-parietalregions associatedwithorientingselectiveattention(bilaterialIPS, MT+,andfrontaleyefields).Further,thestrengthofthese associationsincreasedwithageandreading experience, particularlyintheIPS.Thesefindingssuggestthatselective attentionmaybecriticaltodevelopmentoftheVWFA,per- hapsthroughtheroleoffronto-parietalattentionnetworks inshiftingthefocusofselectiveattentiontodifferentunit sizes(words,letters,orbigrams/trigrams)duringliteracy acquisition.

Thesedataaresuggestivethatselectiveattentionmay beimportantforestablishingtheneuralcircuitsimportant forefficientreading,andinparticularthedevelopmentof responsesintheVWFAtowordstrings.Arelatedquestion, then,iswhetherthere isevidencethatindividuals with SpecificReadingDisorder(dyslexia)showatypicalselec- tiveattention.Indeed,multiplestudieshavedocumented deficitsinaspectsofvisualselectiveattentionamongindi- vidualswithreading disorder, usingboth linguisticand nonlinguisticstimuli(Atkinson,1991;BosseandValdois, 2009;Sperlingetal.,2005;Spinellietal.,2002—butsee alsoShovmanandAhissar,2006).Further,therelationship

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Fig.3. EffectsofattentionalfocusduringanovelwordlearningtaskonlateralizationoftheN170.Toppanel:Participantsreceiveda20-mintrainingona novelsymbolscript.Thescriptcontainedahiddenalphabet,inwhichportionsofthesymbolcorrespondedtoindividualspeechsounds(seerightside,bold forillustrationonly).Duringthetraining,participantswereeitherinstructedtoattendtothesymbolholistically(rightside)ortothegrapheme-phoneme mapping(rightside).Bottompanel:ERPsrecordedtobothtrainedandtransfercharactersduringatestofwordlearningshowedleft-lateralizedN170 responsesinthegrapheme-phonemegrouponly,whereasthewhole-groupgroupshowedabilateralresponse.

Datatakenfrom:Yonchevaetal.(2010).

betweenmeasuresofattentionandliteracyskillmaybe morepronouncedduringtheearlyyearsofliteracyacquisi- tion(BosseandValdois,2009),andseveralrecentreviews haveproposedthatselectiveattentioniscriticaltoearly literacyacquisition(Valdoisetal.,2004;Vidyasagar,2005;

VidyasagarandPammer,2009).Further,thereisevidence tosuggestthatwhilechildrenwithdyslexiaeasilyfocus attentiononlettersintheword-initialposition,theyhave particulardifficultyfocusingattentiononlettersinother positionswithintheword(McCandlissetal.,2003a).As well,usingtheERPselectiveauditoryattentionparadigm describedearlier,inwhichchildren attendselectivelyto

oneoftwosimultaneouslypresentednarratives,wehave recentlyshownthatfive-year-oldchildrenwithpoorpre- literacyskillsshowreducedeffectsofselectiveattention onearlyneuralprocessing(Stevensetal.,2011).

These findings indicatedeficitsin selectiveattention among individualswithreading disorder,buta remain- ingquestioniswhetherorhowtheseattentiondeficitsare relatedtothedevelopmentoftheneuralcircuitsimportant to efficient reading. Several studies document under- activationofleftposteriorregionsofthereadingnetworkin adultsandchildrenwithdyslexia,includingtheVWFA(for reviews,seeMcCandlissandNoble,2003;Pughetal.,2000).

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Interestingly,whiletrainingstudieshavedemonstratedthe abilitytoimprovedecodingskillamongindividualswith dyslexia,includingincreasedactivityintheVWFAevident withfMRI(Shaywitzetal.,2004),therapidtimecourseof neuralactivationinsomeneuralareas,evidentwithmag- netoencephalographicimaging,canremaindelayedeven following intervention (Simos etal., 2002).Thisfinding parallelsbehavioralresultsshowingimproved(non-timed) decodingskills,butrelativeintractabilityofreadingfluency (i.e.,readingthatisbothfastandaccurate)(Shaywitzetal., 2004).Itispossiblethatattentionalcontrolmaybecritical todrivingtheautomatizationindexedbyleft-lateralization oftheN170,andinturnfastandaccuratereading.Although onlysuggestiveatthispoint,onestudydemonstratedthat prior attention training translated to increasedbenefits ofasubsequentremedialwritinginterventionforadoles- cents withdyslexia (Chenault etal., 2006).However,to date nostudieshaveexaminedhow prior (orconcomi- tant)attentiontrainingmayimpacttheefficacyofreading interventions,includingtherecruitmentandtimecourseof activationof neuralsystemsimportantfor reading.This willrepresentanimportantdirectionforfutureresearch and contributetoourunderstandingoftherelationship betweenselectiveattentionandthedevelopmentofneural circuitssupportingreading.

3.3. Selectiveattention&mathematics

Mathematicsisabroaddomain,includingseveraldis- tinctskills.Here,weconsidertheroleofselectiveattention on a particular class of mathematics tasks referred to aswordproblems.Weacknoweldgehoweverthatother aspectsofmathskillmaybeimpactedbyselectiveatten- tion(e.g.,seePiazzaandDehaene,2004).Inwordproblems, anindividualmustholdontoandretainrelevantinfor- mationpresentedlinguisticallyformakingacomputation while not being distracted by extraneous information irrelevanttothecomputation.Furthermore,therelevant informationmustthenbeeffectivelymanipulatedtoarrive at a computationalsolution. Intuitively, word problems placehighdemands onworkingmemory,whichinturn is influenced by selectiveattention.Indeed, it hasbeen proposed that working memory skills are particularly importantduringwordproblemsinordertoformacon- ceptualproblemmodel,asopposedtoapproachingword problemswithrote,direct-translationstrategies(Hegarty etal.,1995;Jonassen,2003;LeBlancandWeber-Russell, 1996).Importantly,this beginsto highlighttheinterac- tion between workingmemory and selective attention.

Althoughthesehavetraditionallybeentreatedasdistinct mentalcapacities,asdetailedbelowthereisconsiderable interactions betweenthese processes, both in terms of functionalsignificanceandneuralbases.

Behavioralstudieshaveassociatedpoorperformanceon mathematicswordproblemswithpoorerworkingmem- oryperformance(AnderssonandLyxell,2007;Fuchsetal., 2006;SwansonandBeebe-Frankenberger,2004;Swanson and Jerman, 2006). Importantly, the working memory deficitsextendbeyondnumericalcontenttovisuo-spatial andverbalworkingmemorytasks(WilsonandSwanson, 2001),andthezero-ordercorrelationsbetweenworking

memoryandwordproblemsarehigherthancorrelations betweenworkingmemoryand basicarithmeticorcom- putation skills (Fuchs et al., 2006). Similarly, errors in mathematicalcomputationareoftenattributedtodeficits in workingmemory, rather thanprocedural knowledge (Ayres,2001),andsomewhatironically,mathematicsanx- ietyisassociatedwithaconcomitantreductioninworking memorycapacityandmathematicsperformance(Ashcraft andKrause,2007).However,studiesthatincludemultiple predictorsofwordproblemperformancesimultaneously in a model often report reduced or eliminated effects ofworkingmemoryonwordproblemperformance(e.g., Fuchsetal.,2006;KailandHall,1999).Whenassociations withworkingmemoryarereducedoreliminatedinstudy results,thismayreflecttheselectionofparticularworking memorymeasures(seeFuchsetal.,2006foradiscussion) ormaybetheresultofsharedvarianceacrosspredictors enteredinthemodel(e.g.,betweenworkingmemoryand verbalprocesses,inattention,andprocessingspeed,see,for example,Fuchsetal.,2006;KailandHall,1999).

Interestingly,recentdatasuggestthatworkingmem- orydeficitsamongindividualswithmathematicsdifficulty are related toimpairments inignoring irrelevant or no longer relevant information during memory tasks. This is seen in a high number of intrusion errors of pre- viously presented, but currently task-irrelevant content duringworkingmemorytasks(Passolunghietal.,1999;

Passolunghi and Siegel,2001).Thispattern of intrusion errorsof to-be-ignoredinformationsuggestsa difficulty suppressingitemsthatareeitherirrelevantorthathave beenprocessedbutarenowirrelevanttothetaskathand.

Although few studies have directly assessed aspects of attention in relation to mathematics performance, one recentstudyreportedthatthedegreeofinterferenceina flankerarrowtaskisassociatedwithpoorermathematics performanceinasampleof12yearolds(ChecaandRueda, 2011).

Thesefindings suggest a link betweenattentionand mathematicsword problems skills that is mediated by the effect of selective attention on working memory.

This hypothesis is yet to be tested directly. However, severalneuroimaging studiessupport therole of selec- tive attention, and distractor suppression in particular, ineffectiveworkingmemoryperformance.For example, ina recentstudyby Vogelet al.(2005),workingmem- orycapacitywasrelatedtoaneurophysiologicalmeasure ofattentionalselection.Individualswithhigherworking memorycapacitywerebetterabletosuppressirrelevant itemsandencodeonlytherelevantitemspresentedina multi-stimulusdisplay.Incontrast,individualswithpoorer workingmemorycapacityencodedmoreinformationfrom thedisplay,includingirrelevantitems.Thissuggeststhat selectiveattention,anddistractorsuppressioninparticu- lar,isimportantforregulatingaccesstoworkingmemory and optimizing working memory capacity (Cowan and Morey,2006).

Additionalsupportfortherelationshipbetweenselec- tiveattentionandworkingmemorywasfoundinarecent studybyZantoandGazzaley(2009).Participantsinthis studyobservedaseriesoffourmulti-dotimages,alternat- ingbetweenstationarysingle-coloreddotsandcoherently

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movinggrey dots.In differentblocks, participantswere instructed to attend either to the moving dot images, thestationarycoloreddotimages,orboth.Afteradelay period,aprobeimageappearedandparticipantsindicated whetherithadappearedinthefour-itemsequence.ERPs ofidenticaldotimagesintheattendedascomparedtothe unattendedpositionwerecompared,separatelyfortrials consideredtohavehighascomparedtolowperformance basedona mediansplit ofreactiontime. Evidence was foundforlargereffectsofattentiononneuralprocessing inthefirstfewhundredmillisecondsafterstimulusonset forhighascomparedtolowperformancetrials.Further, thedifferencesacrosstrialtypeswerespecifictobetter suppressionof irrelevant stimulusdisplays (asopposed togreatersignalenhancementoftheto-be-attendeddis- plays),furthersuggestingthatdistractorsuppressionisa keymechanismassociatedwithimprovedworkingmem- oryperformance.Takentogether,thesedatasuggestthat effectiveallocationofselectiveattentionduringencoding, andinparticularthesuppressionofirrelevantinformation, helpsoptimizeworkingmemoryperformance.

Thelinksbetweenselectiveattentionandmathemat- icsperformanceareclearlymorespeculativethanthose linking selective attention with language and literacy.

However,theabovedatasuggestinterestinglinksbetween selectiveattentionandmathematicsperformance,medi- ated by the effect of selective attention on working memory.Futurestudiescantestthishypothesisdirectly.

Aswell,cleverlydesignedneuroimagingstudiesmaybe abletoassessthedistributionofattentionacrossinforma- tioninwordproblemsusingparadigmsparalleltothose describedearlier.

4. Malleabilityofselectiveattention:Insightsfrom adultpopulations

Giventhevulnerabilityofselectiveattentionskillsand their proposed relevance for processing across several academicdomains,itisreasonabletoaskwhetherselec- tiveattention itself can be trained. If so,such training mightbeexpectedtoactasaforce-multiplier,leadingto improvementsacross a range of domains. Twolines of researchdemonstratethecapacityofselectiveattentionto beenhanced,thefirstoneconcernsactiongameplayand thesecondmind-bodytraining.

Acrossseveralstudies,action gameplayisrelated to enhancementsinvarious aspectsof attention,including selective attention over space, time, or objects (for a review, see Hubert-Wallander et al., 2010). Recently, Mishraetal.(2011)madeuseofthesteady-statevisual evoked potentials technique to understand the neural bases of the attentional enhancement noted in action gamers(seeFig.4).Theyfoundthatactiongamersmore efficiently suppress unattended, potentially distracting information. Participants viewed four different streams ofrapidlyflashedalphanumericcharacters. Eachstream flashedatadistincttemporalfrequencyallowingretrieval ofthebrainsignalsevokedbyeachstreamindependently at all times. Thus, not only could the brain activation evoked by the attended stream be retrieved, but also thoseevokedbyeachoftheunattendedandpotentially

distractingstreams.Actiongamerssuppressedirrelevant streams to a greater extent than non-gamers, and the extent of the suppression predicted the speed of their response. This finding suggests that action video-game play sharpensselectiveattentionbyallowingplayersto betterfocusonthetaskathandbyignoringothersources ofpotentiallydistractinginformation.

A second line of research has examined changes in attentionabilitiesamongexperiencedmeditators.While there is some evidence that different styles of med- itation are associated with unique changes at both a behavioral and neural level (e.g., see Jha et al., 2007;

Lutz et al., 2008), across several studies of different meditationstyles,experiencedmeditatorsshowenhance- mentsinseveralaspectsofselectiveattention(Jhaetal., 2007; Kubose,1976;Linden,1973; Slagteretal., 2007), similar to that reported in action gamers. It has been proposedthatmeditationimprovesattentioninapractice- related manner, with the act of meditation engaging neural systems supporting selective attention. In sup- port of this hypothesis, several neuroimaging studies documentengagementof fronto-parietalregions associ- atedwithdeployingselectiveattentionduringmeditation (Brefczynski-Lewiset al.,2007; Cahnand Polich, 2006), withsimilarregionsrecruitedacrossavarietyofmedita- tivestyles(CahnandPolich,2006).However,asarelatively youngfield,moststudieshavenotdifferentiatedspecific subregionsoffrontalorparietalcortex.

Thestudyofattentionalchangesinactionvideogamers andexperiencedmeditatorsprovidebotha“proofofcon- cept”forthemalleabilityofattentionandalsounderscore severalimportantmethodologicalpoints.First,bothlines ofresearchprovidecausalevidencefortheroleofexperi- enceinshapingattentionthroughtheinclusionoftraining studieswithrandomassignmenttoconditions. Inthese studies, previously inexperienced gamers or meditators show improvements following training in their respec- tivedomainrelative tocomparisoncontrol groups(e.g., seeFengetal.,2007;GreenandBavelier,2003,2006a,b, 2007; Jha et al., 2010; Spenceet al.,2009; Tang et al., 2007).However,withinthestudyofactionvideogamers, theenhancementsinattentionappearmostmarkedwhen theexperienceiswithactionvideogames(e.g.,Medalof Honor,Callof Duty,Unreal Tournament).Similareffects arenotobservedwithothertypesof gamestested(e.g., Tetris,RestaurantEmpire,theSims).Thus,atpresentthis particularlineofresearchhaslimitedutilityethicallyasan attentiontrainingprogramforchildren.

Second,thesestudiesprovideinsightsintothenatureof neuralchangesthattakeplaceinattentionalsystems.For example,itshouldbenotedthatnotallaspectsofattention seemequallyenhancedbyactiongameplay.Whiletop- downattentionalmechanismsarealteredforthebetter, there islittleevidence forchanges inbottom-upmech- anisms,atleastasmeasuredbytheautomaticorienting anexogenouscueproduces(Casteletal.,2005;Dyeetal., 2009a;Hubert-Wallanderetal.,2011).

Third,whenchangesareobserved,thesechangesare not always linear in nature. For example, Brefczynski- Lewis et al. (2007) examined the effects of auditory distractorsoundsonneuralprocessingwhileparticipants

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Fig.4. Plasticityofdistractorsuppressionmechanismsinactionvideogameplayers(VGPs)relativetononactionvideogameplayers(NVGPs).Participants vieweddifferentstreamsofrapidlyflashedalphanumericcharacters.Eachstreamflashedatadistincttemporalfrequency,andsteadystatevisualevoked potentials(SSVEPs)wererecordedateachfrequency.Actiongamerssuppressedirrelevantstreamstoagreaterextentthannon-gamersandtheextentof thesuppressionpredictedthespeedoftheirresponse.

Datatakenfrom:Mishraetal.(2011).

meditatedonavisualstimulus.Comparedtoinexperienced meditators, participants with some meditation experi- enceshowedgreateractivityinfronto-parietalregionsin responsetodistractingauditorysounds.Yet,expertmed- itators showed a striking down-regulationof activation

intheseregionsunderthesamecondition.Thisinverted U-shapepatternis consistentwiththeview thatmedi- tationexperienceinitiallyenablesgreaterrecruitmentof attentionalcontrolsystemsastheattentionaltaskbecomes more effortful; but as expertise develops with extra

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training,meditationexpertisemayallowonetoachieve afocusedstateofattentionalcontrolmoreautomatically, thereforecallinguponfewerattentionalresources(seealso Petersenetal.,1998for reductionsand changesinneu- ral recruitment asautomaticity sets in).The possibility of increasing attentional allocation and its automatic- ityis mirroredin arecent reportdocumenting reduced recruitmentoffronto-parietalnetworksinactiongamers ascomparedtonon-gamersasattentionaldemandswere increased(Bavelieretal.,2011).Furtherstudiesareneeded tolinkchangesinthefronto-parietalnetworkwithbehav- ioralenhancement,howeverthisworkalreadyhighlights theimportanceofconsideringnon-linearchangesinthe dynamicsof selective attentionwith training, including changesinprocessing resources,primary taskdemands, andautomaticitywithtraining(seeLustigetal.,2009for similarconsiderationsaboutworkingmemorytraining).

Finally,thislineofresearchhashighlightedchallenges withsomemeasures of attentioncurrently used in the developmentalliterature.Inparticular,thisworkdemon- stratesthatinterpretationofflankercompatibilityeffects suchasthosemeasuredintheANTparadigm(Fanetal., 2002;Ruedaetal.,2004)shouldnotbeconsideredasan absolutemeasureoftheabilitytodeployefficientfiltering.

Inseveralstudies,actionvideogameplayerswerefound tohavelargerfilteringscoresthannonactiongameplayers (Dyeetal.,2009b;GreenandBavelier,2003,2006a).While thiswouldtypicallybeinterpretedasalackofattentional controlin thedevelopmentalliterature,gamersconcur- rentlyshowreactiontimesonincompatibletrialsthatare fasterthanthoseofnon-gamersoncompatibletrials.In short,theyexcelatthetargettaskwhileexhibitinggreater spill-overofunusedresourcestodistractors.Thissuggests thatasubtractionscorecanbeinfluencedbyoverallreac- tiontimedifferencesacrossgroupsand/orbydifferences acrossgroupsinthedifficultyofthecentraltask,i.e.,differ- encesinperceptualloadoftheprimarytask(seeDyeetal., 2009bforadiscussionofthisissue),andshouldthusbe interpretedcautiously.Thisisofspecialconcernindevel- opmentalstudiesinwhichtypicallygroupsofdifferentages oretiologyshowmajordifferencesalsoinbasicreaction times.

Takentogether,theliteratureonattentionalenhance- ments in adults provides a proof of concept for the malleability of selective attention, and in particular improvementsinattentionalallocationanddistractorsup- pression. Althoughactivities suchas action video-game playandintensemeditationmayseemquitedisparateat firstsight,theymayevokesharedmechanismsbyenabling greaterautomatizationandflexibilityofattentionalcon- trol.The keycomponent thata training regimenwould needtoincludetoachievesuchchangesisanextremely activeareaofresearch.Next,weconsidertheimplications ofthesebenefitsfortrainingprogramsinaneducational context.

5. Malleabilityofselectiveattention:Implications forchildhoodeducation

Giventheevidencethatsomeaspectsofattentioncan betrained,itisnaturaltoaskwhethersuchbenefitscan

be observed following more academic-focused training withchildren,asthismayhaveimportantimplicationsfor educationalpractice.Interestingly,wefirstobservedsuch attentional enhancements in an education setting with childreninresponsetoproposeddomain-specificinterven- tionstargetingauditoryprocessingand/orliteracyskills.

Inonestudy(Stevensetal.,2008),weexaminedwhether sixweeksofhigh-intensitytraining(100min/day)witha computerizedinterventionprogramdesignedtoimprove languageskillswouldinfluencetheneuralmechanismof selectiveauditoryattentionwehadpreviouslyshownto bedeficientinchildrenwithSLI.Followingtraining,both childrenwithSLIandtypicallydevelopingchildrenreceiv- ingthetrainingshowedlargereffectsofselectiveattention onneuralprocessing.Similarchangeswerenotobservedin ano-treatmentcontrolgroup.Inasecondstudy(Stevens etal.,2011),weexaminedfive-year-oldchildreneitheron- trackinpreliteracyskillsorat-riskforreadingdifficulties both beforeandafterthefirstsemesterofkindergarten.

Theat-riskgroupalsoreceivedsupplementalinstruction with the Early Reading Intervention (ERI, an evidence- basedreadingintervention,Simmonsetal.,2007,2003)in additiontotheregularkindergartencurriculum.Children receiving the supplemental reading instruction showed increasesintheeffectsofselectiveattentiononneuralpro- cessingfromthebeginning toend of thefirstsemester of kindergarten.In both ofthestudiesdescribed above, increasesintheeffectsofselectiveattentiononsensorineu- ralprocessingwereaccompaniedbybehavioralchangesin otherdomainsthatweretargetedspecificallybythetrain- ing programs, includinglanguage and preliteracy skills, respectively.Thesefindingsareinlinewithrecentpropos- alssuggestingthatsomeinterventionsdesignedtoimprove languageskillsmightalsotargetortrainselectiveatten- tion(Gillam,1999;Gillametal.,2001a,b;HariandRenvall, 2001;SundbergandLacerda,2003).

Thesedatasuggestthatmodificationsinbehaviorcan arise alongsidechangesin theearlyneuralmechanisms ofattention.However,thesestudiesdidnottargetatten- tiondirectly.Inourmostrecentresearch,wehavebeen investigatingthepossibilitythatattentionitselfmightbe trainable,andthatthistrainingcanimpactprocessingina numberofacademicdomains.Indeed,inhisseminalwork, PrinciplesofPsychology,WilliamJamesraisedtheideaof attentiontrainingforchildren,proposingthatthiswould be“theeducationparexcellence”(James,1890,italicsorig- inal).WhileJameswentontosaythatsuchaneducationis difficulttodefineandbringabout,thedesignofsuchpro- gramshasbecomepreciselythefocusofrecentresearchin cognitivescienceandcognitiveneuroscience.

For example, in a pre/post training study, Rueda etal.(2005)developedacomputerizedattentiontraining programforyoungchildreninvolvingfivesessionsadmin- istered over a two tothree weekperiod. While not an educationalsettingperse,thisstudyusedcomputerized activitiesthat couldeasilybeincorporatedintoanedu- cationalsetting.Childrenintheinterventionengagedin interactive, adaptive computer games that trained sev- eralaspectsofattention.Childrenrandomlyassignedto thecontrolgroupalsovisitedthelaboratorybutinstead watchedvideosthatpausedintermittently,andwhichthey

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