ContentslistsavailableatScienceDirect
Developmental
Cognitive
Neuroscience
jo u r n al ho me p ag e :htt p : / / w w w . e l s e v i e r . c o m / l o c a t e / d c n
How
age
of
bilingual
exposure
can
change
the
neural
systems
for
language
in
the
developing
brain:
A
functional
near
infrared
spectroscopy
investigation
of
syntactic
processing
in
monolingual
and
bilingual
children
K.K.
Jasinska
a,b,
L.A.
Petitto
a,b,∗aUniversityofToronto,Canada bGallaudetUniversity,USA
a
r
t
i
c
l
e
i
n
f
o
Articlehistory:Received15October2012
Receivedinrevisedform23June2013 Accepted30June2013 Keywords: Bilingualism Languagedevelopment Syntax Sentenceprocessing fNIRSneuroimaging NeuralSignatureHypothesis
a
b
s
t
r
a
c
t
Isthedevelopingbilingualbrainfundamentallysimilartothemonolingualbrain(e.g., neu-ralresourcessupportinglanguageandcognition)?Or,doesearly-lifebilinguallanguage experiencechangethebrain?Ifso,howdoesageoffirstbilingualexposureimpactneural activationforlanguage?
Wecomparedhowtypically-developingbilingualandmonolingualchildren(ages7–10) andadultsrecruitbrainareasduringsentenceprocessingusingfunctionalNearInfrared Spectroscopy(fNIRS)brainimaging.Bilingualparticipantsincludedearly-exposed (bilin-gualexposurefrombirth)andlater-exposedindividuals(bilingualexposurebetweenages 4–6).
Bothbilingualchildrenandadultsshowedgreaterneuralactivationinleft-hemisphere classiclanguage areas,andadditionally,right-hemispherehomologues(Right Superior Temporal Gyrus, Right Inferior Frontal Gyrus). However, important differences were observedbetweenearly-exposedandlater-exposedbilingualsintheirearliest-exposed language.Earlybilingualexposureimpartsfundamentalchangestoclassiclanguageareas insteadofalterationstobrainregionsgoverninghighercognitiveexecutivefunctions. How-ever,ageoffirstbilingualexposuredoesmatter.Later-exposedbilingualsshowedgreater recruitmentoftheprefrontalcortexrelativetoearly-exposedbilingualsandmonolinguals. Thefindingsprovidefascinatinginsightintotheneuralresourcesthatfacilitatebilingual languageuseandarediscussedintermsofhowearly-lifelanguageexperiencescanmodify theneuralsystemsunderlyinghumanlanguageprocessing.
© 2013 The Authors. Published by Elsevier Ltd.
∗ Correspondingauthorat:800FloridaAvenueNE,Washington,DC, 20002,USA.Tel.:+12024487512.
E-mailaddress:[email protected](L.A.Petitto).
1. Introduction
Early life experiences can have a profound impact onthe developing brain and its organization (Newman
etal.,2002;Ohnishietal.,2001;Nelson,2000;Greenough
etal.,1987).Actinginunison,developmentandexperience changethebrain’sphysicalstructureandfunctional organi-zation,allowingittoadapttoitsenvironment(Hebb,1949). Exposuretotwolanguagesearlyinlifehasthepotential toyieldstructural changes inthebrain (Mechelli et al., 2004)and changes in the patterns of neural activation
1878-9293© 2013 The Authors. Published by Elsevier Ltd. http://dx.doi.org/10.1016/j.dcn.2013.06.005
Open access under CC BY license.
duringlanguageprocessingwithinthebrain’sleft hemi-sphere“classiclanguage”areasandtheirrighthemisphere homologues(Price,2012;GernsbacherandKaschak,2003), e.g., Left Inferior Frontal Gyrus (LIFG; Kovelman et al.,
2008a;Heim etal., 2005; Caplan,2001; Foundas etal.,
1998)andLeftSuperiorTemporalGyrus(STG;Zatorreand
Belin,2001;Petittoetal.,2000).Thelefthemisphere
dom-inancedoesnotimply that therighthemisphereis not involved in languageprocessing. For instance,the right hemisphere is involved in sentence processing and the integrationofsemanticinformation(Vigneauetal.,2011;
Berletal.,2010;Lukeetal.,2002;Beemanetal.,2000).
Here, we ask whether the age of exposure to two languages would yield changes in the neural resources facilitatingbilinguallanguageuseinthedevelopingbrain’s language(LIFG;STG)andhighercognitivetissue(e.g., Dor-solateralPrefrontalCortex;DLPFC;Balconi,2013;Fuster,
2008;Petrides,2005)?Whilethebrainisundergoing
mat-urational changes that support language development, wouldmonolingualandbilingualchildrenshowsimilaror
differentpatternsofbehaviorandneuralactivationwhen processinglanguage,andwouldanydifferencesberelated totheageofbilingualexposure?
Direct comparisons of bilingual versus monolingual brainswhenprocessinglanguage,specifically,during sen-tenceprocessingtasks,givesinsightsintoquestionsabout whether monolinguals and bilinguals recruit the same brainareas,withthesameextentandvariability,andfor thesame linguistic functions.Extensive bilingual expo-sureresultsinbothfunctionalandstructuralchangesin theperson’s brain(Wanget al., 2011; Kovelmanet al.,
2008a;Mechellietal.,2004;Proverbioetal.,2002).
Learn-ing a second language has been found to increase the densityofgraymatterintheleftinferiorparietalcortex
(Mechelli et al., 2004).Differential recruitmentof
clas-sic language brain areas during a language processing taskhas been observed for bilingual relative to mono-lingualadults(Kovelmanetal.,2008a).Usingfunctional magneticresonanceimaging(fMRI),bilingualadultswere foundto recruita greater extent and variability of the LIFG during a syntactic “sentence judgmenttask” rela-tivetomonolinguals.Thisincreasedrecruitmentofneural resourcessupportinglinguisticprocessinginthebilingual brainrevealeda“neuralsignature”ofbilingualism;early exposureto two languages modifies the neural activa-tionofneuralsitesandpathwaysthatunderlielanguage processing(Kovelmanetal.,2008a).“Extentand variabil-ity”isatermpreviouslypublishedinneuroimagingand morphometrystudies, bothours and others,toindicate theregionsand areasencompassedinneuralactivation (e.g.,Petittoetal.,2000;Penhuneetal.,2003).Here,we refertodifferencesintheregionsandareasofactivation as“extent,”anddifferencesintheincreasedordecreased activationas“variability,”thus,together,the“extentand variability.”
Remarkably, the degree of the neural changes is dependentontheageofacquisitionandtheproficiency levelsinthesecondlanguage(Kleinet al.,2006;Perani etal.,1998).Thefocusontheageatwhichayoungchild is first exposed to another new family or community languagehasreceivedmuchscientificattentionoverthe
pastdecadeandahalfwithinthedisciplineofLanguage Acquisitionbecauseofitsimportancetocoreissuessuchas thecritical(andsensitive)periodhypothesis(C/SPH)and theimpactofdifferentearlyexperienceonthedeveloping brain. From Language Acquisition, research on children withduallanguageexposurewithinthefirst 3years of life hasbeengenerally describedas“early,” asin early-exposed bilinguals (Montrul, 2002; Meisel, 1989,1990,
1994; Genesee etal., 1995; Paradisand Genesee,1996,
1997;Hulk,1997;Genesee,2000;Kovelmanetal.,2008b;
Petittoetal.,2000);theliteraturehasalsoreferredtothese
children as “simultaneous bilinguals” (Kovelman et al.,
2008b;Berensetal.,2013).Bycontrast,researchon
chil-drenwithduallanguageexposurefirstbeginningaround ages3–5yearshasgenerallybeendescribedas“late,”asin late-exposedbilinguals(Kleinetal.,2006;Montrul,2002;
Kovelmanetal.,2008b;Petittoetal.,2000;Montrul,2002;
VihmanandMcLaughlin,1982;McLaughlin,1984).Thisis
because,remarkably,subtledifferencesinlanguageforms (e.g.,phonologicalandsyntactic)havebeenobservedwhen thenewlanguageexposureoccursaftertheseages(again, approximately 3–5 years; Kovelman et al., 2008b); the literaturehasalsoreferredtothesechildrenas“sequential bilinguals”(Kovelmanetal.,2008b;Berensetal.,2013). Thus,the“early”and“late”agebenchmarksaretheresult of research findings investigating timing maturational andlanguageacquisitionmilestonesrelativetoimportant C/SPHandaretheonesusedinthepresentstudy.
Dual-languageexposureinearlylifehasthepotentialto moldneuralorganizationandhumanlanguageprocessing capacity,andthereissubstantialevidencethattheageof secondlanguageexposurehasbothbehavioralandneural implicationsforlanguageprocessing.Earlybilingual expo-sureyieldshighlanguagecompetenceoutcomes(Johnson
andNewport,1989;Weber-FoxandNeville,1996,2001;
McDonald, 2000;Kovelman et al.,2008b).Later second
languageacquisitionimpactstheattainmentlevelsinthe second language(Johnsonand Newport, 1989;Lardiere,
1998;Montrul,2009).Ithasbeensuggestedthatlater
expo-suretoasecondlanguageyieldsadifferentneuralprofile thanearlyexposurewithlater-exposedbilinguals show-inggreaterfrontalandbilateralneuralrecruitmentinthe
secondlanguage(Marianetal.,2003;HahneandFriederici,
2001;Wartenburgeretal.,2003).Theleveloflanguage
pro-ficiencyhasalsobeenfoundtoimpactthepatternofneural activityinthesecondlanguage(Cheeetal.,2004;Perani
etal.,2003;NauchiandSakai,2009);low-proficiency
bilin-gualsdemonstratedecreasedactivityintheLIFGrelativeto high-proficiencybilingualsforaspectofphonologicaland syntacticprocessing.
Certain levels of linguistic organization, critically phonology, aspects of morphology, and syntax, require exposure during key maturationalage periods in order toachievefullbehavioralmasteryandnative-likeneural organization(Lenneberg,1967).Thepresentstudy exam-ined aspectsofsyntacticprocessing inmonolingualand bilingualchildrenandadults.Weconducteddirect com-parisonsofthebrainsofearly-exposed(birthtobeforeage 3)bilinguals,later-exposed(age3–6)bilinguals,and mono-lingualsusingasentencejudgmenttaskthatparticipants performed while undergoing functional Near Infrared
Spectroscopy(fNIRS)neuroimaging.fNIRShassignificantly enhancedtheabilitytoimagehumanlanguageandhigher cognition; thetechnologyprovidesexcellentanatomical andtemporalresolution,isquietand“child-friendly”,and thus exceptionallysuitedfor thestudyoflanguage(see methodsbelowforamoredetaileddescription;seealso
Quaresimaetal.,2012,forareview).Moreover,thepresent
studyprovidesanovelanalyticaladvance.Hereweapplied complementarydataanalysisprocedures,which,together, provideapowerfulnewviewintotheneuralsystemsatthe heartofhumanlanguageprocessing.
Sentence judgment tasks have been widely used to assessgrammaticalknowledgeinmonolingualsand bilin-guals(Kovelmanet al.,2008a;Fernandez,2002;Caplan, 2001).Weusedarelative-clausejudgmenttaskselected from a set previously used by Kovelman et al., 2008a
(seealsoCaplanetal.,2008a,b,2003,2001,2000,1998;
Caplan,2001;Stromswoldetal.,1996).Allgroupsjudged
thesemanticplausibilityofanidenticalsetofsentences inEnglish.Thespecificsentencesconsistedoftwotypes ofsyntacticcomplexity:theobject-subjectsentencetype (OS, as in “The child spilled the juice that stained the rug”);andthesubject-objectsentencetype(SO,asin“The juicethatthechildspilledstainedtherug”).The object-subjectsentencetypeisaright-branchingrelativeclause construction, whereas the subject-object sentence type isa center-embeddedrelativeconstruction.The“easier” right-branchingrelativeclausesentencetypeisconsidered “unmarked”or“default”inEnglish,whereasthe“more dif-ficult”center-embeddedrelative clausesentencetype is consideredtobe“marked”(Stromswoldetal.,1996).
This task has previously yielded highly consistent behavioral and neuroimaging resultsshowingincreased reactiontimesandinaccuracy,andincreasedneural activ-ityintheLIFGfortheSOsentencetyperelativetotheOS sentencetype(e.g.,Kovelmanetal.,2008a;Caplanetal.,
2008a,b,2003,1998).
In thepresent study,we askedwhetherageof bilin-gualexposurecanmodifytheneuralorganizationinthe brain’s classiclanguage areas (LIFG,STG) and cognitive areas(e.g.,DorsolateralPrefrontalCortex;DLPFC)during sentenceprocessing.Domonolingual,early-exposedand later-exposedbilingualchildrenshowsimilarordifferent
patternsofbehaviorandneuralactivation?
Here we wondered whether the changes in neural activation of classic language tissue observed in adult bilinguals(calledthe“neuralsignature”forbilingualism;
Kovelmanetal.,2008a)occursinchildren,and,ifso,when
isit revealedinthedevelopingbrain?Isthepropensity fortheexpandedrecruitmentforlanguagetissue devel-opmentally malleable or fixed? How much depends on experience?
Ifyoungchildren areconsistentwithouradult
find-ings(Kovelmanetal.,2008a;Caplanetal.,2008a,b,2003,
2000,1998),then,regarding sentencetypes,thesechild
participantsarepredictedtoshowgreaterbehavioral inac-curacyandreactiontimesforthemoredifficultSOsentence typesrelativetoOSsentencetypes,withouradultcontrols performingfasterandmoreaccuratelythanthechildren. Regardinggroupdifferences,whentestedintheirearliest exposedlanguage(i.e.,English),wewouldpredictthatall
threegroupsofchildrenwillshowcomparableaccuracy andreactiontimes,thatis,theyoungmonolinguals,the early-exposedbilinguals,andthelater-exposedbilinguals. Behavioralresultsalonecannotrevealwhether mono-linguals, early-exposed and later-exposed bilinguals recruitthesamebrainareas, withthesameextentand variability,andforthesameaspectsofsentenceprocessing. Onlyneuroimagingyieldstestablehypothesesregarding what neural resources facilitate bilingual language use. Direct neuroimaging and behavioral comparisons of
developingmonolingualandbilingualbrainscanshednew light on theextent towhich earlylife experiences can modifytheneuralsystemsunderlyinghumanlanguage.A critical comparison,therefore, is whethermonolinguals, early-exposed bilinguals, and later-exposed bilinguals’ behaviorandpatternofneuralactivationduringlanguage processing is similar or different in theirfirst language and earliest exposed language, in this case, English. Importantly,allparticipantshadbeenexposedtoEnglish sincebirth(theirL1),andwerehighlyproficient,regular usersofthislanguage.Hence,incomparingmonolinguals, early-exposed, and later-exposed bilinguals’ processing andneuralactivationintheirfirstlanguage,incontrastto a comparisonbetweenearly-exposed and later-exposed bilinguals’processingandpatternsofneuralactivationin theirsecond language,wecoulddirectlyassesswhether the age of bilingual exposure would yield changes in neuralorganizationsupportingsentenceprocessinginthe nativelanguageofallparticipants.
Weexaminedthehypothesisthat bilingualexposure reflectsmorerobustneuralactivity;hence,a“neural sig-nature” of bilingualism (Kovelman et al., 2008a), and this increased recruitment of neural resources suppor-tinglinguisticprocessinginthebilingualbrainvarieswith the age of bilingual exposure. That is, early and later-exposedbilingualsshowdifferentialrecruitmentofneural resourcesforsyntacticprocessing.Laterbilingualexposure reflects more robust cognitive-general activity (greater DLPFCrecruitment),relativetobothmonolingualismand earlybilingualism.
Wehavepreviouslyobservedanincreasedextentand variabilityin neuralrecruitmentamong Spanish-English bilingual adults as compared withEnglish monolingual adults(Kovelmanetal.,2008a).Herewetestthe hypoth-esisthatbilingualexposurerecruitsagreaterextentand variabilityoftheneuralresourcesforlanguageprocessing (whichwouldconstitutetheneuralsignatureof bilingual-ism)intheadultbilingualbrain.Wefurtherpredictthatthis neuralsignatureofbilingualismwillbeobservedamong otheradultbilinguallanguagepairssuchasEnglish-French, amongothers.
Ifthedevelopingbilingualbrainshowsgreaterneural activation in classic language tissue, this would lend supporttothe“neuralsignature”hypothesisandrevealits originsindevelopment.Thatis,earlybilinguallanguage exposuremodifiesneuralactivationinlanguage-dedicated neuralsitesandpathwaysbeforetheyarefullymatured. Furthermore, if early-exposed and later-exposed bilin-gualsshowdifferentpatternsofneuralactivityforlanguage processingintheirfirstlanguage,thiswouldindicatethat bilingualism abides by principles of “Sensitive Period
Table1
Participantinformation.
Group/age Ageat testing
Ageoffirstexposureto
Mean English Other
language Monolinguals
Children 8.9 Birth n/a
Adults 19 Birth n/a
Earlybilinguals
Children 8.9 Birth Birth
Adults 19.9 Birth Birth
Latebilinguals
Children 9 Birth 4–6
Hypothesis” (Lenneberg, 1967; Newport, 1990), and crucially,thattheageofdual-languageexposurehasthe potentialtoyieldchangesinneuralactivationsupporting all language processing, and not only second language processing. Additionally, in correspondence with the behavioralpredictionsabove,wepredictthat both chil-dren’s and adults’ neuroimaging data to show greater neural activation in the LIFG for the more difficult SO sentencetypesrelativetoOSsentencetypes.
Thepresentstudyfurtherpermitsusanovellensintoa prevailingcontroversyinthefieldinvolvingthe fundamen-talnatureoflanguageinthebilingualbrain.Ifbilingualismis largelyalanguage-specificactivity,thenbilingualsshould demonstrate more robust neural activity in classic left hemisphere language areas such as the LIFG and STG relative to monolinguals. By contrast, if bilingualism is largelyacognitive-generalactivity,thentheduallanguage processingdemandsplacedonexecutivefunctions(such as,attention)mayyieldmorerobustneuralactivityinthe DLPFCinbilingualsrelativetomonolinguals.
2. Methods
2.1. Participants
20 bilingual children (9 female and 11 male, mean age=8.9, range=7–10 years) and 20 English monolin-gual children (13 female and 7 male, mean age=8.92, range=7–10years)alongwith10bilingualadults(7female and3male,meanage=19.9,range=17–26years)and9 Englishmonolingualadults(8femaleand1male,mean age=19, range=17–24years) participated in the study. We excluded one English monolingual adult from the studyduringofflinedataanalysisastheirfNIRSsignalwas unreliable.Bilingualparticipantswerefurtherdividedinto twogroups:early(3femaleand 7male,meanage=8.9, range=7–10 years) and later exposed (6 female and 4 male,meanage=9,range=7–10years).10bilingualchild and10bilingualadultparticipantsreceivedsimultaneous exposuretotheirtwolanguagesfrombirth(earlyexposed bilinguals).10bilingualchildparticipantsreceived expo-suretotheirsecond languagebetweentheages of 4–6 (laterexposedbilinguals)(seethesummaryofparticipant informationinTable1).
Allparticipantswere native speakersof English and hadbegunacquiringthislanguagefrombirth.Mostofthe
bilingualparticipants(13outof20childrenand2outof10 adults)wereEnglish-Frenchbilinguals.Asaspecificdesign featureofthisstudy,theremainingbilingualparticipants spokelanguagesfromavariedlinguisticpool.These lan-guages included Cantonese,Vietnamese, Tagalog, Tamil, Arabic,Urdu,Punjabi,Spanish,Russian,GermanandGreek. We specifically selected bilingual participants that would yield language pairs from topologically distinct languages covering analytical languages (e.g., English), morphologically rich languages (e.g., Russian, Spanish, Urdu),differentwritingsystems(e.g.,Cyrillic),andword orders (e.g., SVO (German), VSO (Arabic)). In doing so, wecoulddirectlycomparemonolingualversusbilingual brains. If we had only compared bilinguals with one languagepairing(e.g.,English-French) toEnglish mono-linguals,wemayhaveobserveddifferencesthatcouldbe attributable todifferences specifically between English-French bilinguals and English monolinguals. We could not besurethat wehave observed differences general-izable to allbilinguals versus all monolinguals and not onlytoEnglishspeakersversusEnglish-Frenchspeakers. Thatis,differencesbetweengroupscouldreflectdifference between monolinguals and bilinguals, or, alternatively linguisticdifferences between,forexample, Englishand French.Perhaps,somefeatureoftheFrenchlanguagein contrastwiththeEnglishlanguagecouldyielddifferent neuralpatternsofactivation.Thus,ourstudydesign con-trolledforthesepotentialconfounds.
All children were similar in socio-economic status (SES) as indexed by maternal education and
occupa-tion(Vekiri,2010; SéAguinetal.,1999).SESwascoded
on a scale of one through fourbased on the following grouping: upper-SES=professionals with “college grad-uate”, upper-middle-SES=service sector workers with “collegegraduate”,middle-SES=servicesectorwith“high school/GED”and“blue-collarworkers”with“college grad-uate”, and lower-SES=blue collar workers with “high school/GED”.MeanSESrankformonolingualchildrenwas 3.4,meanSESrankforearly-exposedbilingualchildrenwas 3.4andmeanSESrankforlater-exposedbilingualchildren was3.0(F(1,25)=.185,p>.05,ns).
Exclusion criteria for participants consisted of speech/language disorders, reading disabilities, devel-opmental delays, or any other neurological condition. Childrenwithsignificantvisionorhearingproblemsthat wouldinterferewiththeirabilitytoparticipatewerealso excluded.Exclusioncriteria,vision and/orhearing prob-lems were self-reportedby participants,or reportedby parentsofparticipants.Allparticipantswereright-handed. AllparticipantswerelivinginToronto,Canadaatthetime oftesting.Theparentsreceivedmonetarycompensation for their travel and adults received credit toward their first-year psychology course for their participation in thestudy.Thisstudyreceivedethicalapproval fromthe researchethicsreviewboardattheUniversityofToronto.
2.1.1. Participantscreening
2.1.1.1. Assessmentof BilingualLanguage Backgroundand Use. Parents and adult participants filled in a highly detailed standardized, previously validated and pub-lished questionnaire, which contained cross-referenced
questions(internalvalidityquestions)calledthe“Bilingual LanguageBackgroundandUseQuestionnaire”(“BLBUQ;”
seeHolowkaetal.,2002;Kovelmanetal.,2008a,b;Petitto
etal.,2001,2000;Penhuneetal.,2003formoredetails
onthisextensivebilinguallanguagequestionnaire). Par-ticipantsweregroupedasmonolinguals,early-exposedor later-exposedbilingualsbasedontheageoffirstbilingual exposure. All participants and parents of child partici-pants reported highlanguage proficiency and language useinEnglishand intheirsecondlanguage.Proficiency and usewasbasedonreportedinputlanguagesof par-ents,thelanguagesusedinthehomeandatschool,and therelativeamountofexposureineachlanguage through-outtheirlivesontheBilingualLanguageBackgroundand UseQuestionnaire.Thisquestionnaireasked(a)detailed questionsaboutparents’languageuseandattitudes (lan-guagebackground,educationalhistory,employmentfacts, socialcontextsacrosswhicheachparentuseshisorher languages,personallanguagepreferencecontaining stan-dardized questions to assess language dominance and languagepreference,personalattitudesaboutlanguage/s, languageusewiththechildandparticipant’sothersiblings, parents’linguisticexpectationsfortheirchild,parents’ atti-tudestowardbilingualism,parents’self-assessmentabout “balanced”bilingualinput,and(b)detailedquestionsabout thenatureoflanguageinputandusewiththechild lan-guagesusedwiththechild,questionsaboutchildrearing, questions aboutwhocaresfor thechildand number of hours,caretaker’slanguage/s,child’sexposurepatternsto television/radio).
Animportantfeatureinthedesignofanystudy, par-ticularlystudiesofneuralprocessing,istherequirement that there be strong confidence in one’s experimental and controlgroups. While theparticipantswereindeed groupedastotheirageoffirstbilinguallanguageexposure (thatis,“early-exposed”versus“late-exposed”),extreme rigoris appliedtoachieve cross-confirmationfor group inclusion, which is inclusiveof suchfactorsas the par-ticipants’duallanguageproficiency,languageuse,input languages of theirparents, and the like.To ensurethis cross-confirmation rigor, such information is assessed throughouruseofthestandardizedandpreviously vali-datedassessmenttool,BilingualLanguageBackgroundand UseQuestionnaire.
2.2. Stimuli
While undergoing fNIRS neuroimaging, participants were presented withthe sentencejudgment task. Both childrenandadultswerepresentedwith64English sen-tences.Thesetofsentenceshaspreviouslybeenusedby Kovelman,BakerandPetitto(2008a),whichwereprovided directly tothis researchteam by David Caplan (Caplan
etal.,2008a,b,2003,2000,1998;Stromswoldetal.,1996).
SentencesweredividedintoconditionsbasedontheOS/SO syntactic distinction, and further divided into plausible and implausible. Thus, the taskwas comprised of four conditions:OSplausible(Thelight-houseguidedthesailor that pilotedthe boat), OS implausible (*Thesailor guided the light-house that piloted the boat), SO plausible (The sailorthatthelight-houseguidedpilotedtheboat)andSO
implausible(*Thelight-housethatthesailorguidedpiloted theboat).IntheplausibleOSconstruction,theheadofthe relativeclause(thelight-house)istheobjectofthemain clauseandthesubjectoftheverboftherelativeclause. IntheplausibleSOconstruction,theheadoftherelative clause(thesailor)isthesubjectofthemainclauseandthe objectoftheverboftherelativeclause(Chenetal.,2006). A number of considerations were made when the stimuli were designed (Stromswold et al., 1996). The sentences are based on scenarios, with each scenario appearingequallyoftenacrosseachcondition.Thus, differ-encesinsemantics,wordfrequency,wordchoicecouldnot beresponsiblefordifferencesinhemodynamicresponse acrosssentencetypes.Theanimacyofsubjectandobject nounphrases and sentenceplausibility varied orthogo-nally,thus,subjectscouldnotusethesequenceofanimacy inordertomakeplausibilityjudgements.Allnounphrases weresingular, commonand definite.Sentences became implausibleatvariouspointssuchthatparticipantshadto readtheentiresentencebeforemakingajudgment.
Inthisstudy,wesoughttoexaminedifferencesamong monolinguals,early-andlater-exposedbilingualsduring syntacticprocessing.Ourdataanalysisandresults(below) apply only to the plausible OS and SO sentence types. Thefocusofthecurrentstudyonthesyntacticdistinction betweenOSandSOsentencesistheoreticallymotivated. Wespecificallyselectedthesyntacticcomplexity distinc-tion among OS and SO sentences asit permittedus to examinean aspectoflanguagestructure, syntax,which requires linguistic experience during key maturational agesforacquisition.Anadditionaldesignfeatureinusing theOS/SO distinctionisthat,beyondsyntax,itprovides insightintowhetherthebrainmightrevealdifferent neu-ralpatternsof activationfordifferenttypesofsyntactic constructions.It alsorevealswhetherthesemoresubtle syntacticdistinctionsaredifferentiallyimpactedbyearly bilingualexperience.
2.3. Procedure
We used a Dellcomputer runningE-prime software topresent thestimuli and record behavioral responses (response latencies and judgment accuracy). The par-ticipants were seated approx 30cm from the stimulus presentationmonitor.Thisstudyutilizedanevent-related method,withcounterbalancedpresentationofeach sen-tence type. Duration of stimulus presentation varied with participants’ response latency. Participants were instructedtojudgetheplausibilityofeachsentencewitha buttonpress.Crucially,participantswereinstructedtouse onlytheirrightindexfingertomaketheirselectioninorder tokeepmotorneuralactivityconsistentacrossall condi-tions.Afterparticipants’buttonpress,afixationcrosswas displayedfor2s.Theentireexperimentwasapproximately 20min.
2.4. fNIRSbrainimaging
2.4.1. fNIRSadvantagesoverfMRI
LikefMRI,fNIRSmeasureschangesinblood oxygena-tionlevels,buthasseveralcriticaladvantagesoverfMRI.
Fig.1. (a)fNIRSplacement(a)keylocationsinJasper(1958)10–20system.ThedetectorinthelowestrowofoptodeswasplacedoverT3/T4;(b)Probe arrayswereplacedoverleft-hemispherelanguageareasandtheirright-hemispherehomologuesaswellasthefrontalcortex.(c)Locationof46channels.
fNIRShasasamplingrateof10Hz,ascomparedtofMRIs samplingrateof∼onceevery2s.Thus,fNIRSisregarded as a closer measure of neural activity than the fMRI. Unlike fMRI that yieldsa combined blood oxygenlevel density (BOLD) measure (a ratio between oxygenated and deoxygenated hemoglobin), fNIRS yields separate measuresof deoxygenatedand oxygenated hemoglobin in “real time” during recording. fNIRS hasgood spatial resolution and it has better temporal resolution than fMRI(∼<5shemodynamicresponse,HR).fNIRS’depthof recordingisabout∼3–4cmdeep,butthisiswell-suited forstudyingthebrain’shighercorticalfunctions,suchas language.PerhapsfNIRS’greatestadvantageoverfMRIfor cognitiveneuroscienceresearchwithhumansisthatitis verysmall(thesizeofadesktopcomputer),portable,and virtually silent.Thislatter featuremakes it outstanding for testing natural language processing,as the ambient noisetypicalofthefMRI scannerarenotpresent. Other importantadvantagesoverfMRIisthatfNIRSisespecially participant/childfriendly(adultsandchildrensitnormally inacomfortablechair),and,crucially,ittoleratesmoderate movement.Insummary,itisthefNIRS’capacitytoprovide information on changes in blood oxygen level densi-ties/BOLD(includingtotal,oxygenated,anddeoxygenated hemodynamic change), its high sampling rate, relative silence,highermotiontolerancethanothersystems,and childfriendlyset-up,haveleadtothegrowinguseoffNIRS asoneoftoday’sleadingbrainimagingtechnologies.
2.4.2. fNIRSdataacquisition
The hemodynamic response was measured with a Hitachi ETG-4000 Near Infrared Spectroscopy system with 46 channels, acquiring data at 10Hz. The lasers werefactorysetto690and830nm.The18lasersand15 detectorsweresegregated intoone3×5arrayand two
3×3arrays(seeFig.1aandb).Oncetheparticipantwas comfortablyseated,onearraywasplacedoneachsideof theparticipant’sheadandonearraywasplacedovertop. Positioningofthearraywasaccomplishedusingthe10–20 system(Jasper,1958)tomaximallyoverlayregions clas-sicallyinvolvedinlanguageareasinthelefthemisphere as well as their homologues in the right hemisphere, and attentional and executive functioning areas in the frontallobe(foradditionaldetails,andpriorfMRI–fNIRS co-registration procedures toestablish neuroanatomical precision of probe placements,see Petitto et al., 2012;
Kovelmanetal.,2008c,d).
Priortorecording,everychannelwastestedfor opti-malconnectivity(signal/noiseratio)usingHitachi fNIRS inbuilt software.Digital photographsof left,right, front and topviewswerealsotakenofthepositioningofthe probearraysontheparticipants’headpriortoandafter therecordingsessiontoensurethatprobesremainedin theiridenticalandanatomicallycorrectpre-testing place-ment.TheHitachisystemcollectsMPEGvideorecordings ofparticipantssimultaneouswithbrainrecording,which issynchronizedwiththetestingsession.Thisoutstanding feature,among other things,makespossiblethe identi-ficationofanylargermovementartifactsthatmayhave impactedaselectchannelwhichthenbeidentifiedduring offlineanalysis.
2.5. Analysis
2.5.1. Behavioralanalysis
We first asked whethermonolinguals and bilinguals show different or similar latencies and accuracy rates acrosssentencetypes(SOandOS).Next,weaskedwhether performance varied withtheparticipant’sage (Child or Adult)andtheageatwhichtheparticipantacquiredtheir
secondlanguage(L2AoA:EarlyandLate).Weperformed a2×2×2×2(LanguageGroup×SentenceType×Age×L2 AoA)linearmixedeffectsmodelincorporatingcrossed ran-domeffects(i.e.,randomintercepts)ofsubjects.
2.5.2. fNIRSdatapre-processingandanalysis
Aftertheneuroimaging recording session, datawere exportedandthenanalyzedusinganovelanalytical proce-durewhereupontwostatisticaltechniqueswereapplied:
statisticalparametric mapping and multilevel modelingof changesinHbOconcentrations.Bydoingso,weincreased thestatisticalinferencesaffordedbyeachindividual tech-nique, thereby rendering more powerful the insights possiblefromourneuroimagingdata.Inaddition,theuse ofthesetwodifferentstatisticaltechniquespermittedus theabilitytocorroboratethefindingsacrossthe statisti-calapproaches,andthereforeenabledustoincreasethe reliabilityofourresults.
First, data were analyzed using a Matlab-based sta-tisticalsoftwarepackage:StatisticalParametricMapping for NIRS (NIRS-SPM, Version3.1) (Ye et al., 2009; Jang etal.,2009).UsingthemodifiedBeer–Lambertequation, NIRS-SPMconvertsopticaldensityvaluesinto concentra-tionchangesinoxygenatedanddeoxygenatedhemoglobin response(HbOandHbR,respectively).ChangesinHbOand HbR concentrations werefiltered witha Gaussian filter anddecomposed usingaWavelet-MinimumDescription Length (MDL) detrendingalgorithm in order toremove globaltrendsresultingfrombreathing,bloodpressure vari-ation,vasomotion,orparticipantmovementartifactsand improvethesignal-to-noiseratio(Jangetal.,2009). NIRS-SPMallowsthespatialregistrationofNIRSchannelstoMNI spacewithoutstructuralMRI(Singhetal.,2005)byusinga threedimensionaldigitizer(PolhemusCorp.)andprovides activationmapsofHbO,HbRandTHbbasedonthegeneral linearmodelandSun’stubeformulacorrection(Sun,1993;
Sunand Loader,1994).TheHbOvalueswereusedinall
subsequentanalyses(fordetailedmethodsseeespecially,
Kovelmanetal.,2009;Shalinskyetal.,2009).
Secondly,amultilevelmodeling(MLM)frameworkwas alsousedinthisstudy.Thelinearmixedmodelhasbeen showntodecreasethelikelihoodofcommittingbothType IandIIerrorsversusANOVA(Baayenetal.,2008;Locker etal.,2007).Thedatawereanalyzedasatwolevelrandom interceptvariancecomponentmodelwherethedependent variablerepresentedchangeinHbOconcentrationusing thestatistical software package SPSS(IMBInc.). First,a nullmodelcomprisingindividualNIRSchannels(level1) nested in participants (level 2)with no predictor vari-ables wascomputed.In thecase of thenull model,the significanceoftherandomtermindicatesbetweensubject andchannelvariationinHbOconcentrationchanges.Next, thenullmodelwasexpandedtoincludefixedeffectsfor SentenceType,LanguageGroup,Age,Hemisphere,Ageof SecondLanguageAcquisition,aswellasinteractionterms. The improvementsin thefit of thefull modelover the nullmodelwereassessedusingtheLogLikelihoodstatistic (2(1,N=19)=700.03,p=.05).
Inthisstudy,oneinnovationwastheapplicationoftwo different but complementary data analyses approaches (SPMand MLM analyses).SPManalysestest differences
in neuralactivation at specific sites,that is, a seriesof univariatet-testsforeachfNIRSchannel(or,forexample, ifthiswereanfMRIstudy,thefMRIvoxel). Bycontrast, MLManalysesaffordustheabilitytoincorporatetheROI as a variable in themodel. As such, ourMLM analysis permittedustomodeldifferenthemodynamicresponse patterns brain-wide by incorporating the hierarchy of datastructure.Thesignificantadvancethatacombination of SPM and MLM analyses gives us over an SPM-only approach is that we can simultaneously model neural activationacrossallROIs,andthus,donotneedtocorrect forseparate,multiplecontrasts.
Neuroimaginganalysesweredividedintowholebrain andROIanalyses.OurROIanalyseswereconducted indi-viduallyforchildrenandadultsatleftandrightIFG,leftand rightSTG,DLPFC,andPrimaryMotorCortex(controlsite).
2.5.3. Whole-BrainallChannelanalysis
Webeganwithwholebrainanalysesandaskedwhether monolingualandbilingualchildrenshowdifferentor sim-ilarpatternsofneuralactivityacrosssentencetypes(SO andOS),aswellaswhetherthepatternofneuralactivity variedamongearly-exposedandlater-exposedbilingual children. Next,we askedwhetherthepattern of neural activityobserved in monolingualand bilingual children wouldbesimilartoordifferentfromthepatternofneural activityobservedinmonolingualandbilingualadults.To dothis,wefirstgeneratedt-statisticHbOactivationmaps withlefthemisphere,righthemisphereandfrontalviews comparingLanguageGroups(MonolingualandBilingual), SentenceType(OS andSO), and L2AoA (Early-exposed orLater-exposed).Second,weperformeda2×2×2 (Lan-guageGroup×SentenceType×L2AoA)multilevelmodel (MLM) of changes in HbO concentration for child par-ticipantsand a 2×2 (Language Group×SentenceType) multilevel model (MLM)of changes in HbO concentra-tion for adult participants across all channels. Values representingconcentrationchangesinHbO werenested withinchannels,whichwerenestedwithineach partici-pant.Thus,ourmodelincorporatedcrossedrandomeffects (i.e.,randomintercepts)ofparticipantsandindividualNIRS channels.
2.5.4. IdentifyingRegionsofInterest(ROI)forfurther analysis
In the3×3and 3×5 recordingarrays, channelsare definedastheareabetweenadjacentlasersanddetectors. Eachchanneliscomprisedoftwoattenuationvaluesfrom the690nmand830nmlasers,aspersettingsofthe ETG-4000system.Attenuationvaluesfromeachchannelwere convertedtoHbOandHbRvaluesusingtheModified Beer-Lambertequation(Shalinskyetal.,2009;Yeetal.,2009; Jangetal.,2009).Thus,thechannelsreferredtochangesin HbOandHbRconcentrationsintheregionsbetweenlasers anddetectors.WeperformedspatialregistrationofNIRS channelstoMNIspaceusingMNIcoordinatesfrom avail-ableSPMtemplateimages(Yeetal.,2009;Jangetal.,2009). ThespatialregistrationyieldedvaluesforBrodmannareas maximallyrepresentedbyeachchannel,whichguidedthe selectionofROIs.Asanaddedmeasure,weselected chan-nelsoverthePrimaryMotorCortexthatdidnotcorrespond
Table2
MonolingualsandbilingualsperformedmorerapidlyandmoreaccuratelyonOSsentencesthanSOsentences.
Group/age RT(ms) %Correct Mean(SD) Mean(SD) SO OS SO OS Monolinguals 5988(436) 4956(435) 56.7(3.7) 75.5(3.7) Children 6969(419) 6123(418) 49.5(3.6) 63.5(3.6) Adults 5006(766) 3788(764) 64.0(6.6) 87.5(6.6) Earlybilinguals 6088(420) 5347(420) 62.9(3.6) 82.3(3.6) Children 6964(519) 6378(518) 56.1(4.4) 74.6(4.4) Adults 5212(661) 4316(662) 69.6(5.6) 90.0(5.6) Latebilinguals Children 6547(713) 5831(712) 63.1(6.2) 69.3(6.2)
toareasoflanguageorhighercognitiveprocessingas con-trolsites.
PCAanalyses:asanaddedmeasure,wealsoperformed aPCAtoidentifyclustersofchannelswithrobust activ-ity.FromthesePCAresults, wematchedthesechannels tothecorrespondingBrodmannareastovalidateourROI selection.12componentsemergedfromtheprincipal com-ponentanalysis,ofwhichthefirstfouraccountedfor45.3% of thetotal variance. Channels correspondingto region ofthe frontallobeincludingtheDLPFC weremost cor-relatedwiththefirstcomponent,bilateralSTG channels weremostcorrelated withthesecond component,LIFG channelsweremostcorrelatedwiththethirdcomponent, andleftposteriorSTGchannelsweremostcorrelatedwith thefourthcomponent.Thus,ourROIsincludedthebrain’s classiclanguageprocessingareas,especiallychannels max-imallyoverlayingtheLIFG(BA45/47;Broca’sarea44/45) andtheSTG(BA42/22),channelsmaximallyoverlayingthe DLPFC(BA9/46),aswellasacontrolsite.
2.5.5. RegionsofInterest(ROI)analysis
Weperformeda2×2×2(LanguageGroup×Sentence Type×L2 AoA) multilevel model (MLM) of changes in HbOconcentrationforchildparticipantsanda2×2 (Lan-guageGroup×SentenceType)multilevelmodel(MLM)of changesinHbOconcentrationforadultparticipantsacross sixbrainregions:leftIFG,rightIFG,leftSTG,rightSTG, DLPFCandPrimaryMotorCortex(controlsite).
3. Results
3.1. Behavioralresults 3.1.1. Reactiontime
Thisanalysisrevealeda maineffectofsentencetype (OSand SO;F(1,67)=33.353,p<.001)and a maineffect ofage(Child andAdult;F(1,67)=11.839,p<.001).There wasnomaineffectoflanguagegroup(Monolingualand Bilingual;F(1,67)=.174,p>.05)orL2AoA(Early-exposed orLater-exposed;F(1,91).316,p>.05).Overall,all partic-ipantsdemonstrated significantlyfaster latenciesfor OS thanSOsentences,andadultsdemonstratedsignificantly fasterlatenciesthanchildren(seeTable2).
3.1.2. Accuracy
Thisanalysisalsorevealeda main effectof sentence type(OSandSO;F(1,67)=29.776,p<.001),amaineffect
ofage(Childand Adult;F(1,67)=13.958,p<.001).There wasnomaineffectoflanguagegroup(Monolingualand Bilingual;F(1,67)=2.064,p>.05)orL2AoA(Early-exposed or Later-exposed;F(1,67)=.017, p>.05).Overall,all par-ticipantsdemonstratedsignificantlyhigheraccuracyrates onOSthanSOsentences,andadultsdemonstrated signifi-cantlyhigheraccuracyratesthanchildren(seeTable2).
3.2. Neuroimagingresults
MaineffectsofSentenceType,LanguageGroup,andAge ofSecondLanguageExposureacrossallchannelsandat ROIsaresummarizedinTable3.
3.2.1. Whole-BrainallChannel
3.2.1.1. Children. SentenceType:TheMLMrevealeda sig-nificantdifferencebetweenthemoredifficultSOversus OSsentencetypes(F(1,3715444)=4.472,p<.05).HbO acti-vationmapsalsorevealedasignificantdifferencebetween SOandOSsentences(seeFig.2a).Greaterneural activa-tionwasobservedforSOascomparedwithOSsentences.
LanguageGroup:TheMLMrevealedasignificantdifference between monolingualsand bilinguals (F(1,1701)=4.464,
p<.05).HbO activationmaps alsorevealed asignificant differencebetweenmonolingualsandearly-exposed bilin-guals(seeFig.3).Greaterneuralactivationwasobserved for early-exposed bilinguals as compared with mono-linguals. Age of Second Language Exposure: The MLM revealed a significantdifference betweenearly-exposed and later-exposedbilinguals (F(1,1701)=4.464,p<.001). HbO activation maps also revealed a significant differ-encebetweenmonolinguals,early-exposedbilinguals,and later-exposed bilinguals. Greater neural activation was observed for later-exposedbilingualsas comparedwith early-exposedbilinguals(seeFig.4)andforlater-exposed bilingual as compared with monolinguals (see Fig. 5). WealsoobservedasignificantLanguageGroup×Sentence Type (F(1,3715438)=193.509, p<.001) and a significant AgeofSecondLanguageExposure×SentenceType inter-action(F(1,3715438)=142.814,p<.001).
3.2.1.2. Adults. Sentence Type: The MLM revealed a sig-nificantdifferencebetweenthemoredifficultSOversus OSsentencetypes(F(1,1267769)=115.882,p<.001).HbO activation maps also revealed a significant difference betweenSOandOSsentences(seeFig.2b).Greater neu-ral activation was observed for SO as compared with
Table3
MaineffectsofSentenceType,LanguageGroup,andAgeofSecondLanguageExposureacrossallchannelsandatROIs.
SentenceType LanguageGroup AgeofSecondLanguageExposure
Whole-BrainallChannel
Children SO>OSF(1,3715444)=4.472,p<.05 Bilinguals>Monolinguals
F(1,1701)=4.464,p<.05 Later-Exposed>Early-Exposed F(1,1701)=4.464,p<.001 Adults SO>OSF(1,1267769)=115.882, p<.001 Bilinguals>Monolinguals F(1,851)=8.351,p<.01 N/A
LeftInferiorFrontalGyrus
Children SO>OSF(1,157185)=24.407,p<.001 Non-sig.F(1,70)=.180,p>.05 Later-Exposed>Early-Exposed
F(1,157186)=269.702,p<.001 Adults SO>OSF(1,44109)=25.158,p<.001 Non-sig.F(1,31)=.655,p>.05 N/A
RightInferiorFrontalGyrus
Children SO>OSF(1,131688)=36.179,p<.001 Non-sig.F(1,57)=.180,p>.05 Non-sig.F(1,57)=.007,p>.05 Adults SO>OSF(1,56322)=125.458,p<.001 Non-sig.F(1,31)=.655,p>.05 N/A
LeftSuperiorTemporalGyrus
Children SO>OSF(1,125084)=18.068,p<.001 Non-sig.F(1,57)=.050,p>.05 Later-Exposed>Early-Exposed
F(1,57)=8.992,p<.01 Adults SO>OSF(1,65128)=124.052,p<.001 Non-sig.F(1,43)=.846,p>.05 N/A
RightSuperiorTemporalGyrus
Children SO>OSF(1,185108)=27.417,p<.001 Bilinguals>monolinguals
F(1,82)=4.170,p<.05
Later-Exposed>Early-Exposed
F(1,82)=4.556,p<.05 Adults Non-sig.F(1,70921)=.122,p>.05 Bilinguals>monolinguals
F(1,46)=3.145,p=.083
N/A
DorsolateralPrefrontalCortex
Children SO>OSF(1,636222)=7.983,p<.01 Non-sig.F(1,287)=2.579,p>.05 Later-Exposed>Early-Exposed
F(1,287)=20.121,p<.001 Adults SO>OSF(1,160885)=20.666,p<.001 Non-sig.F(1,102)=2.068,p>.05 N/A
Controlsite(PrimaryMotorCortex)
Children Non-sig.F(1,821388)=.000,p>.05 Non-sig.F(1,376)=.192,p>.05 Non-sig.F(1,376)=2.553,p>.05 Adults Non-sig.F(1,269369)=.451,p>.05 Non-sig.F(1,177)=3.040,p>.05 N/A
OS sentences. Language Group: The MLM revealed a significant difference between monolinguals and bilin-guals(F(1,851)=8.351,p<.01).HbOactivationmapsalso revealed a significant difference between monolinguals and early-exposedbilinguals(seeFig.6).Greaterneural activationwasobservedforbilingualsascomparedwith monolinguals. We also observed a significant Language Group×SentenceTypeinteraction(F(1,1267769)=7.373,
p<.01).
3.2.2. Regionsofinterest
3.2.2.1. LeftInferiorFrontalGyrus.
3.2.2.1.1. Children. SentenceType:TheMLMrevealeda significantdifferencebetweenthemoredifficultSOversus OS sentence types (F(1,157185)=24.407, p<.001). Lan-guageGroup:TheMLMdidnotrevealasignificant differ-encebetweenmonolingualsandbilinguals(F(1,70)=.180,
p>.05). Age of Second Language Exposure: The MLM revealeda significantdifferencebetweenearly-exposed
Fig.2.NeuralactivationsforSOrelativetoOSsentencetypesfor(a)childparticipantsand(b)adultparticipants(t-statisticmapfromHbO,p=.05,corrected). ParticipantsshowedincreasedneuralactivityinthelefthemisphereSOsentencetypesrelativetoOSsentencetypes.Childrenshowedincreasedneural activityinthetemporallobe(MTG)andadultsshowedincreasedneuralactivityintheLIFG.
Fig.3.Neuralactivationofearly-exposedbilingualchildrenascomparedtomonolingualchildren(t-statisticmapfromHbO,p=.05,corrected). Early-exposedbilingualchildrenshowmorerobustneuralactivationin(a)theleftand(b)therighthemispheres(bilateralInferiorParietalLobule,STG),and(c) frontallobes(DLPFC)ascomparedtomonolingualchildren.
Fig.4.Neuralactivationoflater-exposedbilingualchildrenascomparedtoearly-exposedbilingualchildren(t-statisticmapfromHbO,p=.05,corrected). Later-exposedbilingualchildrenshowmorerobustneuralactivationin(a)theleftand(b)therighthemispheres(bilateralSTG,rightInferiorParietal Lobule)and(c)frontallobes(DLPFC,Frontopolararea)ascomparedtoearly-exposedbilingualchildren.
Fig.5.Neuralactivationoflater-exposedbilingualchildrenascomparedtomonolingualchildren(t-statisticmapfromHbO,p=.05,corrected). Later-exposedbilingualchildrenshowmorerobustneuralactivationin(a)theleftand(b)therighthemispheres(bilateralSTG),and(c)frontallobes(DLPFC, Frontopolararea)ascomparedtomonolingualchildren.
Fig.6.Neuralactivationofearly-exposedbilingualadultsascomparedtomonolingualadults(t-statisticmapfromHbO,p=.05,corrected).Bilingualadults showmorerobustneuralactivationin(a)theleft(IFG,STG)and(b)therighthemispheres(IFG,InferiorParietalLobule)ascomparedtomonolingualadults. (c)Bilingualandmonolingualadultsdonotdifferinfrontallobeactivation.
Fig.7.HbOconcentrationinbilateralBroca’sarea(BA),SuperiorTemporal Gyrus(STG)andDorsolateralPrefrontalCortex(DLPFC)forObject-Subject (OS)andSubject-Object(SO)sentencestypesacrossmonolinguals, early-and later-exposed bilinguals. Later-exposed bilinguals show greater changeinHbOconcentrationinbilateralBroca’sArea(BA)andinthe DorsolateralPrefrontalCortex(DLPFC)forbothObject-Subject(OS)and Subject-Object(SO)sentencestypesrelativetomonolinguals(p<.05). Standarderrorsareindicatedbybars.
andlater-exposedbilinguals(F(1,70)=4.801,p<.05).We alsoobservedasignificantAgeofSecondLanguage Expo-sure×SentenceType(F(1,157186)=269.702,p<.001;see
Fig.7).
3.2.2.1.2. Adults. Sentence Type: The MLM revealed a significantdifferencebetweenthemoredifficultSOversus OSsentencetypes(F(1,44109)=25.158,p<.001).Language Group: The MLM did not reveal a significant differ-encebetweenmonolingualsandbilinguals(F(1,31)=.655,
p>.05).
We also observed a significant Language Group×Sentence Type interaction (F(1,44109)=11.392,
p<.01).
3.2.2.2. RightInferiorFrontalGyrus.
3.2.2.2.1. Children. Sentence Type: The MLM revealed a significant difference between the more difficult SO versus OS sentence types (F(1,131688)=36.179,
p<.001). Language Group: The MLM not reveal a sig-nificantdifferencebetweenmonolinguals andbilinguals (F(1,57)=.180, p>.05). Age of Second Language Expo-sure: The MLM did not revealed a significant differ-encebetweenearly-exposedandlater-exposedbilinguals (F(1,57)=.007, p>.05). We also observed a significant Language Group×Sentence Type (F(1,131688)=21.490,
p<.001)andAgeofSecondLanguageExposure×Sentence Type interaction (F(1,131688)=178.531, p<.001; see
Fig.7).
3.2.2.2.2. Adults. Sentence Type: The MLM revealed a significant difference between the more difficult SO versusOSsentencetypes(F(1,56322)=125.458,p<.001).
Language Group: The MLM did not reveal a signifi-cant difference between monolinguals and bilinguals (F(1,31)=.655,p>.05).
We also observed a significant Language Group×Sentence Type interaction (F(1,44109)=11.392,
p<.01), bilinguals showed greater neural activation as comparedwithmonolingualsforSOsentencetypes.
3.2.2.3. LeftSuperiorTemporalGyrus.
3.2.2.3.1. Children. Sentence Type: The MLM revealed a significant difference between the more difficult SO versusOSsentencetypes(F(1,125084)=18.068,p<.001).
LanguageGroup:TheMLMnotrevealasignificant differ-encebetweenmonolingualsandbilinguals(F(1,57)=.050,
p>.05). Age of Second Language Exposure: The MLM revealeda significantdifferencebetweenearly-exposed andlater-exposedbilinguals(F(1,57)=8.992,p<.01).We also observed a significant Language Group×Sentence Type(F(1,125084)=56.051, p<.001)and significantAge ofSecondLanguageExposure×SentenceTypeinteraction (F(1,125084)=53.865,p<.001;seeFig.7).
3.2.2.3.2. Adults. Sentence Type: The MLM revealed a significant difference between the more difficult SO versus OS sentence types (F(1,65128)=124.052,
p<.001). Language Group: The MLM did not reveal a significant difference between monolinguals and bilin-guals (F(1,43)=.846, p>.05). We also observed a sig-nificant Language Group×Sentence Type interaction (F(1,65128)=20.213,p<.01).
3.2.2.4. RightSuperiorTemporalGyrus.
3.2.2.4.1. Children. Sentence Type: The MLM revealed a significant difference between the more difficult SO versusOSsentencetypes(F(1,185108)=27.417,p<.001).
Language Group: TheMLM revealed a significant differ-encebetweenmonolingualsandbilinguals(F(1,82)=4.170,
p<.05). Age of Second Language Exposure: The MLM revealeda significantdifferencebetweenearly-exposed andlater-exposedbilinguals(F(1,82)=4.556,p<.05).We also observed a significant Language Group×Sentence Type(F(1,185108)=161.878,p<.001)andsignificantAge ofSecondLanguageExposure×SentenceTypeinteraction (F(1,185108)=38.024,p<.001;seeFig.7).
3.2.2.4.2. Adults. Sentence Type: The MLM did not reveal a significant difference between the more dif-ficult SO versus OS sentence types (F(1,70921)=.122,
p>.05).LanguageGroup:TheMLMrevealedamarginally significant difference between monolinguals and bilin-guals (F(1,46)=3.145, p=.083). We also observed a significant Language Group×Sentence Type interaction (F(1,70921)=30.599,p<.001).
3.2.2.5. DorsolateralPrefrontalCortex.
3.2.2.5.1. Children. SentenceType:TheMLMrevealeda significantdifferencebetweenthemoredifficultSOversus OSsentencetypes(F(1,636222)=7.983,p<.01).Language Group: The MLM didnot reveal a significantdifference between monolinguals and bilinguals (F(1,287)=2.579,
p>.05). Age of Second Language Exposure: The MLM revealeda significantdifferencebetweenearly-exposed and later-exposedbilinguals(F(1,287)=20.121,p<.001). WealsoobservedasignificantLanguageGroup×Sentence Type(F(1,636222)=88.466, p<.001)and significantAge
ofSecondLanguageExposure×SentenceTypeinteraction (F(1,636222)=18.180,p<.001;seeFig.7).
3.2.2.5.2. Adults. Sentence Type: The MLM revealed a significant difference between the more difficult SO versusOSsentencetypes(F(1,160885)=20.666,p<.001).
Language Group: The MLM did not reveal a signifi-cant difference between monolinguals and bilinguals (F(1,102)=2.068,p>.05).
We also observed a significant Language Group×SentenceTypeinteraction(F(1,160885)=182.348,
p<.001).
3.2.2.6. Controlsite(PrimaryMotorCortex).
3.2.2.6.1. Children. Sentence Type: The MLM did not reveal a significant difference between the more dif-ficult SO versus OS sentence types (F(1,821388)=.000,
p>.05). Language Group: The MLM did not reveal a significant difference between monolinguals and bilin-guals (F(1,376)=.192, p>.05). Age of Second Language Exposure: The MLM did not reveal a significant differ-encebetweenearly-exposedandlater-exposedbilinguals (F(1,376)=2.553,p>.05).
3.2.2.6.2. Adults. Sentence Type: The MLM did not reveal a significant difference between the more dif-ficult SO versus OS sentence types (F(1,269369)=.451,
p>.05).Language Group: TheMLM didnotreveala sig-nificantdifferencebetweenmonolingualsand bilinguals (F(1,177)=3.040,p>.05).
4. Discussion
Thepresentstudyseeksinsightsintothenatureof lan-guageprocessinginthedevelopingbilingualbrain.Does bilinguallanguageexperienceinearlylifechangethe func-tionalorganizationofthebrainthatsupportslanguageand aspects of higher cognitiveprocessing? We were espe-ciallyinterestedtolearnwhethertheageoffirstbilingual languageexposurecanyieldneuralchangesinclassic lan-guageareas(LIFG,STG)andcognitiveareas(e.g.,DLPFC) duringsyntactic processing.Do youngbilingualsrecruit neuralresourcessupportingsentenceprocessingina man-ner similar to or different from adult bilinguals? If so, doesthis increasedneuralactivationin classiclanguage areasdependontheageofbilingualexposure(earlyversus later)?Thesequestionsallowedustogainnewinsightsinto whetherthedevelopingbrainalsoexhibitsthepropensity forexpandedneuralrecruitmentofclassiclanguagetissue thathasbeenobservedintheadultbilingualbrain,called “theneural signatureof bilingualism” (Kovelmanet al.,
2008a).
Usingasentencejudgmenttaskconsistingofsentences varyinginsyntacticand semanticcomplexity(including “default”OSsentences,andmoredifficultSOsentences),as predicted,ourbehavioraldatarevealedgreaterinaccuracy andreactiontimeswhenchildrenandadultsjudgedSOas comparedtoOSsentencetypesinEnglish(Kovelmanetal.,
2008a;Caplanetal.,2008a,b,2003,2000,1998;Chenetal.,
2006;Stromswoldetal.,1996).Here,weobservedgreater
neuralrecruitmentofthebilateralIFGforSOascompared withOSsentencetypesamongadults,corroborating previ-ousresearch(Kovelmanetal.,2008a;Caplanetal.,2008a,b,
2003,2000, 1998; Chen etal., 2006; Stromswoldet al.,
1996).Childrenalsoshowedgreaterneuralrecruitmentof thebilateralIFGforSOascomparedwithOSsentencetypes. However,whileadultsshowedmorerobustactivationfor SOsentencetypesintheIFG,childrenshowedmorerobust activationforSO sentencetypesintheMTG.While this is anintriguingdevelopmentaldifferencebetweenchild andadult,initself,theactivationpatternobservedisnot whollyunexpected.TheSTGisinvolvedinprocessing com-plexsentences, particularlyin integrating semantic and syntacticinformation(Friedericietal.,2009),theMTGis alsoinvolvedinsentenceprocessing(Vandenbergheetal.,
2002;Newmanetal.,2001).
Why might we seethe differences in neural activa-tionbetweenchildandadult?ToexplainwhytheIFGis more activeintheadultand theMTGismore activein thechild,weoffertheobservationthatmaturational dif-ferencesovertimehavebeenobservedelsewhereinthe literature,and,thereby,byanalogy,rendthepresent neu-ralpatternwellmotivatedbytypicalbraindevelopmental changes.Forexample,findingsreviewedinFriedericiand
Gierhan(2013)identifyneuralpathwaysthatconnectthe
STGwiththeIFG.Followingfromthis,weofferthatthe mat-urationoftheseorrelatedneuralpathwaysmaycontribute tothepresentfindingshowingdevelopmentaldifferences betweentemporalcortex(here, specificallytheMTG)in children,andtheIFGinadults.Otherstudiesshow intrigu-ingdevelopmentalchangesaswell.Theneuralactivationin leftinferiorparietal,leftsuperiortemporalandright tem-poralregionshavebeenfoundtodeclinewithage(Devous etal.,2006),whileactivationintheLIFGhasbeenfoundto increasewithage(Moore-Parksetal.,2010).Adults’greater LIFGactivationmightberelatedtoenhanced‘top-down’ controlthatisinvolvedinmakingaplausibilityjudgment aboutasyntacticallycomplexsentence(Moore-Parksetal.,
2010).
Regarding differences among our monolingual and bilingualgroups,behavioraldatarevealedsimilarreaction times and accuracy across the three groups (monolin-guals,early-exposedbilinguals,later-exposedbilinguals). Althoughbilingual childrendemonstrated better perfor-mance on thesentence judgment taskrelative totheir monolingualpeers,thiseffectwasnotstatistically signif-icant(e.g.,accuracyratesof56.1%and74.6%forSO and OSsentencesrespectivelyamongearly-exposedbilingual, as compared with49.5%and 63.5% amongmonolingual children). While thebehavioral data didnot revealany group differencesin sentenceprocessing, onlythe neu-roimagingdatarevealeddifferencesinneuralrecruitment amongmonolinguals,early-exposedbilingualsand later-exposedbilinguals—thosethatcarryimportanttheoretical implicationsregardingcontemporaryquestionsaboutthe nature of the bilingual brain. It is clear that this fas-cinating finding warrants more formal study, but one hypothesis(amongseveral)thatwewouldtestisthatthe Englishshowsgreateractivationinlaterexposedbilinguals because there may be stronger linguistic co-activation betweentheearlier-exposedand thelater-exposed lan-guage.
First,ourbilingualadultcontrolscorroboratedthe find-ing that adult bilinguals recruit a greater extent and
variabilityofclassiclanguageareasascomparedto mono-lingualadults(Kovelmanetal.,2008a,c).HereourSPMand MLM analysesbothrevealed greaterneuralrecruitment oftheSTGamongbilingualsascomparedwith monolin-guals.Yetoneofthemostsurprisingfindingsofthestudy weretheneuraldifferencesthatweobservedineventhe youngest bilingual child, as compared with her mono-lingualpeer.Besheanearly-exposedoralater-exposed bilingualchild,wefoundgreaterneuralactivityinclassic lefthemispherelanguagetissue,aswellastheirright hemi-spherehomologues,inourbilingualgroupsascomparedto monolinguals.Despitethefactthattheyoungbrainhasyet toundergosubstantialmaturationalchangesthatwill facil-itatelanguageprocessing,earlylifebilingualexperience hasmodifiedtheextenttowhichclassiclanguagetissue (LIFG, Broca’s, STG, and their right hemisphere homo-logues)isrecruitedforaspectsofsentenceprocessing.That this “neural signature”of bilingualismwasalso present in the developing brain suggests that the neural tissue underlyinglanguageprocessing, theLIFG and STG,may bemodifiedasaresultofbilingual languageexperience
beforeithasmaturedandindicatesthatbilingualismabides byprinciplesof“SensitivePeriodHypothesis”(Lenneberg,
1967;Newport,1990).
Anoveldesignfeatureofthisstudyisthatweexamined youngearly-exposedbilingualchildren(agesbirthtoage3 years)ascomparetolater-exposedbilingualchildren(ages 4–6years)—withparticularattentiongiventothenature oflanguageprocessingintheirfirst/earliestexposed lan-guage(inthis case,English).Whileitisunderstoodthat languageproficiencycanimpactneuralprocessing(Marian
et al., 2003; Hahne and Friederici, 2001; Wartenburger
etal.,2003;Cheeetal.,2004;Peranietal.,2003;Nauchi
andSakai,2009),weheldconstant languageproficiency
by comparingall bilingualgroups’ earliestexposed lan-guage(English)withEnglishmonolingualcontrols.Here we foundthat early-exposed bilingual children showed a differentpattern of neural activation as compared to later-exposedbilingual children.Later-exposed bilingual childrenshowedgreaterneuralrecruitmentofclassic lan-guageareas(LIFG,Broca’sArea,STG)andcognitive-general areas (DLPFC) as compared toearly-exposed bilinguals. Thisobservationimpliesthattheageoffirstbilingual lan-guage exposurehasthe potentialto modifythebrain’s developmentaltrajectorysupportinglanguageprocessing. Previous research has found differences in behavioral and neural activation for early-exposed bilinguals and later-exposedbilingualsintheirsecondlanguage(Marian
et al., 2003; Hahne and Friederici, 2001; Wartenburger
etal.,2003;Cheeetal.,2004;Peranietal.,2003;Nauchi
and Sakai, 2009). The field has attributed these
differ-encestothelaterageofacquisitionand/ortothelower proficiencylevelsin thesecondlanguage.However,the bilingualsinthepresentstudyperformedthetaskintheir earliest exposed language,which they had all acquired frombirth,usedregularly,andwerehighlyproficientin. Thus, we were ableto directly assess whether theage ofbilinguallanguageexposurewouldmodifytheneural organization supportinglanguageprocessing inthefirst languageofallparticipants.Thiswaspreciselywhat we observed.
Thepresent findings alsorevealed newinsights into theneural resources that facilitate languageprocessing inthebilingualbrain.Isbilingualismlargelya cognitive-generalprocess,wherebyduallanguageprocessingplaces increaseddemands onhigherexecutivefunctions?Oris bilingualismlargelysupportedbychangestothebrain’s classiclanguagetissue?Here,weobservedrobust recruit-mentofclassiclanguageareasinbilingualchildren (and adults)relativetomonolinguals,providingsupportforthe hypothesis that thefundamental natureof languagein thebilingualbrainissupportedbychangestoclassic lan-guagetissue.Tobesure,weobservedgreatestincreased recruitment of classic cognitive-general tissue (DLPFC) amonglater-exposedbilinguals.Thus,theneuralresources (language-specific,orcognitive-general)thatsupportthe processingoftwodifferentlanguageswithinonebrainare modifiablebytheageoffirstbilingualexposure.
5. Conclusion
Compellingevidence wasobservedinsupportof the hypothesisthatbilingualismimpartsfundamentalchanges to classic language areas as opposed to alterations to brain regions governing classic higher cognitive execu-tivefunctions.However,theageoffirstbilingualexposure doesmatter.Withrespecttothelater-exposedbilinguals, we observed the neural recruitment of both increased cognitive-generalandlanguage-specificresourcesas com-paredtomonolingualsandearly-exposedbilinguals.These resultsrevealnewinformationaboutthepotentialextent andvariabilityoflanguage-dedicatedneuraltissueandits developmentaltrajectory,andhowthismaybemodified throughexperiencewhenachildisexposedtooneortwo languages atdifferentpoints in development.Dual lan-guageexposureappears tohavean impactonhow the bilingualbrainengagestheregionsandareasthat under-liehumanlanguageandthedegreeofactivationinthese areas.Takentogether,andmostfascinatingtous,isthis: Thebilinguallanguageusermayprovideapowerfulnew windowintothehumanlanguageprocessingpotentialthat isnotfullyrecruited(engaged)inmonolinguals.The find-ingsfromthebilingualbrainleadustoatantalizingview ofthefullestbiologicalextentoftheneuraltissue underly-inglanguage,whichmaybeexploitedinthebilingualand possiblylostinthemonolingual.
How much can bilingual exposure modify the neu-ral organization for language, whethermultilingualism, relative to bilingualism, yields more variable neural recruitment,andatwhatpointinlanguagedevelopmentis thebrainmostsusceptibletoexperience-basedchanges,all demandfurtherinvestigation.Yetoneobservationstands strong:Thebilingual’srobustrecruitmentofclassic lan-guageareasmayconstitutetheunderlyingneuralsystems that give rise to the language and reading advantages observedamongbilingualchildrenrelativetotheir mono-lingualpeers(Kovelmanetal.,2008b).
Acknowledgments
The research was made possible through funds to L.A. Petitto (P.I.) in her NIH R01 Grant (USA:
NIHR01HD04582203).Additionalfundingwasalsomade possiblethroughL.A.Petitto(P.I.)’sNIHR21Grant(USA: NIHR21HD05055802). Petittois exceedingly gratefulto NIH,andsheextendsspecialthankstoDr.Peggy McCar-dle(NIH). Thisresearch wasalsomade possibleby the USA National Science Foundation’s Science of Learning Center–“VisualLanguageandVisualLearning,VL2,”and Gallaudet University (NSF Grant SBE-0541953). Petitto extendsspecialthankstoDrs.Soo-SiangLim andTanya Korelsky(NSF), and Dr.Carol Erting(Gallaudet). Petitto alsothanksthefollowingfortheirwonderful infrastruc-turesupportandfortheirinvaluableassistanceinsecuring Petitto’sHitachiETG-4000functionalNearInfrared Spec-troscopysystem:CanadianFoundationforInnovation,and theOntario Research Fund. Petitto and team thank the Hitachi Corporationfor theirkindassistance.We thank DavidCaplanforsharinghissentencestimuliwithus.We thankErinSpurgeonandCaseyCochranfortheircareful readingofpreviousversionsofthismanuscript.Weextend ourheartfeltthankstotheindividualsandfamilieswho gaveustheirtimeinordertocarryoutthisresearch.
Conflictofintereststatement:Noconflictsdeclared.
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