Cerebral Organization For Language in Deaf and Hearing Subjects - Biological Constraints and Effects of Experience

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Cerebral organization for language in deaf and hearing

subjects: Biological constraints and eects of experience
February 3, 1998
vol. 95 no. 3
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METHODS
RESULTS
Abstract
Cerebral organization during sentence processing in English and in American Sign Language (ASL) was
characterizedbyemployingfunctionalmagneticresonanceimaging(fMRI)at4T.Effectsofdeafness,age
of language acquisition, and bilingualism were assessed by comparing results from (i) normally hearing,
monolingual, native speakers of English, (ii) congenitally, genetically deaf, native signers of ASL who
learned English late and through the visual modality, and (iii) normally hearing bilinguals who were native
signers of ASL and speakers of English. All groups, hearing and deaf, processing their native language,
English or ASL, displayed strong and repeated activation within classical language areas of the left
hemisphere.DeafsubjectsreadingEnglishdidnotdisplayactivationintheseregions.Theseresultssuggest
thattheearly acquisition of a natural language is important in the expression of the strong bias for these
areastomediatelanguage,independentlyoftheformofthelanguage.Inaddition,nativesigners,hearing
anddeaf, displayed extensive activation of homologous areas within the right hemisphere, indicating that
the specific processing requirements of the language also in part determine the organization of the
languagesystemsofthebrain.
Thedevelopmentandaccessibilityofneuroimagingtechniquescontinuetopermitdetailedcharacterization
of the neural systems active during perception and cognition in the intact human brain. Research along
theselinesrevealstheadulthumanbrainasahighlydifferentiatedamalgamofsystemsandsubsystems,
eachspecializedtoprocessspecificanddifferentkindsofinformation.Acentralissueishow these highly
DISCUSSION
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References
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specializedsystemsariseinhumandevelopment,thedegreetowhichtheyarebiologicallyconstrained,and
theextenttowhichtheydependonandcanbemodifiedbyinputfromtheenvironment.Extensiveresearch
at many levels of analysis has documented that, within the domain of sensory processing, strong biases
constrain development, but many aspects of sensory organization can adapt and reorganize after both
increases and decreases in sensory input (113). For example, in humans who have sustained auditory
deprivationsincebirthsomeaspectsofvisualprocessingareunchangedwhereastheprocessingofmotion
isenhancedandreorganized(10,14,15).
It is likely that the development of the neural systems important for higher cognitive functions, including
language, are also guided by strong biases but that some of these are modifiable by experience, within
limits. Several lines of evidence suggest that cerebral organization for a language depends on the age of
acquisition of the language, the ultimate proficiency in the language, whether an individual learned more
thanonelanguage,andthedegreeofsimilaritybetweenthelanguageslearned(1621).Behavioralstudies
suggest that early exposure to language is necessary for complete linguistic proficiency, and several
differenttypesofevidenceraisethehypothesisthatearlyexposuretoalanguagemaybenecessaryforthe
hallmark specialization of the left hemisphere for language (19, 2224). Little is known about which
aspect(s) of early language experience may be important in this development. It has been proposed that
the demands of processing rapidly changing acoustic spectra is a key factor whereas other evidence
suggests that the grammatical recoding of information may be central in the differentiation of the left
hemisphereforlanguage(2527). The effects of language structure and modality on neural development
canprovideevidenceontheseproposals.
ComparisonofcerebralorganizationinnativespeakerswhoareandarenotalsonativeusersofAmerican
Sign Language (ASL) and of native signers who are and are not also native users of English permits a
uniqueperspectiveontheseissues.StudiesoftheeffectsofbraindamageinearlylearnersofASLsuggest
thatsoundbasedprocessingoflanguagemaynotbenecessaryforthespecializationofthelefthemisphere
(2830). Electrophysiological and lesionbased evidence provide limited and apparently contradictory
evidence on the proposal that the right hemisphere may play a role in processing ASL (2832). Different
linesofevidencesuggestthatareaswithintherighthemisphere may be included in the language system
when the perception and/or production of the language depend on spatial contrasts. Additionally, several
studies suggest that bilingualism is associated with a different cerebral organization than monolingualism,
but there is very little evidence on the effects of sign/spoken bilingualism on the development of the
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languagesystemsofthebrain.
ToaddresstheseissuesweemployedfMRItocomparecerebralorganizationinthreegroupsofindividuals
with different language experience.(i) Normally hearing, monolingual, native speakers of English who did
not know any ASL. (ii) Congenitally, genetically deaf individuals who learned English late and imperfectly
and without auditory input. The deaf subjects native language was ASL, a language that makes use of
spatiallocationandmotionofthehandsingrammaticalencodingoflinguisticinformation(33).(iii)Agroup
of normally hearing, bilingual subjects who were born to deaf parents and who acquired both ASL and
Englishasnativelanguages(hearingnativesigners).
METHODS
Subjects.Allsubjectswererighthanded,healthyadults(seeTable1).
Table1
In this window (922/T1.expansion.html)
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Demographicandbehavioraldataforthethreesubject
groups
Experimental Design/Stimulus Material.Eachpopulationwasscannedbyusingfunctionalmagnetic

resonance imaging while processing sentences in English and in ASL. The English runs consisted of
alternatingblocksofsimpledeclarativesentences(readsilently)andconsonant strings, all presented one
word/string at a time (600 msec/item) in the center of a screen at the foot of the magnet. The ASL runs
SUBMITANARTICLE
(HTTP://WWW.PNASCENTRAL.ORG)
consisted of film of a native deaf signer producing sentences in ASL or nonsign gestures that were
physicallysimilartoASLsigns.Thematerialwaspresentedinfourdifferentruns(twoofEnglishandtwoof
ASLpresentation counterbalanced across subjects). Each run consisted of four cycles of alternating 32
secblocksofsentences(EnglishorASL)andbaseline(consonantstringsornonsigns).Noneofthestimuli
wererepeated.SubjectshadapracticerunofASLandofEnglishtobecomefamiliarwiththetaskandthe
natureofthestimuli.
Behavioral Tests. At the end of each run, subjects were asked yes/no recognition questions on the
sentences and nonwords/nonsigns to ensure attention to the experimental stimuli (see Table 1). ANOVAs
were performed on the percentcorrect recognition. Deaf subjects also took 10 subtests of the
GrammaticalityJudgmentTest(34)toassessknowledge of English grammar (see Table 1). At the end of
each run subjects indicated whether or not specific sentences and nonword/nonsign strings had been
presented.
MR Scans.Gradientechoechoplanarimageswereobtainedbyusinga4TwholebodyMRsystem,fitted
witharemovablezaxisheadgradientcoil(35).Eightparasagittalslices,positionedfromthelateralsurface
ofthebraintoadepthof40mm,werecollected(TR=4sec,TE=28ms,resolution2.5mm2.5mm5
mm, 64 time points per image). For each of the subjects, only one hemisphere was imaged in a given
session because a 20cm diameter transmit/receive radiofrequency surface coil was used to minimize rf
interactionwiththeheadgradientcoil.Thesurfacecoilhadaregionofhighsensitivitythatwaslimitedtoa
singlehemisphere.
MR Analysis. Subjects were asked to participate in two separate sessions (one for each hemisphere).
However, this was not always possible, leading to the following numbers of subjects: (i) hearing, eight
subjects on both left and right hemispheres(ii) deaf, seven subjects on both left and right hemispheres,
plusfoursubjectslefthemisphereonlyandfivesubjectsrighthemisphereonly,(iii)hearingnativesigners,
sixsubjectsonbothleftandrighthemispheres,plusthreesubjectslefthemisphereonlyandfoursubjects
righthemisphereonly.Betweensubjectanalyseswereperformedbyconsideringleftandrighthemisphere
datafromallthreegroupsasabetweensubjectvariable.Individualdatasetswerefirstcheckedforartifacts
(runswithvisiblemotionand/orsignallosswerediscardedfromtheanalysisresultinginthelossofthedata
fromfourhearingnativesigners:twolefthemisphereonEnglish,onelefthemisphereonASL,andoneright
hemisphereonEnglish).Acrosscorrelationthresholdingmethodwasusedtodetermineactivevoxels(36)
(r 0.5, effective df = 35, alpha = .001). MR structural images were divided into 31 anatomical regions
accordingtotheRademacheretal.(37) division of the lateral surface of the brain (see Fig. 1) between
subject analyses were performed on these predetermined anatomical regions. Activation measurements
were made on the following two variables for each region and run: (i) the mean percent change of the
activation for active voxels in a region and (ii) the mean spatial extent of the activation in the region
(corrected for size of the region). In addition, a region was not considered further unless at least 30% of
runsdisplayedactivation.Multivariateanalysiswasusedtotakeintoaccounteachofthesedifferentaspects
oftheactivation.TheanalysesreliedonHotellingsT2(38)statistic,anaturalgeneralizationoftheStudents
tstatistic,andwereperformedbyusing BMDPstatisticalsoftware.Inallanalyses,thelogtransformsofthe
percent change and spatial extent were used as dependent variables, and data sets were used as
independentvariables.Activationwithinaregionwasassessedbytestingthenullhypothesisthatthelevel
ofactivationintheregionwaszero.Comparisonsacrosshemispheresand/orlanguageswereperformedby
enteringthesefactorsastreatments.
(922/F1.expansion.html)
Figure1
In a new window (922/F1.expansion.html)
Download PPT (/powerpoint/95/3/922/F1)
Corticalareasdisplayingactivation(P<.005)forEnglishsentences(vs.nonwords)foreachsubject
group.
RESULTS
The behavioral data confirmed that subjects were attending to the stimuli and were better at recognizing
sentencesthannonsensestrings[stimulus effect F(1,55) = 156, P < .0001]. All groups performed equally
well in remembering both the (simple, declarative) English sentences and the consonant strings [group
effectnotsignificant(NS)].HearingsubjectswhodidnotknowASLperformedatchanceinrecognizingASL
sentencesandnonsignsunlikethetwoothernativesignergroups(groupeffect,F(2,55)=41,P<.0001).
DeafandhearingsignersperformedequallywellonASLstimuli(groupeffectNS)(Table1).
English.When normally hearing subjects read English sentences they displayed robust activation within
the standard language areas of the left hemisphere, including inferior frontal (Brocas) area, Wernickes
area [superior temporal sulcus (STS) posterior], and the angular gyrus. Additionally, the dorsolateral
prefrontalcortex(DLPC),inferiorprecentralcortex,andanteriorandmiddleSTSwereactive,inagreement
withrecentstudiesindicatingarolefortheseareasinlanguageprocessingandmemory(3942).Withinthe
right hemisphere there was only weak and variable activation (less than 50% of runs) reflecting the
ubiquitouslefthemisphereasymmetrydescribedbyoveracenturyoflanguageresearch(Fig.1aTable2).
Incontrasttothehearingsubjects,deafsubjectsdidnotdisplaylefthemispheredominancewhenreading
English(Fig.1bTable2).Inparticular,noneofthestandardlanguagestructureswithinthelefthemisphere
displayed reliable and asymmetrical activation (all less than 50% of runs). In addition, unlike hearing
subjects, deaf subjects displayed robust activation of middle and posterior temporalparietal structures
withintherighthemisphere[seeTable2andFig.1bgroup(deaf/hearing)hemisphereeffect,Wernickes
(STSpost)P<.01angulargyrusP<.01,angularoccipitalsulcusP<.008].Thereareseveralaspectsof
these deaf subjects different experiences with English that might have accounted for this departure from
thepatternseeninnormallyhearingsubjects.First,thepossibilitythatlearningASLasa native language
contributedtotheactivationwithintherighthemispherewasassessedbyobservingtheresultsdisplayedby
thebilingual,hearingnativesigners.AsseeninFig.1candTable2,thesesubjectsdidnotdisplayreliable
righthemisphereactivation, but, as for the normally hearing, monolingual subjects, they displayed a clear
left hemisphere lateralization of the activation and a reliable recruitment of anterior left hemisphere
languageareas[group(hearing/hearingnativesigners)allareasNS].Posteriorlanguage areas within the
lefthemisphereweremoreweaklyactivatedbutweresignificantlyasymmetrical(left>right,Table2).Thus,
thelackoflefthemisphereasymmetryandthepresenceofrighthemisphereactivationwhendeafsubjects
readEnglishwasprobablynotduetotheacquisitionofASLasafirstlanguage,becausethehearingnative
signersdidnotdisplaythispattern.TheresultsforASLclarifytheinterpretationoftheseresults.
Table2
SignificancelevelsforEnglish(sentencesvs.consonant
strings)forthelefthemisphere(left),righthemisphere
(right),andthehemisphereasymmetry(hemi)foreach
groupstudied.
ASL.Next,byobservingthepatternofactivationduringsentenceprocessinginASL,weevaluatedtheroles
ofotherfactorsthathavebeenimplicatedinestablishingand/ormodulatinglanguagespecialization within
thelefthemisphere,includingtheacquisitionofanaural/orallanguagethatrequirestheprocessingofrapid
shifts of auditory temporal information, the acquisition of a natural (grammatical) language early in
development,andthestructureandmodalityofthelanguage(s)acquired.
As seen in Fig. 2a and Table3, hearing subjects who did not know ASL did not display any difference in
activationbetweenmeaningfulandnonmeaningfulsigns(consistentwiththeirbehavioraldata).
Figure2
Corticalareasdisplayingactivation(P<.005)forASLsentences(vs.nonsigns)foreachsubjectgroup
Figure3
Anatomicalregionsanalyzedinthisstudy.SeeTables1and2.
Table3
SignificancelevelsforASL(sentencesvs.nonsigns)for
thelefthemisphere(left),righthemisphere(right),and
thehemisphereasymmetry(hemi)foreachofthe
groupsstudied
Would sentence processing within a language that relies on the perception of spatial layout, hand shape,
and motion recruit classical language areas within the left hemisphere? As seen in Fig. 2b and Table 3,
whenprocessingASLdeafsubjectsdisplayedsignificantlefthemisphereactivationwithinBrocasareaand
Wernickes area. In addition, activation within DLPC, the inferior precentral sulcus, and anterior STS was
similartothatobservedinhearingsubjectswhenprocessingEnglish(Fig.2bTable3).Thisresultsuggests
thatacquisitionofaspokenlanguageisnotnecessarytoestablishspecializedlanguagesystemswithinthe
lefthemisphere.Remarkably,processingofASLsentencesindeafsubjectsalsostronglyrecruitedtheright
hemisphere, including the entire extent of the superior temporal lobe, the angular region, and inferior
prefrontalcortex(seeFig.2bandTable3).IsthisstrikingrighthemisphereactivationduringASLsentence
processing attributable to auditory deprivation or to the acquisition of a language that depends on
visual/spatialcontrasts?AsseeninFig.2candTable3,whenprocessingASL,hearingnativesignersalso
displayed right hemisphere activation similar to that of the deaf subjects (all group effects NS). Thus, the
activationoftherighthemispherewhenprocessingsentencesinASLappearstobeaconsequenceofthe
temporalcoincidence between language information and visuospatial decoding. In addition, within the left
hemisphere,robustactivationofBrocasarea, DLPC, precentral sulcus, Wernickes area, and the angular
gyrusalsowasobservedinthesehearingnativesigners(Fig.2cTable3).
DISCUSSION
Insummary,everysubjectprocessingtheirnativelanguage(i.e.,hearingsubjectsprocessingEnglish,deaf
subjectsprocessingASL,hearingnativesignersprocessingEnglish,andhearingnativesignersprocessing
ASL) displayed significant activation within left hemisphere structures classically linked to language
processing.Theseresultsimplythattherearestrongbiologicalconstraintsthatrendertheseparticularbrain
areas well designed to process linguistic information independently of the structure or the modality of the
language.Thiseffect was more robust for anterior than for posterior regions and suggests that language
experience may more strongly influence the development of posterior language areas. Elucidation of the
functionalorganizationandthefunctionalsignificanceofthelanguageinvariantareasidentifiedbythetype
of neuroimaging technique used in the present study (i.e., blood oxygenation leveldependent contrast)
requires further research. However, eventrelated brain potential (ERP) studies comparing the timing and
activationpatternsofsentenceprocessinginEnglishandASLsuggestthatsimilarneuraleventswithsimilar
timingandfunctionalorganizationoccurwithinthelefthemisphereofnativespeakersandsigners(31).The
ERP research, in line with the present study, also points to extensive right hemisphere activation in early
learnersofASLandsupportstheproposalthatactivationwithinparietooccipitalandanteriorfrontalareasof
therighthemispheremaybespecificallylinkedtothelinguisticuseofspace.AlthoughfMRIandERPresults
suggest both hemispheres are active during ASL processing in neurologically intact native signers, lesion
evidence suggests that the contribution of the right hemisphere may not be as central as that of the left
hemisphere because lasting impairments of sign production and perception have been reported after left
hemispherelesionsbutfewerdeficitshavebeenreportedafterrighthemispheredamage(28,32).Ifupheld
in future studies of congenitally deaf native signers who sustain neurological damage, such results would
suggestthatstudiesoftheeffectsoflesionsonbehaviorandneuroimagingstudiesofneurologicallyintact
subjects provide different types of information. The former point to areas that may be necessary and
sufficientforparticulartypesofprocessingwhereas the latter index areas that participate in processing in
theneurologicallyintactindividual.
RecentlesionstudiesandneuroimagingstudiesofnormaladultsreadingEnglishhaveidentifiedadditional
languagerelevantstructuresbeyondBrocasandWernickesareas,includingtheleftDLPCandtheentire
extent of the left superior temporal gyrus (3946). In the present study these areas were active when
normalhearingsubjectsreadEnglishandwhenhearinganddeafnativesignersviewedASL.Theseresults
suggest that these newly identified language areas may, like the classical language areas, mediate
languageindependentlyofthesensorymodalityandstructureofthelanguage.
The results showing a lack of left hemisphere asymmetry when deaf subjects read English are consistent
with previous behavioral and electrophysiological studies (23, 24). Previous studies of deaf subjects and
hearing bilingual subjects who perform differently on tests of English grammar suggest this effect may be
linkedtotheageofacquisitionand/orthedegreetowhichgrammaticalskillshavebeenacquiredinEnglish
(19,24).ThestrongrighthemisphereactivationindeafsubjectsreadingEnglishmaybeinterpretedinlight
of behavioral studies that report many deaf individuals rely on visualform information when reading and
encodingwrittenEnglish(47).Inthepresentstudy,asinpreviousstudies,therighthemisphereeffectwas
variableinextentandwasobservedinabout70%ofdeafsubjects.
The hearing native signers were true bilinguals, native users of both English and ASL from infancy. Their
resultsarestrikingbecausetheydisplayed,withinthesameexperimentalsession,astronglyleftlateralized
pattern of activation for reading English but robust and repeated activation of both the left and the right
hemispheres for sentence processing in ASL. The activation patterns of these subjects, although similar,
werenotidenticaltoeitherthoseofthemonolingualhearingsubjectsreadingEnglishortothecongenitally
deafsubjectsviewing ASL. For example, when reading English, both hearing groups displayed strong left
hemisphereasymmetriesoverinferiorfrontalregions. However, the hearing native signers did not display
asrobustactivationovertemporalbrainregions.Itmaybethatanteriorregionsperformsimilarprocessing
onlanguageinputindependentlyoftheformandstructureofthelanguagewhereasposteriorregionsmay
be organized to process language primarily of one form (e.g., manual/spatial or oral/aural). Further
research characterizing cerebral organization during language acquisition will contribute to an
understanding of this effect. When processing ASL, both deaf and hearing native signers displayed
significant activation of both left and right frontal and temporal regions. However, whereas the activations
were uniformly bilateral or larger in the right hemisphere for the deaf subjects, over anterior areas they
tendedtobelargerfrom the left hemisphere in the hearing native signers. This pattern suggests that the
earlyacquisitionoforal/aurallanguageinfluencestheorganizationofanteriorareasforASL.
The hearing native signers (bilinguals) displayed considerable individual differences during sentence
processing of both English and ASL. These results are reminiscent of recent reports of a high degree of
variabilityfromindividualtoindividualandareatoareaoflanguageactivationinhearing,speakingbilinguals
wholearnedtheirsecondlanguageaftertheageof7years(20,21).Thus,thesedataareconsistentwith
the proposal that in addition to individual differences in the age of acquisition, proficiency, and learning
and/orbiological substrates, the structure and modality of the first and second languages also determine
cerebralorganizationinthebilingual.
In summary, classical language areas within the left hemisphere were recruited in all groups (hearing or
deaf)whenprocessingtheirnativelanguage(ASLorEnglish).Incontrast,deafsubjectsreadingEnglishdid
notdisplayactivationintheseareas.Theseresultssuggestthattheearlyacquisitionofafullygrammatical,
natural language is important in the specialization of these systems and support the hypothesis that the
delayedand/orimperfectacquisitionofalanguageleadstoananomalouspatternofbrainorganizationfor
that language. Furthermore, the activation of right hemisphere areas when hearing and deaf native
signersprocesssentencesinASL,butnotwhennativespeakersprocessEnglish,impliesthatthespecific
nature and structure of ASL results in the recruitment of the right hemisphere into the language system.
Thisstudyhighlightsthepresenceofstrongbiasesthatrenderregionsofthelefthemispherewellsuitedto
process a natural language independently of the form of the language, and reveals that the specific
structural processing requirements of the language also in part determine the final form of the language
systemsofthebrain.
Acknowledgments
We thank Dr. Robert Balaban of the National Heart, Lung, and Blood Institute at the National Institutes of
HealthforprovidingaccesstotheMRIsystem,studentsandstaffatGallaudetUniversityforparticipationin
thesestudies,Drs.S.PadmanhabanandA.PrinsterandC.Hutton,T.Mitchell,A.Newman,andA.Tomann
forhelpwiththesestudies,Dr.J.Haxbyforlendingusequipment,andM.Baker,C.VandeVoorde,andL.
Heidenreichforhelpwiththemanuscript.ThisresearchwassupportedbygrantsfromtheNationalInstitute
on Deafness and Communication Disorders, the Human Frontiers Grant, and the J.S. McDonnell
Foundation.
Footnotes
Towhomreprintrequestsshouldbeaddressedat:DepartmentofPsychology,1227UniversityofOregon,Eugene,OR
974031227.
ThispaperwaspresentedatacolloquiumentitledNeuroimagingofHumanBrainFunction,organizedbyMichael
PosnerandMarcusE.Raichle,heldMay2931,1997,sponsoredbytheNationalAcademyofSciencesattheArnold
andMabelBeckmanCenterinIrvine,CA.
ThedeafsubjectsinthisstudyscoredmoderatelyontestsofEnglishgrammar(Table1).However,deafsubjectswho
fullyacquirethegrammarofEnglish(i.e.,score95%ontests)displayevidenceoflefthemispherespecializationfor
English(48).
ABBREVIATIONS
fMRI,
functionalmagneticresonanceimaging
ASL,
AmericanSignLanguage
ERP,
eventrelatedbrainpotential
DLPC,
dorsolateralprefrontalcortex
STS,
superiortemporalsulcus
Copyright1998,TheNationalAcademyofSciences
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