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Bozic Et Al_Bihemispheric Foundations of Human Speech Comprehension_PNAS_10

Bozic Et Al_Bihemispheric Foundations of Human Speech Comprehension_PNAS_10

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Bihemispheric foundations for humanspeech comprehension
Mirjana Bozic
, Lorraine K. Tyler
, David T. Ives
, Billi Randall
, and William D. Marslen-Wilson
Medical Research Council Cognition and Brain Sciences Unit, Cambridge CB2 7EF, United Kingdom;
Department of Experimental Psychology, Universityof Cambridge, Cambridge CB2 3EB, United Kingdom;
Department of Physiology, Development, and Neuroscience, University of Cambridge, CambridgeCB2 3EG, United Kingdom; and
Laboratoire de Psychologie de la Perception, Centre National de la Recherche Scienti
que, Université Paris Descartes, 75005Paris, FranceEdited by Willem J. M. Levelt, Max Planck Institute for Psycholinguistics, Nijmegen, Netherlands, and approved August 17, 2010 (received for review January14, 2010)
Emerging evidence from neuroimaging and neuropsychology sug-gests that human speech comprehension engages two types ofneurocognitive processes: a distributed bilateral system underpin-ning general perceptual and cognitiveprocessing, viewed asneuro-biologically primary, and a more specialized left hemisphere systemsupportingkeygrammaticallanguagefunctions,likelytobespeci
cto humans. To test these hypotheses directly we covaried increasesin the nonlinguistic complexity of spoken words [presence or ab-senceofanembeddedstem,e.g.,
)]withvariationsintheirlinguistic complexity (presence of in
ectional af
xes, e.g.,
).Nonlinguisticcomplexity, generatedbytheon-line competitionbetween the full word and its onset-embedded stem, was found toactivatebothrightandleftfronto-temporalbrainregions,includingbilateral BA45 and -47. Linguistic complexity activated left-lateral-ized inferior frontal areas only, primarily in BA45. This contrastre
ects a differentiation between the functional roles of a bilateralsystem, which supports the basic mapping from sound to lexicalmeaning, and a language-speci
c left-lateralized system that sup-ports coredecompositionalandcombinatorialprocessesinvokedbylinguisticallycomplexinputs.Thesedifferencescanberelatedtotheneurobiological foundations of human language and underline theimportance of bihemispheric systems in supporting the dynamicprocessing and interpretation of spoken inputs.
onsidered as a neuroscienti
c phenomenon, human languagecomprehension
and human language function in general
is both remarkably speci
c and remarkably distributed in itsneural instantiation. One hundred
fty years of neuropsycho-logical research demonstrate the irreplaceable role of lefthemisphere perisylvian networks (linking left inferior frontal andposterior temporal brain areas) in supporting key combinatoriallanguage functions in the domain of in
ectional morphology and syntax. At the same time, evidence from lesion studies andneuroimaging of the intact brain shows that dynamic access tolexical meaning, and the ability to rapidly construct semantic andpragmatic interpretations of incoming speech, can remain strik-ingly intact even when the left perisylvian language areas aredestroyed, implying a distributed bihemispheric substrate. Webelieve that these contrasts re
ect a fundamental distinction inthe types of processing operations underlying normal languagecomprehension and in the neural networks that support thesefunctions. In this event-related fMRI study of lexical processing, we test the hypothesis that general purpose processing demandsengage both right and left perisylvian systems, whereas linguis-tically speci
c processing demands selectively engage left hemi-sphere systems. A critical element of this account is its emphasis on thebihemispheric foundations of human speech communication.Functional imaging shows that bilateral activation of temporallobe structures in and around primary auditory processing areasis not limited to low-level acoustic and phonetic analyses, butalso implicates lexical processes. There is complementary evi-dence from neuropsychological and neuroimaging studies for theinvolvement of bihemispheric temporal regions in processesrelated to accessing lexical meaning (1). Compared with low-levelacoustic baselines, spoken words activate superior and middletemporal gyri bilaterally, regions related to meaning-based pro-cesses in language comprehension. Although researchers disagreeon the aspects of lexical processing supported by left and righthemispheres(e.g.,ref.2),neuropsychologicaldatastronglysuggestthat both hemispheres have access to representations of lexicalmeaning. Patients with extensive damage to left frontal and su-perior temporal regions but spared right hemisphere (RH)homologs can still recognize simple spoken words and producesemantic priming effects and reaction times within the normalrange, demonstrating rapid and ef 
cient access to lexical identity and meaning from auditory inputs (3). At the same time, superimposed on this highly effective basicbilateral system is a left-dominant perisylvian core languagesystem, linking left inferior frontal cortex (LIFC) with temporaland parietal cortices. Damage to these regions can cause per-manent disruption of language functions although damage toparallel RH regions typically does not. Particularly salient here isdisruption to the combinatorial aspects of language. Patients with left hemisphere (LH) damage, especially in LIFC, haveproblems with syntax and in
ectional morphology, both in pro-duction and in comprehension (4). Evidence from neuroimagingcon
rms the salience of LH contributions to language, primarillocated in inferior frontal, temporal, and inferior parietal cortex (5). In terms of grammatical function, research focused aroundregular in
ectional morphology reveals a key role for this LHfronto-temporal network in processes related to morpho-pho-nology and morpho-syntax. The selective de
cits for regular in-
ectional morphology, shown by many LH non
uent patients,point to a decompositional network linking LIFC with superiorand middle temporal cortex (6). This network handles the pro-cessing of regularly in
ected words (such as
), which are argued not to be stored as whole forms and insteadrequire morpho-phonological parsing to be segmented into stemsand in
ectional af 
 xes.These observations, combining detailed psycholinguistic andneural theories, raise basic questions about the properties of theprocessing systems that underpin human language function. Tounderstand what is special about the core LH fronto-temporalsystem, we need a better understanding both of the properties of RH systems and of the aspects of language processing that are
Author contributions: M.B., L.K.T., B.R., and W.D.M.-W. designed research; M.B. performedresearch; D.T.I.andB.R. contributednew reagents/analytic tools; M.B., L.K.T.,andW.D.M.-W.analyzed data; and M.B., L.K.T., and W.D.M.-W. wrote the paper.The authors declare no con
ict of interest.This article is a PNAS Direct Submission.Freely available online through the PNAS open access option.Data deposition: The fMRI data have been deposited in XNAT Central,http://central.xnat.org(Project ID: speech).
To whom correspondence should be addressed. E-mail:w.marslen-wilson@mrc-cbu.cam.ac.uk.This article contains supporting information online atwww.pnas.org/lookup/suppl/doi:10.1073/pnas.1000531107/-/DCSupplemental.
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common to both hemispheres. These considerations lead tospeci
c questions about the processing and representationalpropertiesofthebasicbilateralsystemhypothesizedtosupporttheaccess of simple spoken words. We predict that both hemispheres willbeinvolvedtoasimilardegreewhenthelinguisticinputconsistsof morphologically simple, high-frequency, high-imageability  words.Thesetypesofwords,inalanguagelikeEnglish,willengagegeneral purpose perceptual processing mechanisms that are notspeci
cally linguistic in nature. Such mechanisms are engaged by the unfolding nature of the speech signal, where word onsets maponto multiple lexical representations. This triggers competitionbetween these perceptual alternatives and requires additionalprocessing to select the correct candidate. Competition and se-lection between multiple alternatives are common to a range of cognitive functions, from visual perception to working memory,and are associated with increased bilateral frontal activation (7).To selectively engage these mechanisms we used words thatare not linguistically complex and do not require decompositionalanalysis, but are nonetheless perceptually complex. These aremorphologically simple words like
, which can bedirectly mapped onto underlying full-form representations, butthat also haveanonset-embedded stem (
).Thepresence of this second potential candidate for lexical access cre-ates competition between the two simultaneously activated stems.Successful choice of the correct lexical representation will there-fore involve additional decision and selection processes. Previouslanguage research indicated that selection processes require theinvolvement ofinferiorfrontalregions (8), but with fewexceptions(e.g., ref. 9) focused on LH effects. On the approach taken here,selection processes operate on lexical candidates whose analysis isconducted bilaterally, triggering the involvement of bilateral IFC.When the input changes to include linguistically more complex material, we predicted a shift in fronto-temporal involvement acrossthe hemispheres. This shift affects both the degree of left (L) tem-poral involvement in superior temporal and middle temporal gyri(STG/MTG) and the degree of LH fronto-temporal interaction.Here we focused on regular in
ectional morphemes, such as theEnglish past tense {-
}, which lead a spoken lexical input to interactdifferentially with the machinery of lexical access and linguistic in-terpretation (10). When a phonetic input such as /pre
d/ is encoun-tered,correspondingtotheword
,thelistenermustbothaccessthe lexical information associated with the stem {
} and extractthe processing implications of the presence of the grammaticalmorpheme {
}. It is the capacity to support this segmentation intostem- and af 
 x-based processes that is disrupted in patients with LHperisylvian damage (6). A key concept here is the notion of the
 ectional rhyme pattern
(IRP) as a dynamic modulator of fronto-temporalintegrationthatindicateswhetherthecurrentspeechinputcarries in
ectional information necessary for its on-line structuralinterpretation (11).TheIRPisaphonologicalpatterninEnglishthatsignalsthattheendingofacomplexwordmaybeanin
 xandthereforeshould not be treated as part of the stem. It is de
ned in terms of speci
c phonological markers
 whether the
nal consonant iscoronal [i.e., (d, t, s, z)] and whether it agrees in voice with thepreceding segment
 which are shared by all regular {-
} and {-
), in pseudoin
ected forms wherea simple word hasanapparentin
ectionalending (
). Recent fMRI results suggest that the presence of theIRP has an across-the-board triggering effect on LIFC activation,correlatedwithLtemporallobeandLanteriorcingulateactivation(11).Consistentwiththis,patientswithLIFCdamageshowmarkeddisruptions in performance when confronted with IRP stimuli,again independent of lexical status (12). Behavioral studies withunimpaired young adults (13) show increased processing com-plexity associated with the presence of the IRP for real words andnonwords and for both major types of regular in
ection in English(the past tense -d and plural -s).These results indicatea dynamic interaction between stem-accessprocesses mediated bilaterally by temporal lobe structures andpredominantly left frontal systems critical for morpho-phonologicaland syntactic parsing of the input stream (6, 12). To probe theseinteractions we covaried the two sources of processing complexity described above: whether a word ends in the IRP, invoking speci
-cally linguistic complexity, and whether it has an embedded stem,modulatinggeneralprocessingcomplexity.Simplewordslike
,exhibiting neither type of complexity, contrast both with words like
, which have an embedded stem (
) but no IRP, and with words like
, which end in a potential suf 
 x, but have no em-bedded stem. Intermediate cases like
exhibit bothforms of complexity 
each ends in a potential in
ectional af 
 x, andeachhasapotentialembeddedstem(
).Variationsinthedegree of stem competition should modulate activation bilaterally, with greater competition increasing the likelihood of IFC in- volvement. In contrast, presence or absence of the IRP should pri-marily modulate LH activation, especially where fronto-temporallinks are concerned.Because this approach predicts that LH networks, especially LIFC, should be sensitive to both of these types of processingcomplexity, it raises the question of whether the activations eli-cited will be spatio-temporally distinct or overlapping. Issues of functional specialization in LIFC are widely debated and allowfor several possible outcomes: If linguistic computations (tappedinto by the IRP conditions) are domain and region speci
c, they may generate activity in more dorsal LIFC (BA44/45), whereasdomain-general computations, elicited by stem competition,should engage more orbito-frontal areas, including BA47 (14,15). Alternatively, on a network-based account (16), the sameLIFC areas may support both linguistic and nonlinguistic pro-cessing functions, but do so in the context of different distributedprocessing networks.Finally, to be able to isolate the lexical processing network fromlower-level auditory processing, we compared word processingagainst a baseline that unambiguously separates complex auditory processing from speci
cally acoustic
phonetic analyses. Correctchoice of baseline is critical for a convincing demonstration of RHlexicalprocessing,whereinappropriatebaselines leadeither tofalsenegatives or to false positives. Our baseline for speech sounds was
musical rain
(MuR) as described in ref. 17. MuR was chosen overacoustic baselines such as spectrally rotated, noise-vocoded or re- versedspeechbecauseitprovidesaprincipledbasisforclaimingthatit closely tracks the acoustic properties of speech, while at the sametime not being interpretable as speech. The temporal envelope of each MuR segment was extracted from the corresponding speechsegment, and the two were matched in terms of the long-termspectro-temporal distribution of energy and root mean square(RMS)level.Nevertheless,despitethesimilaritiesinthedistributionof energy over frequency and time, the absence of continuous for-mantsinthesignalmeansthatMuRisnotinterpretableasbeingtheoutput of a human vocal tract and is not heard as speechlike. MuRproduces a similar level of neural activation to that of vowels in theauditory pathway up to and including primary auditory cortex inHeschl
s gyrus and planum temporale (17). In secondary auditory regions, however, such as anterior superior temporal cortex, it pro-duces much less activation than the corresponding speech.In the context of this strict auditory baseline, we can evaluatedirectly the hemispheric distribution of contrasting lexical pro-cessing systems, using a setof stimuli that covarystem competitionand suf 
 x decomposition demands(Table1).Wordsin theregularpast tense condition (e.g.,
) were all morphologically com-plex, consisting of stems and suf 
 xes. These words should triggera decomposition process on the basis of the presence of the suf 
 x. Althoughthey have aphonologicallyembeddedstem, this maynottrigger strong lexical competition because
is not thought tobe separately lexically represented (6). The second conditionconsistedofmonomorphemicwordswitharealwordembeddedattheonsetandanIRPending,e.g.,
,thustriggeringbothstemcompetitionand suf 
 x decomposition. The third condition consisted of mono-morphemic words with an IRP ending but without an onset em-beddedword,e.g.,
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generate a decomposition process, but there is no basis for stemcompetition because the remaining set of phonemes (e.g.,
)does not form a real word. Words in the fourth condition weremonomorphemic,withanembeddedstembut noIRPending,e.g.,
Thesewordsshouldtriggerstem competitionbecauseoftheembedded stem (e.g.,
). The
fth condition consisted of monomorphemicwordswith neitherembedded stemsnorIRPs,e.g.,
These are simple words that do not exhibit either lin-guistic or perceptual processing complexity, placing least demandson both bilateral and L perisylvian processing systems.
Behavioral Data.
Participants performed a gap detection task (18). All errors (1.5%) and time-outs [reaction time (RT)
3,000 ms,0.1%] were removed, and data were inverse transformed. Meanreaction times and SD for the test conditions (
responses inthe gap detection task) are shown in Table 1. A univariate ANCOVA was performed on the inverse-trans-formed RTs, with condition as a
 xed factor and speech
le dura-tion as a covariate. The results showed a signi
cant difference inRTs between conditions [
1(4, 44) = 11.6,
2(4, 194) =2.6,
0.05]. Effects of IRP presence and embeddedness weretested by grouping conditions according to presence of IRP andembedded stems and comparing them against the RTs for simple words. Simple words (e.g.,
) were responded to signi
cantly fasterthanwordswithIRPs(
2(1, 159) = 6.9,
0.01], or embedded stems (
0.05].There wasno signi
cant difference between RTs forthewords with IRPsandembeddedstems[
0.1]. These results indicate a general increase in lexical pro-cessing load for the complex items, consistent with earlier studiesusing gap detection (18).
Imaging Data.
On the basis of previous evidence (1, 15) and ourpredictions, we focused on bilateral fronto-temporo
parietalregions as the volume of interest for the analyses. Using WFUPickatlas, a mask was constructed, consisting of bilateral temporallobes (superior, middle and inferior temporal gyri, and angular gy-rus), inferior frontal gyri (pars orbitalis, pars opercularis, pars tri-angularis, and precentral gyrus), insula, and the anterior cingulate.We
rst established the network that supports complex acousticprocessing by subtracting null events from MuR. This contrastshowed bilateral activity in primary auditory cortices and sur-roundingsuperiortemporalregions(BA42/22,peaksat
, Table S1). Laterality analyses showed generally bilateralactivation, with only medial temporal activation stronger in LHcompared with RH. To conduct these laterality analyses, EPIimages were normalized onto a symmetrical T1 template, and thestandard
ipped along the
axis and compared with the original maps ina series of 
tests (19).To extract the activity speci
cally related to speech-driven lex-ical processing we contrasted words with the MuR baseline. Thiscomparison showed that lexical processes activated regions thatare anterior and ventro-lateral to the activity observed for lower-leverauditoryprocessing(Fig.1).Theselexicalactivationswereinbilateralmiddletemporalgyri(BA21)extendingintofusiformandhippocampal regions (BA20/37), angular gyrus (BA39), and an-teriorcingulate(BA32),aswellasLinferiorfrontalregionsonthelower statistical threshold of 0.01. Despite the signi
cant RH ac-tivity, these activations had a strong LH bias: The laterality anal- yses showed that lexical activity (words minus MuR) wassigni
cantly stronger in LIFC (BA44/45/47) and left angular gyrus(BA39), whereas no region showed signi
cantly more RH lexicalactivation (
, Table S2).Turning to our key questions concerning patterns of fronto-temporal activation as a function of different types of lexicalprocessing complexity, and their hemispheric distribution, we
rstconducted exploratory analyses using the multivariate linear ap-proach implemented in the MLM toolbox (20). These analysesclassi
ed conditions on the basis of the patterns of activation they evoke in the fronto-temporal volume of interest (relative to theMuR baseline) and calculated orthogonal eigencomponents thatshow greatest difference between conditions. Two eigencompo-nentsspeakdirectly tothecritical contrastsinthisstudy(detailsin
). The
rst of these (Fig. 2
) dissociates conditions withand without an embedded stem,with the divergence between
, and
(each with actual or potential embeddedstems) versus
(no embedded stems). Overlaid onthe brain (Fig. 2
) this eigencomponent shows a bilateral fronto-temporal distribution with IFC activation focused in BA47 (parsorbitalis) and extending dorsally into BA45 (pars triangularis). Inseparate analyses on RIFC and LIFC regions of interest (ROIs),the same dominant pattern emerges, accounting for 77% of the variance in RIFC and 64% of the variance in LIFC. The secondeigencomponent of interest (Fig. 2
) dissociates conditions with
Table 1. Experimental conditions and behavioral results inmilliseconds
Experimentalcondition ExampleEmbeddedstemSuf
x(IRP)RT(SD)*1. Regular past tense
? (pray) Y 970 (90)2. Pseudoregulars
Y (tray) Y 942 (65)3. No stem, with IRP
N Y 955 (68)4. Stem only
Y (clay) N 967 (92)5. Simple
N N 924 (71)
N, no; Y, yes.*Behavioral results, reaction time.
Fig. 1.
cant activation for complex acoustic processing (orange) andlinguistic processing (blue) rendered onto the surface of a canonical brain.Threshold at
0.001 voxel level and
0.05 cluster level corrected formultiple comparisons is shown.
Fig. 2.
Selected MLM eigencomponents and their overlay. Bar graphs are inthe unit of the beta images. (
) Component dissociating embedded fromnonembedded words; (
) component dissociating IRP from non-IRP words;(
) overlay on a canonical brain of the embeddedness (orange) and IRP (blue)components, shown at
1, with the overlap between them in purple.
Bozic et al. PNAS Early Edition
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