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Contents lists available at SciVerse ScienceDirect

Neuropsychologia

jo u rn al hom epa ge : www.elsev ier .com/ locate /neuropsychologia

anguage lateralisation in late proficient bilinguals: lexical decision fMRI study

aeme R.P. Park, Gjurgjica Badzakova-Trajkov, Karen E. Waldie ∗

esearch Centre for Cognitive Neuroscience, Department of Psychology, The University of Auckland, Auckland, New Zealand

r t i c l e i n f o

rticle history:eceived 22 April 2011eceived in revised form 8 December 2011ccepted 3 January 2012vailable online xxx

eywords:emisphereerebral laterality

a b s t r a c t

Approximately half the world’s population can now speak more than one language. Understanding theneural basis of language organisation in bilinguals, and whether the cortical networks involved dur-ing language processing differ from that of monolinguals, is therefore an important area of research.A main issue concerns whether L2 (second language) is processed using the same neural mechanismsthat mediate L1 (first language) processing. Moderating factors include the age of L2 acquisition and thelevel of proficiency. Here we used a lexical decision task with five conditions during functional magneticresonance imaging (fMRI) to investigate language processing in eight late proficient bilinguals whenusing Macedonian (L1) and English (L2). Bilinguals had greater bilateral activation during both L1 and L2

ilingualismanguage acquisitionroficiencyeuroimagingOLD2onolingual

processing, and therefore weaker language lateralisation, compared to matched control English monolin-guals. A greater amount of overall activation was also seen in bilinguals, especially during L2 conditions.Late proficient bilinguals living in their L2 environment employ a more extensive neural network thanmonolinguals when processing their second language.

© 2012 Published by Elsevier Ltd.

. Introduction

The role of the dominant left hemisphere in language and otherelated tasks has been well established, with lesion and imagingtudies showing a common network of cortical areas in the left peri-ylvian region (e.g. Abutalebi, Cappa, & Perani, 2001; Binder et al.,997; Hinke et al., 1993; Hugdahl, 2005; Mohr et al., 1978; Ojemann

Whitaker, 1978; Shaywitz et al., 1995; van der Kallen et al., 1998).lthough there is some evidence for right hemispheric involve-ent in linguistic functions, numerous studies show that around

7% of normal right-handed people and around 70% of normaleft-handed people have language lateralised in their left hemi-phere (e.g. Badzakova-Trajkov, Häberling, Roberts, & Corballis,010; Fabbro, 2001; Knecht et al., 2000; Obler & Gjerlow, 1999;oga & Thompson, 2003; Waldie & Mosley, 2000).

Evidence from clinical and experimental studies suggest that

Please cite this article in press as: Park, H. R. P., et al. Language lateralNeuropsychologia (2012), doi:10.1016/j.neuropsychologia.2012.01.005

eing able to speak and use more than one language may modifyrain functioning such that it differs from speakers of one lan-uage (e.g. Abutalebi et al., 2001; Aglioti, Beltramello, Girardi, &

∗ Corresponding author at: Department of Psychology, The University of Auck-and, Private Bag 92019, Auckland 1142, New Zealand. Tel.: +64 9 373 7599x88521;ax: +64 9 373 7450.

E-mail address: k.waldie@auckland.ac.nz (K.E. Waldie).

028-3932/$ – see front matter © 2012 Published by Elsevier Ltd.oi:10.1016/j.neuropsychologia.2012.01.005

Fabbro, 1996; Fabbro, 2001; Ojemann & Whitaker, 1978; Vaid,1983). Reports of clinical case studies where bilingual aphasicsshow differential language loss and/or recovery patterns have led tothe idea that bilinguals have a more global cortical representation oflanguages compared to monolinguals (Kainz, 1960; see for reviews,Fabbro, 2001; Friederici & Wartenburger, 2010; Paradis, 2001). Thisis partially supported by behavioural and neuroimaging studies,which show some evidence for spatially distinct cortical networksbetween L1 and L2 (Gandour et al., 2007; Illes et al., 1999; Kim,Relkin, Lee, & Hirsch, 1997; Meschyan & Hernandez, 2006; Pillaiet al., 2003; see for reviews, Abutalebi, 2008; Hull & Vaid, 2006,2007). These differences range from L2 eliciting a more widelydistributed pattern of activation in the left hemisphere when com-pared to L1 (e.g. Golestani et al., 2006) to the finding of additionalright hemispheric activity when using L2, leading to more bilaterallateralisation than observed for L1 (e.g. Liu, Hu, Guo, & Peng, 2010).

On the other hand, studies have reported convergent corticalrepresentation of both L1 and L2 in bilinguals (e.g. Chee, Tan, &Thiel, 1999; Illes et al., 1999; Klein, Milner, Zatorre, Zhao, & Nikelski,1999). These indicate that L2 is processed by much the same neuralareas as L1, and therefore share the same language-specific corti-

isation in late proficient bilinguals: A lexical decision fMRI study.

cal network (Klein, Milner, Zatorre, Meyer, & Evans, 1995; see forreview, Indefrey, 2006). Such variability across studies suggeststhat the main issue in bilingual research is not whether the twolanguages are mediated by completely separate neural systems, but

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ather to determine the extent to which learning a second languageodifies the language network.Two factors have been identified which are thought to partic-

larly affect the neural representation of languages: the age of2 acquisition and the level of L2 proficiency (e.g. Meschyan &ernandez, 2006; Perani & Abutalebi, 2005; Wartenburger et al.,003). The age at which the second language is acquired is thoughto have an impact on the level of proficiency attained and the rate ofearning. Generally, individuals who learn a language after a certainge do not reach the same degree of proficiency compared to youngearners (Birdsong, 1992, 1999; Hakuta, Bialystok, & Wiley, 2003).verall, the age of 6–7 years tends to be the cut-off point to deter-ine “early” versus “late” second language acquisition (Dehaene

t al., 1997; Zevin & Seidenberg, 2002).Earlier imaging studies suggest an effect of age of L2 acquisi-

ion on brain activation patterns. Weber-Fox and Neville (1996)eported different event-related potential peak latencies betweenarly and late bilinguals, where syntactic processes were observedo be affected by age as early as 1–3 years in contrast to semanticrocessing which only showed age effects around 11 years. Theseesults suggest that such differences are more likely to be greateror late bilinguals compared to early bilinguals. Kim et al. (1997)tilised fMRI to determine the spatial representation of L1 and L2y using a silent sentence-generation task in early and late bilin-uals. They found separate, distinct areas of activation for L1 and L2ithin the left inferior frontal cortex for late bilinguals only, in lineith the theory that the neural basis of L2 varies as a function of age

f acquisition. Other studies suggest an increased right hemispherenvolvement for L2 in late bilinguals compared to early bilinguals,eading to a more bilateral pattern of lateralisation (Dehaene et al.,997; Genesee et al., 1978). These results all indicate that when2 is learned late (i.e. after the age of 7), it is organised in a par-ially different manner to L1 compared to monolinguals and earlyilinguals.

Proficiency level in L2 appears to be another important factor inetermining the organisation of language processing. Research hashown that increasing proficiency in L2 mediates neural changes inate bilinguals (Meschyan & Hernandez, 2006; Perani et al., 2003,998). Wartenburger et al. (2003) used three subject groups toscertain the effects of both age of acquisition and proficiency lev-ls on bilinguals: early acquisition high proficiency (EAHP); latecquisition high proficiency (LAHP); and late acquisition low profi-iency (LALP). They found age of acquisition effects in grammaticaludgment tasks only, with larger activations in those subjects whocquired L2 after the age of 6. However, both grammar and semanticrocessing were affected by proficiency level, with greater activ-

ty seen in the LALP group compared to the LAHP subjects. Othertudies also show similar cortical activations for both L1 and L2 pro-essing in highly proficient bilinguals (Klein et al., 1995; Tan et al.,003), but not for less fluent L2 speakers (Dehaene et al., 1997).

Abutalebi et al. (2001) reviewed the role of both linguistic factorsn 11 neuroimaging studies and found that early bilinguals showedo cortical differences in L1 and L2. However, different patterns ofctivation were found between less proficient and highly proficientate bilinguals, which led the authors to conclude that proficiencyevel has the greatest effect on the cortical representation and pro-essing of the second language. They further stressed that when thisactor is kept constant, age of acquisition does not seem to affectow the languages are organised in the bilingual brain. These differ-nces in activation between proficient and less proficient bilingualsay be attributed to a lack of cognitive control and the need for

reater cognitive effort in those who are not fluent in L2.

Please cite this article in press as: Park, H. R. P., et al. Language lateraNeuropsychologia (2012), doi:10.1016/j.neuropsychologia.2012.01.005

Much of the past and present literature suggests that theeural organisation of language in bilinguals is a multifacetedrocess which is influenced by various external factors. From neu-oimaging studies, it has been shown that the age of acquisition

PRESSlogia xxx (2012) xxx– xxx

and proficiency factors differently affect left hemisphere neuralnetworks, but the results are unclear. No general consensus hasyet been reached on whether these variables have an effect on thelateralisation of languages in bilinguals. In particular, most of theresearch focusing on proficiency has involved bilinguals who areadvanced L2 speakers still living in their native (L1) environment.

Here, the aim was to examine the neural basis of bilingualismby identifying the key cortical regions associated with linguisticprocessing in late but proficient bilinguals with a high level ofexposure to L2 (living in the L2 environment). Functional MRI wasutilised to investigate the possible differences between bilingualsand monolinguals when performing lexical decision tasks first intheir native language and then in English (L2). Particular attentionwas paid to whether bilinguals engage additional brain areas, asso-ciated with extra cortical effort, compared to monolingual Englishspeakers, when using L2. Laterality indices were also calculated fortwo regions of interest (frontal and temporal lobes) based on theactivations seen in these areas.

2. Methods

2.1. Participants

A total of 8 late proficient bilinguals (4 males, M = 25.00, SD = 3.27; 4 females,M = 24.75, SD = 2.50) and 9 monolinguals (2 males, M = 26.00, SD = 1.41; 7 females,M = 26.71, SD = 7.78) were recruited from the University of Auckland, New Zealand,and through advertising at community events for bilinguals. Subjects gave theirinformed consent to participate in the study and all experimental procedures wereapproved by the University of Auckland Human Subjects Ethics Committee. All par-ticipants completed the Edinburgh Handedness Inventory (Oldfield, 1979) and wereright handed.

The monolingual group included only pure English speakers. The bilingual grouptargeted for this study was Macedonian–English bilinguals. This group was cho-sen because of the relatively large Macedonian community in Auckland, and alsobecause we were able to translate the task ourselves. Potential bilingual participantswere asked to fill in a questionnaire regarding the age of L2 (English) acquisition,manner of L2 acquisition, age of immigration to L2 environment, time spent in L2environment and also self-reported language proficiency. They were required to bepermanent NZ residents or NZ citizens who acquired L2 after the age of 6 in a formalsetting (school).

L2 proficiency was assessed using a computerised Quick Placement Test (QPT;University of Cambridge, 2001) where the participants’ L2 listening, reading, gram-mar and vocabulary were measured. The QPT is a 15–20 min computerised testwhich automatically adapts the difficulty level based on the participants’ previousanswers. It has been validated by more than 5000 English students in 20 countries.The results are categorised into one of six levels based on their score (out of 100)from Beginner (0–39) to Very Advanced (80–100). The cut off criterion for the cur-rent study was a score of 60 which corresponded to the Upper Intermediate levelin the test, and from the initial recruitment, four bilingual volunteers who did notmeet this criterion were excluded from the study.

2.2. Procedure and stimuli

The study design was a blocked experimental design that used a ‘go/no-go’response paradigm (e.g. participants were instructed to press a button with theirright hand if the letter string was a real word). In total, three experimental and threefixation/baseline blocks were used for the three conditions in the study: each exper-imental block lasted for 48 s and was preceded by an 18 s fixation/baseline block.Stimuli were presented in Courier New Bold, 35 font size, using E-Prime (Psycho-logical Software Tools, Pittsburgh, PA). Twenty stimuli were randomly presented ina black font on a grey background for each experimental block. Each stimulus waspresented for 2000 ms followed by a 400 ms interstimulus interval, which was ablank grey screen.

Participants were instructed to press the mouse button when the shapes werepointy for the nonverbal condition; when the letters were upper-case for theletter case judgment condition; and when the words were real, regular wordsfor the lexical decision condition. Both reaction times and accuracy data wererecorded.

Both the monolingual and the bilingual participants completed the three con-ditions in the same order: nonverbal; letter case judgment; and lexical decision.The bilinguals completed the experiment once in L1 (Macedonian) and once in L2

lisation in late proficient bilinguals: A lexical decision fMRI study.

(English). The order of language used was counterbalanced between the subjects,with half the subjects doing the tasks in L1 first and then L2, and the other halfstarting with L2 and finishing with L1.

Stimuli in the letter case judgment condition consisted of letter strings whichwere presented either in lower- or upper-case (e.g. PMFGH or wvmgh). Stimuli in

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he lexical decision condition were regular words that were spelt phonetically andength-matched non-words that could easily be sounded out but did not exist (e.g.AIN or FRAC). These words were all presented in upper-case letters. The controlonverbal stimuli consisted of various shapes which either had pointy or smoothdges.

.3. Image acquisition

Images were acquired using a 1.5T Siemens Avanto scanner (Erlangen, Germany)t the Centre for Advanced Magnetic Resonance Imaging (CAMRI) in Grafton, Auck-and.

Scanning sessions began with acquisition of T1-weighted structural volumessing 3D MP-RAGE sequence (TR = 11 ms; TE = 4.94 ms; flip angle: 15◦; FOV:5.6 cm × 20.8 cm; matrix size: 256 × 208; 170–176 axial slices parallel to the AC-PC

ine; interslice gap: 0 mm; resulting in 1 mm × 1 mm × 1 mm voxels, axial acquisi-ion, parallel to AC-PC line, ensuring whole brain coverage). Forty-four scans werecquired for each condition, resulting in a total of 220 T2*-weighted volumes for theilingual subjects (nonverbal, letter case judgment and lexical decision task in L1,

etter case judgment and lexical decision task in L2), and a total of 132 T2*-weightedolumes for the monolingual subjects (nonverbal, letter case judgment and lexi-al decision task) in the EPI sequence. These also consisted of 2 initial ‘dummy’cans at the beginning of each sequence to control for T1 saturation, which were notncluded in the analysis. The EPI acquisition sequence parameters were as follows:R = 3000 ms; TE = 50 ms; flip angle = 90◦; FOV = 19.2 cm; matrix size: 64 × 64; withnterleaved slice acquisition, starting at the bottom; 30 slices parallel to AC-PC line;lice thickness: 4 mm; 25% gap: resulting in 3 mm × 3 mm × 5 mm voxels; wholerain coverage of 150 mm.

.4. Image pre-processing and analysis

The fMRI data were analysed using SPM5 software implemented onATLAB (Wellcome Department of Imaging Neuroscience, London, UK;

ttp://www.fil.ion.ucl.ac.uk). The first volume of the first session was used as reference for coregistration of the first volume for the subsequent sessions. Theemaining volumes were realigned to the first volume within each session and aean of all volumes across the conditions were created. The realigned volumesere corrected for slice timing differences and referenced to the middle slice. The

1 volumes were coregistered and averaged. The average T1-weighted structuralmage was then coregistered to the mean of the functional volumes. By usinghe unified segmentation procedure, normalisation parameters were estimatedAshburner & Friston, 2005), which were then used to normalise both the functionalnd structural mages to the stereotactic coordinate system defined by the Montrealeurological Institute (MNI). Finally, the functional data were smoothed with annisotropic Gaussian filter of 9 mm × 9 mm × 15 mm (three times the voxel size)ull width at half maximum (FWHM) using a standard SPM method.

Functional data were analysed by performing a random-effects factorial ANOVA.wo 3 × 2 factorial ANOVAs with condition (nonverbal, letter case, lexical decision)s a within-subjects factor and group (monolinguals, bilinguals) as a between-ubjects factor were evaluated for L1 and English, separately. A third 3 × 2 factorialNOVA with condition (nonverbal, letter case, lexical decision) and language (L1,2) as within-subject factors was calculated for the bilingual group only. Correctionor possible heterogeneity of variance as well as for the violation of sphericity result-ng from the use of repeated measures was implemented by SPM5. Each condition

as compared to fixation and an uncorrected threshold of p < .001, and a contiguityhreshold of 10 voxels was used for each comparison.

.5. Laterality index calculations

Laterality indices (LI) were calculated to determine the language lateralisationor both the monolingual and bilingual groups. These indices range from −1 to1 in values, with −1 representing complete right hemispheric lateralisation and1 complete left hemispheric lateralisation (Wilke & Lidzba, 2007). The LI toolboxpplies a bootstrapping technique which calculates about 10,000 indices at different

Please cite this article in press as: Park, H. R. P., et al. Language lateralNeuropsychologia (2012), doi:10.1016/j.neuropsychologia.2012.01.005

hresholds generating a robust minimum, maximum, and mean LI.

I =∑

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activation(right)∑

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activation(right)

able 1ean median reaction times (RTs) in milliseconds and mean accuracy for each condition

Group Condition

Nonverbal (shapes) Letter

RT Accuracy RT

Monolinguals 629.34 .94 527.44Bilinguals’ L1 527.91 .84 496.90Bilinguals’ L2 527.91 .84 431.24

PRESSlogia xxx (2012) xxx– xxx 3

An overall weighted bootstrapped LI is then calculated by taking these thresh-olds into account. For the present study, this weighted mean LI was calculated fortwo regions of interest (ROI). These ROIs were the frontal and temporal lobes whichwere predefined in the LI toolbox (Wilke & Lidzba, 2007).

2.6. Behavioural analyses

Four separate statistical analyses were performed to determine if there were anysignificant behavioural differences both between and within groups. The four typesof analyses consisted of: between-group comparison of performance during thenonverbal (shapes) task; between-group comparison of performance during boththe letter case judgment and the lexical decision conditions in their native language(L1); between-group comparison of performance during both conditions in English(L2 for bilinguals); and within-group comparison of performance for L1 and L2 in thebilingual group only. SPSS Version 14.0 for Windows was used for all data analyses.Effects were considered significant at p < .05 level and pairwise comparisons wereanalysed with a Bonferroni adjustment to the alpha level.

3. Results

3.1. Behavioural results

3.1.1. Nonverbal taskThe accuracy and reaction time (RT) data were subjected to an

independent samples Group t-test. No significant differences werefound with either the accuracy or RT data between the groups.

3.1.2. L1The accuracy and RT data were subjected to a Condition × Group

Split plot ANOVA, with Condition as a within-subjects factor. Therewere no significant main or interaction effects for either analysis.

3.1.3. EnglishThe accuracy and RT data were subjected to a Condition (let-

ter case judgment, lexical decision task) × Group Split plot ANOVA,with Condition as a within-subjects factor. The data revealed nosignificant main or interaction effects. The RT data revealed a sig-nificant main effect of Condition (F(1,11) = 22.80, p = .001) and asignificant Group by Condition interaction (F(1,11) = 11.52, p = .006).Bilinguals performed significantly faster during letter case judg-ments than during lexical decision-making (p < .001). Importantly,group differences were not found within conditions.

3.1.4. L1 versus L2 in bilingualsThe accuracy and RT data were subjected to a Condi-

tion × Language (L1, L2) repeated measures ANOVA. The accuracydata showed no significant main or interaction effects. The RT datarevealed a significant effect for Language (F(1,7) = 43.26, p < .001)and a significant Condition by Language interaction (F(1,7) = 6.144,p = .042). There were no differences between L1 and L2 in termsof RT for the letter case condition. For the lexical decision condi-tion, the difference between the languages approached significance(p = .058), with faster RTs in L1 compared to L2. For L1, there wereno response time differences between the two conditions but a

isation in late proficient bilinguals: A lexical decision fMRI study.

significant difference was found for L2 (p < .001).Overall, the behavioural data showed that the task performance

of the bilinguals in English was comparable to the monolingualswith both groups achieving an accuracy rate of ≥84% (Table 1).

(nonverbal, letter case, lexical decision) for monolinguals and bilinguals.

case Lexical decision

Accuracy RT Accuracy

.95 605.55 .97 .90 571.21 .84

.87 651.38 .89

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Fig. 1. Significant clusters of activation for the monolingual group (A) and the bilin-gual group using L1 (B) and L2 (C), for the Lexical decision versus Baseline contrasto

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hemisphere including areas such as the inferior and middle frontalgyri, inferior and superior parietal gyri, as well as the fusiform

n section overlay (uncorrected, p < .001).

.2. fMRI results

Functional MRI results for both the monolingual and bilingualroups were analysed and organised according to the contrast ofnterest. The four contrasts used for the current study were, in

Please cite this article in press as: Park, H. R. P., et al. Language lateraNeuropsychologia (2012), doi:10.1016/j.neuropsychologia.2012.01.005

rder of presentation of the findings: (1) Nonverbal minus (i.e.ersus) Baseline; (2) Letter case judgment versus Baseline; (3)

PRESSlogia xxx (2012) xxx– xxx

Lexical decision versus Baseline; (4) Lexical decision versus Lettercase judgment.

In addition, three separate group analyses were also performedon the fMRI data. The analyses consisted of a between-group com-parison in L1, a second between-group comparison in English, anda within-group comparison of the bilinguals’ performances in L1and L2. The contrasts of interest used for these group comparisonswere: (1) Letter case judgment versus Baseline; (2) Lexical decisionversus Baseline.

3.2.1. MonolingualsFor the Nonverbal task and Letter case judgment contrasts, both

of which did not require a high level of linguistic processing, pre-dicted cortical activity was observed in the occipital areas such asthe left middle occipital gyrus. Further significant bilateral activa-tion was seen in the inferior parietal lobule and inferior frontal gyrias well as in the right fusiform and lingual gyri.

The Lexical decision versus Baseline contrast elicited the great-est spread of activation than that observed for the other threecontrasts (Nonverbal, Letter case judgment, and Lexical decisionversus Letter case judgment). The subjects predominantly showedcortical activity in the left hemisphere including the inferiorand middle occipital gyri, inferior frontal gyrus, precentral gyrus,superior temporal gyrus, and inferior parietal gyrus. Some righthemisphere activation was observed in the lingual and fusiformgyri, the insula cortex and the superior medial gyrus.

In the Lexical decision versus Letter case judgment contrast, thesubjects only showed slight right hemispheric activations in theinferior frontal gyrus and the cingulate gyrus.

3.2.2. Bilinguals – L1 (Macedonian)The subjects showed significant bilateral activity for both the

Nonverbal task and Letter case judgment contrasts. This wasobserved especially in the lingual gyri, the parietal lobule and theoccipital gyri. In the right hemisphere, most of the activity was con-centrated within the inferior and middle frontal gyri area while inthe left hemisphere, inferior parietal and middle occipital gyri wereactivated. In addition, significant activation was also seen in the leftsupramarginal gyrus and the cerebellum.

In the Lexical decision versus Baseline condition, the bilingualsshowed the most significant activity in the left postcentral gyrus,left inferior frontal gyrus, left middle occipital gyrus, and the leftinferior occipital gyrus indicating left lateralisation for this com-parison. Right hemispheric activation was also observed to a lesserextent in the fusiform gyrus, precuneus, superior parietal lobule,inferior occipital gyrus, and the cerebellum.

In the Lexical decision versus Letter case judgment condition,activity was observed only in the left inferior frontal gyrus, rightcerebellum, and the parietal lobule.

3.2.3. Bilinguals – L2 (English)In the Letter case judgment conditions, the bilingual group

again showed significant activity in both the left and right hemi-spheres. Left hemispheric activations included regions of inferiorparietal lobule, middle occipital gyrus, and the fusiform gyrus. Inthe right hemisphere, activity was observed in the inferior and mid-dle frontal gyri, superior parietal lobule, and the precentral andangular gyri.

In the Lexical decision versus Baseline condition, significantbilateral activity was seen in the occipital region such as the middleoccipital gyrus. Much of the activations were observed in the right

lisation in late proficient bilinguals: A lexical decision fMRI study.

and angular gyri. Other left hemispheric activations included theinferior and superior parietal lobule.

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In the Lexical decision versus Letter case comparison, the par-icipants showed significant activations in the left inferior frontalyrus and the left precentral gyrus (Fig. 1).

.2.4. Between group comparisons – L1Significant differences between groups were observed in the

etter case versus Baseline comparison, with the bilingual grouphowing greater activation than the monolingual group in the rightuperior occipital gyrus, right superior parietal lobule, right post-entral and superior orbital gyri, right insular lobe, and the rightiddle temporal gyrus. Greater activity in the left hemisphere was

een in the fusiform and lingual gyri.In the Lexical decision versus Baseline condition, significant

ifferences between the groups were again present. Monolingualubjects showed greater activation only in the right supramarginalyrus. Bilingual subjects showed significantly greater activation,specially in the left hemispheric regions such as the middle anduperior occipital gyri, lingual and fusiform gyri, and the cuneus.ctivity in the right hemisphere was also present in the middleccipital gyrus.

.2.5. Between group comparisons – EnglishSignificant differences were found between the two groups

hen using English (L2 for the bilingual group). Monolinguals didot show any greater activation compared to bilinguals for either ofhe two comparisons. In the Letter case versus Baseline condition,he bilinguals showed greater bilateral activation than the mono-inguals in the superior temporal gyrus. Further right hemispherectivity was observed in the cuneus, cerebellum, precentral andostcentral gyri, and the inferior frontal and middle occipital gyri.

In the Lexical decision versus Baseline condition, bilingualshowed several significant areas of bilateral activity including theusiform, postcentral, and the middle occipital gyri. In addition, leftemispheric activity was seen in the lingual gyrus. Greater activa-ion in the right middle occipital gyrus was also observed (Fig. 2).

.2.6. Within group comparisonsSignificant differences between the two languages were found

n the bilingual group. These differences were found in the L2 > L1i.e. English minus Macedonian) direction only, suggesting that

ore cortical effort is needed when using their second language. Inoth contrasts, greater activation was observed in the right hemi-phere in the bilinguals (Table 2).

.3. Laterality index results

.3.1. Between group results for L1In the frontal lobe, the bilinguals showed right hemispheric lat-

ralisation (M = −.258, SD = .368), compared to monolinguals whohowed left lateralised activation (M = −.246, SD = .287) for the Let-er case condition. This difference was significant (t(15) = −3.161,

= .006).There were no significant differences observed in the Nonverbal

nd Lexical decision conditions.In the temporal lobe, a general trend of overall weaker left hemi-

phere activity was evident in the bilingual group when comparedo monolinguals. These differences, however, did not reach statis-ical significance.

.3.2. Between group results for L2 (English)There were no significant differences in laterality between the

ilingual and monolingual groups in the frontal lobe.

Please cite this article in press as: Park, H. R. P., et al. Language lateralNeuropsychologia (2012), doi:10.1016/j.neuropsychologia.2012.01.005

In the temporal lobe, the monolinguals showed strong left later-lity for all three conditions. The bilinguals showed left hemisphereateralisation in the Nonverbal condition and bilateral languagerocessing in the Letter case condition. These differences were

language. (B) Activation clusters between the two groups for the same contrast ofinterest in English (L2 for bilinguals).

again not significant. In the Lexical decision comparison, the mono-linguals showed left lateralised activation in the temporal lobe(M = −.440, SD = .274). This pattern of left lateralisation was alsoobserved in the bilinguals but to a much lesser extent (M = .069,SD = .376). This difference in the degree of lateralisation was signif-icant (t(15) = −2.349, p = .033) (Fig. 3).

4. Discussion

The results from the present study indicate that during lan-guage processing, bilinguals are left hemisphere dominant, with aneural network that is mostly similar to that of monolinguals. How-ever, a more extensive pattern of activation in the left hemisphereand some right hemispheric activity were observed, resulting in aweaker lateralisation of language for bilinguals compared to mono-

isation in late proficient bilinguals: A lexical decision fMRI study.

linguals. Bilinguals also exhibited more activity when using boththeir native and second languages compared to monolinguals, andmore activity when using their L2 compared to L1.

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6 H.R.P. Park et al. / Neuropsychologia xxx (2012) xxx– xxx

Table 2Cortical regions showing significant differences between the native language and second language (L2) within the bilingual group during letter case judgments and lexicaldecision. Cluster extent in mm3, with summary T-statistics, Brodmann areas (BA), and Talairach coordinates for the peak activation voxel are also shown.

Differences within the group between L1 and L2 for each contrast

Region Cluster extent mm3 T X Y Z BA

Letter case versus baselineL1 > L2

No suprathreshold clustersL2 > L1

(1) R. Postcentral G. 12 6.04 33 −25 35 2Lexical decision versus baseline

L1 > L2No suprathreshold clusters

L2 > L1

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(1) L. Cerebellum 10(2) R. Middle Frontal G. 10

(3) R. Middle Frontal G. 21

In the monolingual participants, there were cortical activationsn both the left and right hemispheres for all three tasks (non-erbal, letter case, lexical decision). For both nonverbal and letterase conditions, analyses revealed bilateral activations which wereimited to the parietal and occipital lobes, corresponding to theon/low-level linguistic nature of the task. In contrast, the lexi-al decision task produced robust activations in the left inferiorrontal gyrus (Broca’s area) and also in the left superior tempo-al (Wernicke’s area) and fusiform gyri, supporting the classicalodel of language representation. Although some right hemi-

phere activity was observed in the inferior frontal, fusiform andingual gyri, the majority of the brain activity was lateralised to theeft.

The fMRI results for bilinguals showed a greater spread andmount of overall activation for both Macedonian (L1) and EnglishL2) compared to monolinguals. When using Macedonian, signif-cant bilateral activity was observed in the lingual gyrus and thearietal lobe for the nonverbal task, and in the inferior occipitalnd frontal gyri, as well as in the fusiform gyrus for the letter caseudgment task. Although the lingual and fusiform gyri have consis-ently been associated with word recognition and language, earlier

Please cite this article in press as: Park, H. R. P., et al. Language lateraNeuropsychologia (2012), doi:10.1016/j.neuropsychologia.2012.01.005

vidence has shown that these regions may also be activated inesponse to stimuli that are not word-specific and have roles inon-word processing and object recognition (Price, 2000; Price &evlin, 2003).

ig. 3. Mean frontal and temporal lobe laterality indices (LI) for between-group comparisoersus Baseline; Lexical decision versus Baseline). The monolingual group and the bilinguctivity in the left hemisphere, and negative LIs indicate greater activity in the right hemisrrors are indicated by error bars.

4.16 −24 −28 174.12 48 32 26 464.01 33 53 20 10

The regions of activation seen in the bilinguals for the lexicaldecision task in Macedonian were very similar to the areas foundin the monolingual group, including the left inferior frontal and theoccipito-temporal region (i.e. fusiform gyrus). The neural circuitsfor language in bilinguals and monolinguals are therefore simi-lar when using their native language. Findings clearly show theimportance of the inferior frontal area for lexical decision makingand silent reading of single words. Some right hemispheric activitywas observed in the superior parietal lobule, the inferior occipitalgyrus, the fusiform gyrus and the cerebellum. The right hemisphereactivation, seen in both the bilinguals and monolinguals when util-ising their native languages, supports the idea that complete leftlateralisation of written language is rarely observed.

The bilingual participants showed a more pronounced patternof bilateral activation when performing lexical decision tasks inEnglish compared to when using Macedonian, with significant rightinferior and middle frontal gyri activity (in addition to the typicalleft hemispheric language areas). Interestingly, robust activationswere also observed in the left and right superior parietal lobuleand the left inferior parietal lobule. Although the parietal cortex isnot generally known for linguistic properties, its multimodal and

lisation in late proficient bilinguals: A lexical decision fMRI study.

integrative role in a variety of cognitive tasks could explain theobserved activations. Additional cortical areas might be recruitedas a result of more effortful word-form processing (Culham &Kanwisher, 2001).

ns using three contrasts of interest (Nonverbal versus Baseline; Letter case judgmental group were compared in English (L2 for bilinguals). Positive LIs indicate greater

phere. Significant differences between the groups are marked by asterisks. Standard

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To sum thus far, the cortical regions which were consistentlyctivated when performing linguistic tasks were mostly support-ve of the classical model of language organisation, which includedctivations in the fusiform and lingual gyri and the superior tempo-al and inferior frontal gyri, for both the monolingual and bilingualroups. In addition, predicted activity in the occipital regionsas observed. However, variations in neural activity between the

ilinguals and monolinguals were also detected, and to furtheretermine the precise cortical differences between the two groups,roup analyses and laterality indices were performed.

Surprisingly, between group comparisons revealed that theilinguals showed additional neural activity compared to mono-

inguals for both L1 (Macedonian) and L2 (English). Even thoughther neuroimaging studies have found that bilinguals recruit addi-ional brain regions when using their second language (e.g. Chee,on, Lee, & Soon, 2001), our finding of greater activity in bilinguals

or their native language, when compared to monolinguals, wasnusual. Although it is not possible to determine whether the neu-al differences observed between groups for L1 are the direct resultf bilingual cognitive processes due to the lack of a Macedonianonolingual group, they may otherwise be explained in terms of

anguage plasticity.Evidence for brain plasticity comes from studies such as

echelli et al. (2004), who found increased grey matter densityn the inferior parietal cortex in bilinguals relative to monolin-uals. Perani et al. (2003) have also suggested that the cerebralepresentation of languages in bilinguals may be affected by dif-erential exposure to a given language. Therefore it is possible thathanges may have occurred in L1 processing as a result of acquir-ng English, as the bilingual subjects in the present study wereroficient bilinguals living and working for many years in Newealand. Such intense exposure to their second language may haveesulted in some first language cortical modification. In support,adzakova-Trajkov, Kirk, and Waldie (2008) found greater rightemisphere involvement during a linguistic dual task for both L1nd L2 in late proficient bilinguals living in their L2 environment.he authors suggested that the late acquisition of L2, coupled withntense exposure to that language, may have led to slight changesn cortical representation of language in the bilinguals. Together,hese results support findings from earlier studies which indicatehat bilinguals exert more cortical effort than monolinguals whenrocessing words in L2 (e.g. Hasegawa, Carpenter, & Just, 2002).his may be a neural compensatory mechanism to cope with lessortical efficiency when using L2.

A surprising finding from the fMRI results was the relativeypoactivation of left temporal regions for the English lexical deci-ion task in bilinguals, which is normally dedicated to languagerocessing (Wernicke’s area). This area was found to be active forhe L1 lexical decision task in both the monolingual and bilingualroups, suggesting that the minimum activity observed is partic-lar to L2 only. Dehaene et al. (1997) also found, in their study of

anguage representation in moderately proficient bilinguals, thathen using L2, the participants’ left temporal areas consistently

ailed to engage for word comprehension tasks. It is possible thathis activation failure of a key linguistic region is compensated byther areas of the brain, as indicated by the bilinguals’ accurateerformance (89%). This further suggests that the additional activ-

ty seen in the bilingual brain is not due to separate language areaspecifically dedicated to processing L2, but rather due to greaterortical recruitment as result of computational difficulty.

Such differences in the cortical regions activated for languagerocessing in bilinguals and monolinguals suggest a slightly differ-

Please cite this article in press as: Park, H. R. P., et al. Language lateralNeuropsychologia (2012), doi:10.1016/j.neuropsychologia.2012.01.005

nt pattern of lateralisation between the two groups. The lateralityndex results revealed that, in the frontal lobe, both groups showedtrong left laterality when performing lexical decision tasks in theirative language. In the temporal lobe, monolinguals showed strong

PRESSlogia xxx (2012) xxx– xxx 7

left lateralisation for all three tasks, whereas bilinguals displayed amore bilateral pattern of activity. However, these between-groupdifferences for L1 were not significant. The L2 results indicatedthat, in the frontal lobe, the bilinguals displayed a weaker left lat-eralisation for language compared to monolinguals. The largestdifferences in laterality between monolinguals and bilinguals wereobserved in the temporal lobe. In particular, there was a significantdifference in the degree of lateralisation for the lexical decisiontask, with the bilinguals showing a much smaller left hemisphericdominance compared to monolinguals. This suggests that utilis-ing a second language instigates a greater overall spread of corticalactivation compared to when using the native language.

When the behavioural, fMRI and laterality index results aretaken together, they support the idea that bilinguals employ a sim-ilar linguistic network to that of monolinguals, but show a weakerasymmetry leading to a less marked lateralisation of language. Thiswas found for both their native and second languages. This is incontrast to earlier research showing no differences in the repre-sentations of languages in late proficient bilinguals (e.g. Chee et al.,1999). Although our participants were proficient bilinguals (livingin an English-speaking country), their late age of English acquisi-tion seems to have had a greater impact on language processingthan their very good mastery of English, (e.g. Perani et al., 2003;Wartenburger et al., 2003; Weber-Fox & Neville, 1996).

With regard to English processing and the greater activations weobserved in bilinguals, it is possible that, although proficient bilin-guals use mostly the same neural machinery for both languages,the network is less than perfect at managing both languages. Assuch, the recruitment of right hemisphere activation, mainly in thetemporal and occipital lobes, is necessary. Overall, the results alsosuggest that the activations found in bilinguals did not differ largelyfrom the monolinguals. The participants’ strong English proficiencymay therefore play a strong role here. Although the overall corticalactivation during English tasks was greater than during Macedo-nian, the additional recruitment was not associated with inferiorperformance as the bilinguals performed well (89% correct total)on the lexical decision tasks in English.

In conclusion, the present study found neural differences withinand between groups. This suggests that learning a second languageis a dynamic process which has a significant effect on the cor-tical organisation of language in bilinguals, in terms of amountand extent of activation. However, the key linguistic areas acti-vated when bilinguals utilise L2 are mostly similar to the areasobserved in monolinguals. Bilinguals do engage additional corti-cal areas, which may be associated with language plasticity forL1, and greater cortical effort for L2 processing. The lateralityindex results indicate a weaker pattern of lateralisation for bothlanguages in bilinguals, compared to monolinguals, due to therecruitment of extra regions both in the left and right hemispheres.Finally, even though the bilinguals in the current study werehighly proficient in L2, these differences in cortical activity betweenthe bilinguals and monolinguals suggest that the age of acquisi-tion factor is the main determinant of language representation inbilinguals.

Further research is required to determine if the neural networkfor English compared to Macedonian in the bilinguals is the pre-requisite or the end results of English mastery. In fact, the findingof cortical differences in the native languages of bilinguals andmonolinguals raises another interesting question of the poten-tial extent of plasticity in language-dedicated neural areas, andwhether these areas can be modified through experience whenpresented with more than one language. In addition, the inclusion

isation in late proficient bilinguals: A lexical decision fMRI study.

of a Macedonian monolingual group is necessary to clarify if theneural differences seen in the between group analysis for L1 aremainly due to cognitive processes underlying bilingualism or dueto the specific language used.

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