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Available online at www.sciencedirect.com
Journal homepage: www.elsevier.com/locate/cortex
Note
Language proficiency modulates the engagement of cognitive
control areas in multilinguals
Jubin Abutalebi a,b, Pasquale A. Della Rosa a, Guosheng Ding c, Brendan Weekes b,
Albert Costa d and David W. Green e,*
a
Vita-Salute San Raffaele University and San Raffaele Scientific Institute, Milan, Italy
Division of Speech and Hearing Sciences, University of Hong Kong, Hong Kong
c
State Key Laboratory of Cognitive Neuroscience and Learning, Beijing Normal University, Beijing, China
d
Universitat de Pompeu Fabra & ICREA, Barcelona, Spain
e
Cognitive, Perceptual and Brain Sciences, University College London, United Kingdom
b
article info
abstract
Article history:
Language proficiency should modulate the regions involved in language control in
Received 29 March 2012
predictable ways during language switching. However, prior studies reveal inconsistent
Reviewed 15 June 2012
effects on the regions involved in language monitoring [pre-Supplementary Motor Area/
Revised 3 July 2012
Anterior Cingulate Cortex (pre-SMA/ACC)] and language selection (left caudate) conceivably
Accepted 22 August 2012
because variations in relative proficiency are confounded with other between-group differ-
Action editor Roberto Cubelli
ences. We circumvented this problem in an fMRI (functional Magnetic Resonance Imaging)
Published online 1 September 2012
study of overt picture naming in trilingual participants. In this case, the difference between
a high-proficient and a low-proficient further language can be assessed within subjects
Keywords:
with no between-group confound. We also used a monolingual group to assess the neural
Bilingual
correlates of switching between two categories of response within the same language.
Cognitive control
We report a novel result: relative language proficiency dissociates response of the pre-
Language control
SMA/ACC and left caudate during language switching. Switching between languages
Multilingual
increased pre-SMA/ACC response regardless of proficiency differences. By contrast, left
Language switching
caudate response did vary with proficiency differences. Switching from the most to the
least proficient language increased the response. Within-language switching, as contrasted
with between-language switching, elicited a comparable increase in pre-SMA/ACC
response but a decrease in left caudate response. Taken together, our data support
a wider role of pre-SMA/ACC in task monitoring and establish the critical role of the left
caudate in the selection of the less proficient language in language switching.
ª 2012 Elsevier Ltd. All rights reserved.
1.
Introduction
Language use and cognitive control are intimately related in
bilingual language processing. For successful communication
bilinguals have to control their two languages in order to
select the correct language for use and to avoid unwanted
interference from the language not in use. Bilinguals achieve
this feat by engaging brain areas closely related to cognitive
* Corresponding author. Cognitive, Perceptual and Brain Sciences, University College London, Gower Street, London WC1E 6BT, UK.
E-mail address: [email protected] (D.W. Green).
0010-9452/$ e see front matter ª 2012 Elsevier Ltd. All rights reserved.
http://dx.doi.org/10.1016/j.cortex.2012.08.018
906
c o r t e x 4 9 ( 2 0 1 3 ) 9 0 5 e9 1 1
control such as the pre-Supplementary Motor Area/Anterior
Cingulate Cortex (pre-SMA/ACC), prefrontal cortex and the
left caudate (Abutalebi and Green, 2007). The relative demand
on each region relates to its cognitive function. The pre-SMA/
ACC is important for monitoring the language context, for
detecting conflict and for avoiding errors that may arise
during language selection. Prefrontal regions are implicated in
the top-down control required for selecting the correct
language and eventual error correction (Hernandez, 2009)
whereas the left caudate is more specifically implicated in
selecting the intended language (Crinion et al., 2006). Indeed,
lesions to the left caudate and the prefrontal regions may lead
to errors in language selection such as pathological language
switching in bilinguals (Abutalebi et al., 2000).
The activation of the regions in the language control
network might be expected to vary as a function of language
proficiency. This issue can be addressed in the language
switching paradigm in which participants name pictures in
each of their two languages in an intermixed fashion contingent on a specific cue (see for review, Luk et al., in press). In
this paradigm we would expect that switching into a less
proficient language would increase demand on the left
caudate and so increase its activation. If ACC activation
reflects conflict or error avoidance then it too would show an
increase on switching to the less proficient language. Alternatively if the region monitors language context, activation
would increase on a switch trial but not as a function of
language proficiency. However results to date using this
paradigm present an inconsistent picture. One reason is that
differences in relative language proficiency are confounded by
other between-group differences. In a study with highly
proficient SpanisheCatalan bilingual speakers, Garbin et al.
(2011) reported that switching into the first language (L1) elicited greater activation only in the pre-SMA/ACC complex,
while switching into the second language (L2) engaged the left
caudate. In contrast, in a study with low proficiency ChineseeEnglish bilingual speakers, Wang et al. (2007) recorded no
engagement of the caudate and ACC activation only when
bilinguals switched into the low-proficient L2.
In this study, we aimed to achieve a better characterization
of the response of critical regions in the language control
network during language switching. Instead of using bilinguals, we studied language switching in early multilingual
speakers. With such participants, we can investigate within
subjects how a difference in relative proficiency for the two
further languages alters the response of these regions. We
compared the neural response to switching to a highproficient L2 relative to L1 and the response to switching to
a lower-proficient third language (L3) relative to L1. Moreover,
we also compared neural response to language switching in
our multilinguals with the neural response to a withinlanguage switching task in a group of monolinguals. This
comparison allowed us to explore the selectivity of neural
response to between-language switching.
2.
Materials and methods
Participants in the study comprised 14 healthy right-handed
multilinguals (GermaneItalianeEnglish) and 14 healthy right-
handed Italian speaking monolinguals matched for socioeconomic background, education and age (mean ¼ 23.35 years,
SD ¼ 4.5). All were female with normal or corrected-to-normal
vision. All multilinguals were from South Tyrol. They learned
German from birth as their L1. They attended school from age
six and were taught in German and Italian and so they learned
Italian from age six. All participants also had a reasonable
mastery of English (L3) which they learned at around the age of
eight. We investigated language proficiency with translation
tasks (see Abutalebi et al., 2007). For L1 and L2, subjects translated 81.1% of words correctly from L1 into L2 and 74.2% of words
correctly from L2 to L1. Translation from L1 into L3 and L3 to L1
yielded lower accuracy rates of 64.8% and 69.2%, respectively.
Hence, L2 was classified as a high-proficient and L3 as
a medium-proficient language (see Supplemental material for
demographic data). There was no significant correlation
between AoA (Age of acquisition) and test performance for
translation into L2 (R ¼ .223; p ¼ .444) or into L3 (R ¼ .328;
p ¼ .252).
The investigation was approved by the Ethics Committee
of the University San Raffaele and informed consent was obtained from participants.
2.1.
Task and procedures
Participants (multilinguals and monolinguals) performed an
overt picture-naming task (see Fig. 1A for details) with two
runs for each naming context. For the multilinguals the order
of presenting the two contexts (L1eL2 and L1eL3) was counterbalanced over participants. For all languages, 32 different
pictures (8.5 8.5 cm) were selected from the Snodgrass and
Vanderwart (1980) set. Each picture was repeated three
times for each language across the conditions, totaling 96
stimuli in each of the two contexts for multilinguals and the
single context for monolinguals. Four pre-randomized lists
were created defining the order in which the stimuli appeared.
All stimuli were checked for frequency and syllable length in
each language, based on the norms for each of the languages
(German: Genzel et al., 1995; Italian: Laudanna et al., 1995;
English: Leech et al., 2001). Pictures with cognate names were
excluded.
Each picture was displayed for 2 sec, followed by an ISI
(Inter-Stimulus Interval) of 1880, 3550, or 4950 msec for the
purposes of optimizing statistical power.
Trials could be switch trials or non-switch trials. For the
multilinguals, these were defined by the language required on
the prior trial. It was a switch trial if a picture-to-be-named
was preceded by one named in a different language and
a non-switch trial if a picture-to-be-named was preceded by
one named in the same language. In total there were 48 switch
trials (for each language) and 48 non-switch trials (for each
language) in each experimental context. Switch trials could
occur in an unpredictable manner.
For monolinguals, switch and non-switch trials were
defined by whether the same or a different category of naming
response (noun or verb) was required on the current
compared to the preceding trial. Again there were 48 switch
and 48 non-switch trials. Our analysis concerned trials on
which pictures were named with a noun (noun naming trials)
to match the response of multilingual speakers in their L1.
c o r t e x 4 9 ( 2 0 1 3 ) 9 0 5 e9 1 1
907
Fig. 1 e In (A), the experimental paradigm employed in our study. Multilinguals had to name pictures respectively in an
L1eL2 and L1eL3 switching condition. In each condition, the color of the image-to-be-named indicated the language. In the
L1eL2 context, green pictures indicated naming in German and blue pictures in Italian. In the L1-L3 context, green indicated
naming in German and red in English. In order to have a comparable condition, monolinguals were asked to generate
a noun when the color of the picture was red and a verb for green pictures. In (B), the pattern of brain activity related to the
differences between switching contrasts versus non-switch contrast images at the first level for both multilinguals and
monolinguals and the respective box plot calculated in the left caudate cluster (M [ monolinguals). In (C), the pattern of
brain activity related to the average positive effects of all switching versus non-switch contrast and relatively, the box plots
as calculated at the pre-SMA/ACC cluster.
Technical constraints precluded the recording of voice onset
times in either group.
Prior to scanning all participants were trained using
a different set of pictures.
2.2.
Scanning, image processing and preprocessing
The fMRI-event-related technique was used (3T Intera Philips
body scanner, Philips Medical Systems, Best, NL, eight channelssense head coil, sense reduction factor ¼ 2, TE ¼ 30 msec,
TR ¼ 2400 msec, FOV ¼ 240 240, matrix size ¼ 128 128, 30
contiguous axial slices per volume, 210 volumes per each run,
slice thickness ¼ 4 mm). Each run was preceded by 10 dummy
scans that were discarded prior to data analysis of correct noun
naming trials (i.e., trials on which pictures were named with
a noun). Multilinguals only completed such trials whereas they
were a subset of trials for the monolinguals.
A high resolution structural MRI (Magnetic Resonance
Imaging) was acquired for each participant (MPRAGE, 150
slice T1-weighted image, TR ¼ 8.03 msec, TE ¼ 4.1 msec; flip
angle ¼ 8 , TA ¼ 4.8 min, resolution ¼ 1 1 1 mm) in the
axial plane.
SPM (Statistical Parametric Mapping) running on Matlab 6.5
was used for all preprocessing steps and statistical analysis.
Slice-timing correction was carried out by interpolating the
voxel time series using sinc interpolation and resampling with
the middle (fifteenth) slice in time as a reference point.
Functional volumes were realigned with the first one in the
time series to correct for between-scan motion. The structural
T1-weighted volume was segmented to extract a gray matter
image for each subject, which was spatially normalized to a
gray matter image of the MNI (Montreal Neurological Institute)
template (MNI; http://www.bic.mni.mcgill.ca/ServicesAtlases/
ICBM152NLin2009). After normalization, all volumes were
resampled in 2 2 4 mm voxels using sinc interpolation in
space. Finally, the T2*-weighted volumes were smoothed
using a Gaussian kernel with 8 mm full-width at halfmaximum (FWHM).
2.3.
Statistical analysis
A General Linear Model (GLM) analysis was performed at the
first single subject level specifying eight regressors for
multilinguals coding switch and non-switch trials, and four
regressors for monolinguals coding for switch and nonswitch trials. Five contrasts of interest (four for multilinguals and one for monolinguals) were then assessed at the
second level.
908
c o r t e x 4 9 ( 2 0 1 3 ) 9 0 5 e9 1 1
For multilinguals (noun naming in different language
contexts)
- switching
context;
- switching
context;
- switching
context;
- switching
context;
into L1 versus L1 non-switch trials in L1eL2
into L2 versus L2 non-switch trials in L1eL2
into L1 versus L1 non-switch trials in L1eL3
into L3 versus L3 non-switch trials in L1eL3
For monolinguals (noun naming in a nouneverb context)
- switching to noun naming versus. non-switch noun naming
trials. Switching to noun naming matches the response
required for L1 naming on switch trials in the multilingual
participants.
At the second level, a one-way ANOVA model was implemented in SPM5 and two contrast maps were computed:
(1) An F-contrast (increases and decreases of activation) coding
the differences among the five contrasts above (switching
vs non-switch contrasts) with a threshold of p ¼ .019 FDR
(False Discovery Rate) corrected at the voxel level.
(2) A T-contrast calculating the average positive effect of the
five contrasts above (resulting in areas in which an
increase of activation was detected for all conditions) with
a threshold of p ¼ .029 Family Wise Error (FWE) corrected at
the cluster level.
Effects of interests for each of the five contrasts were then
plotted for the activation cluster of the left caudate (x ¼ 6,
y ¼ 16, z ¼ 4) highlighted in contrast one; and for the pre-SMA/
ACC cluster of activation (x ¼ 4, y ¼ 2, z ¼ 56) resulting from
contrast two. In order to compute the significance of the
effects plotted at the second level, beta values were extracted
for each condition included in the second level one-way
ANOVA (Analysis of Variance) at the left caudate (x ¼ 6,
y ¼ 16, z ¼ 4) and at the pre-SMA/ACC (x ¼ 4, y ¼ 2, z ¼ 56) at
the single subject level. Two one-way ANOVA analyses, one
for the left caudate and one for the pre-SMA/ACC, were
computed on the extracted beta values for each of the five
switching conditions. Post-hoc comparisons using Tukey
(HSD, honestly significant difference) post-hoc tests were then
computed to assess significant differences between the five
switching conditions.
3.
Results
The mean total error percentage for naming in multilinguals
was 1.04% (SD ¼ 1.03) for L1, 4.86% (SD ¼ 2.62) for L2 and
27.08% (SD ¼ 3.65) for L3, confirming that L3 was the less
proficient language. The mean total error percentage for noun
naming (i.e., naming a picture with a noun rather than a verb)
in the monolingual group was 5.21% (SD ¼ 1.38). There was no
significant relation between AoA and in-scanner naming
accuracy (R ¼ .158; p ¼ .590 between L2 AoA and L2 accuracy;
and R ¼ .072; p ¼ .806 between L3 AoA and L3 accuracy).
However, picture naming in L1 elicited significantly more
errors in the monolinguals than in the trilinguals (p ¼ .003,
T-test) and we consider the implications in the discussion.
Turning to the functional neuroimaging results, the four
switching contrasts in multilinguals are reported in Fig. 2, in
order to illustrate the areas involved in language control such
as the caudate and the pre-SMA/ACC complex. The pre-SMA/
ACC complex was engaged by all four switching conditions in
multilinguals whereas the left caudate was more engaged
specifically when multilinguals had to switch into L3 (i.e., red
color in Fig. 2).
The main effect of all differences among the switching
contrasts resulted in extensive bilateral caudate activity and
two smaller foci in the thalamus. No difference was found in
the left prefrontal cortex and the ACC (see Fig. 1B). The
average positive effects of all switch contrasts engaged only
the pre-SMA/ACC area (see Fig. 1C). As to the plots of the left
caudate cluster (i.e., significant differences between the
various switching conditions, see Table 1 for beta values), it is
important to underline that switching to noun naming in
monolinguals differed significantly in the left caudate when
compared to the switching conditions in multilinguals (see
Table 1 for p-values). It showed decreased response. In
multilinguals, caudate activity increased with switching into
L2 compared to switching into L1 in the L1eL2 context.
Caudate activity increased further when switching into L3
compared to switching into L1 in the L1eL3 context. As reported in Table 1, our HSD Tukey tests reported for this latter
comparison a trend of significance (p ¼ .056).
The plots of the pre-SMA/ACC cluster (calculated as the
area of average positive effect of all switching contrasts),
revealed a different pattern (see Table 1 for the beta values).
Switching between languages in both contexts in multilinguals and switching into noun naming in monolinguals activated the pre-SMA/ACC to the same degree.
4.
Discussion
Our study aimed to resolve inconsistent results in the literature on the neural response to language switching. A key
determinant of response is likely to be differences in language
proficiency but to establish this requires control of other
individual differences. Such control is difficult when differences in relative language proficiency are tested in betweengroup studies. We circumvented the problem by studying
language switching in trilingual speakers for whom their
second and third languages differed in proficiency. We
establish that relative language proficiency is a key factor
affecting regional neural response during language switching.
More specifically, we were able to dissociate responses in two
dominant regions of the language control network: the left
caudate and the pre-SMA/ACC. Left caudate response varied
with proficiency differences but the pre-SMA/ACC did not. The
left caudate showed the greatest increase for switching from
the most (L1) to the least proficient language (L3). Such an
outcome is consistent with the left caudate’s role in selecting
the name in the required language in the face of interference
from the alternative language. Its relative deactivation when
909
c o r t e x 4 9 ( 2 0 1 3 ) 9 0 5 e9 1 1
Fig. 2 e Brain activity patterns for the four different switching conditions in multilinguals (p < .001 uncorrected at the voxel
level with a cluster extent of k [ 10) superimposed on the brain template. The 2nd level T-maps are overlaid and rendered
on the mean structural image of the study sample with MRIcron (http://www.sph.sc.edu/comd/rorden/mricron/). The yellow
color indicates switching into L1 (L1eL2 context), dark blue indicates switching into L2 (L1eL2 context), green indicates
switching into L1 (L1eL3 context), and red indicates switching into L3 (L1eL3 context). Color mixtures indicate that brain
regions were engaged by more than one switching condition.
monolingual speakers switched to naming the picture e
a more familiar type of response e rather than generating
a verb in response to it, indicates a broader role in the resolution of response conflict (Ali et al., 2010). By contrast,
switching between languages increased pre-SMA/ACC
response regardless of differences in relative proficiency.
Such an outcome is consistent with the view that the preSMA/ACC monitors the language context for bilingual or
Table 1 e Beta values for each contrast extracted at left caudate [L6 16 4] and pre-SMA/ACC [L4 2 56] at the single subject
level. Reported p values are from HSD Tukey tests. The numbers (1e5) in the second column characterize the switching
contrast to which the contrast of the first column was compared [1 [ switching into L1 (L1eL2 context); 2 [ switching into
L2 (L1eL2 context); 3 [ switching into L1 (L1eL3 context); 4 [ switching into L3 (L1eL3 context); 5 [ switching into nouns
(monolinguals)]. (*) [ Significant difference, (^) [ trend of significance.
Left caudate e cluster at
x ¼ 6, y ¼ 16, z ¼ 4
Mean differences
1. Switching into L1 (L1-L2 context)
2. Switching into L2 (L1-L2 context)
3. Switching into L1 (L1-L3 context)
4. Switching into L3 (L1-L3 context)
5. Monolinguals (switching into nouns)
2
3
4
5
1
3
4
5
1
2
4
5
1
2
3
5
1
2
3
4
.1892088
.2415788
.5109324
.9957076
.1892088
.4307876
.3217235
1.1849164
.2415788
.4307876
.7525112
.7541288
.5109324
.3217235
.7525112
1.5066399
.9957076
1.1849164
.7541288
1.5066399
(*)
(*)
(^)
(^)
(^)
(*)
(*)
(*)
(^)
(*)
pre-SMA/ACC e cluster at
x ¼ 4, y ¼ 2, z ¼ 56
p-Value
Mean differences
p-Value
.958
.903
.344
.008
.958
.519
.765
.001
.903
.519
.056
.077
.344
.765
.056
.000
.008
.001
.077
.000
.1790382
.0888992
.1819147
.1688550
.1790382
.0901390
.3609529
.0101832
.0888992
.0901390
.2708139
.0799558
. 1819147
.3609529
.2708139
.3507697
.1688550
.0101832
.0799558
.3507697
.954
.997
.951
.969
.954
.996
.610
1
.997
.996
.820
.998
.951
.610
.820
.679
.969
1
.998
.679
910
c o r t e x 4 9 ( 2 0 1 3 ) 9 0 5 e9 1 1
multilingual speakers as part of a more general role in task
monitoring.
Conceivably, response of the pre-SMA/ACC and the
caudate reflect general task difficulty or, more specifically,
differences in the ease of switching between languages in the
same or in a different language family. We can reject both
alternative accounts of the data. If task difficulty was
explanatory, response in pre-SMA/ACC in monolinguals (who
showed increased error in picture naming) would be greater
than that shown by trilingual speakers in their L1 and less
than that revealed by these speakers naming in their L3
(English). In fact as indicated in Table 1 there was no difference. Similarly we should predict increased response in the
left caudate in comparison with naming in L1 in trilingual
speakers. But the data showed the opposite effect. Increased
caudate response when switching into English (L3) from
German (L1) relative to switching into Italian (L2) from
German (L1) might alternatively reflect a greater difficulty of
switching within a language family (German and English are
both non-Romance languages) than between language families (Italian is a Romance language). If so, the converse should
hold: switching into German (L1) should be more difficult
when switching from English (L3) than from Italian (L2).
Inspection of Table 1 indicates that switching into L1 in an L3
context does not increase activation more than switching into
L1 in an L2 context either for the left caudate or for the preSMA/ACC. On the bases of these data then we have no
reason to believe that language family makes a difference to
the neural response to switching but it is possible that more
extreme differences (e.g., between European and nonEuropean languages) may do so.
Our results underline the importance of cognitive control
to language use in bilingual and trilingual speakers but the
brain regions activated are not special to bilinguals. We
presumed their use in monolingual speakers as they switched
between noun and verb naming and would expect their
recruitment when multilingual speakers perform the same
task within each of their languages. The importance of our
data is that they show for the first time that differences in
language proficiency, defined within participants, differentially modulate activity in core regions of the language control
network during language switching. Switching language
increases demand on a region associated with monitoring the
language in use (pre-SMA/ACC) and switching to the least
proficient language increases demand in the region implicated in selecting the language in use (left caudate). Such
demands change with proficiency and are likely to underlie
the adaptive response to gray matter in these regions
(Abutalebi et al., 2012; Zou et al., 2012). The prefrontal cortex
revealed no differential effect of language switching
conceivably because it plays a role in the sustained inhibition
of a language not in use. It would then not be engaged in
a context where one or more languages are required as in the
present study but would be engaged where a single language
was required consistent with recent findings (Parker-Jones
et al., 2012; Guo et al., 2011).
In summary, by examining differences in relative language
proficiency within trilingual speakers we were able to dissociate responses of two core regions of the language control
network during language switching. The pre-SMA/ACC region
responded comparably to both between-and within-language
switches and, within our trilingual speakers, was less sensitive to the effects of proficiency. By contrast, response of the
left caudate increased markedly with a switch from the most
to the least proficient language. Further work is needed to
characterize neural responses to language switching in
trilingual speakers for whom the less proficient language is
a member of a distinct language family.
Supplementary data
Supplementary data related to this article can be found at
http://dx.doi.org/10.1016/j.cortex.2012.08.018.
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