r Human Brain Mapping 30:3625–3635 (2009) r

Greater Leftward Lateralization of the Inferior
Frontal Gyrus in Second Language Learners with
Higher Syntactic Abilities
Arihito Nauchi,1,2 and Kuniyoshi L. Sakai1,2*
1

Department of Basic Science, Graduate School of Arts and Sciences, The University of Tokyo,
Komaba, Tokyo, Japan
2
CREST, Japan Science and Technology Agency, Kawaguchi-shi, Japanrr

Abstract: There is a great individual variability for acquiring syntactic knowledge in a second language(L2). Little is, however, known if there is any anatomical basis in the brain for individual differencesin syntactic acquisition. Here we examined brain structures in 95 nonnative speakers of English,
including 78 high-school students and 17 adult international students. We found a signiﬁcant correlation between the performance of a syntactic task and leftward lateralization of a single region in thetriangular part (F3t) of the inferior frontal gyrus, which has been proposed as the grammar center.
Moreover, this correlation was independent of the performance of a spelling task, age, gender, andhandedness. This striking result suggests that the neural basis for syntactic abilities in L2 is independent of that for lexical knowledge in L2, further indicating that the individual differences in syntactic acquisition are related to the lateralization of the grammar center. Hum Brain Mapp 30:3625–3635,
2009. VC 2009 Wiley-Liss, Inc.
Key words: brain anatomy; lateralization; frontal cortex; human; language acquisition; syntaxrr

INTRODUCTION
Why does the ability to master a L2 differ considerably
among individuals, while anyone can master a ﬁrst language (L1)? Recent functional imaging results have shownthat both L1 and L2 are processed in the same corticalContract grant sponsor: Ministry of Education, Culture, Sports,
Science, and Technology of Japan; Contract grant numbers:
17022013, 2022005; Contract grant sponsor: Japan Science andTechnology Agency (JST).
*Correspondence to: Kuniyoshi L. Sakai, Department of Basic Science, Graduate School of Arts and Sciences, The University of Tokyo, Komaba, 3-8-1 Komaba, Meguro-ku, Tokyo 153-8902, Japan.
E-mail: sakai@mind.c.u-tokyo.ac.jp
Received for publication 27 December 2008; Revised 24 February
2009; Accepted 26 February 2009
DOI: 10.1002/hbm.20790
Published online 27 April 2009 in Wiley InterScience (www.
interscience.wiley.com).
C 2009 Wiley-Liss, Inc.
V

regions [Perani and Abutalebi, 2005; Sakai, 2005], indicating that the L2 acquisition mechanisms may be partly
shared with L1 acquisition mechanisms. Voxel-based morphometry (VBM) studies have reported that the relativegray matter (GM) density of the inferior parietal cortex or
the bilateral posterior supramarginal gyri was correlatedwith individual vocabulary scores [Lee et al., 2007; Mechelli
et al., 2004]. However, the previous anatomical studies haveexamined the linguistic proﬁciency only at the word level.
Functional imaging studies have also clariﬁed the distinct
activation patterns for lexico-semantics in left parieto-temporal regions and those for syntax in left frontal regions[Price, 2000; Sakai, 2005], suggesting differential neural correlates for acquiring lexical and syntactic knowledge. There
are a large number of functional studies that have attempted
to localize brain regions engaged in syntactic processing,although the interpretation of these studies varies [Caplan,2001]. For instance, the anterior portion of the superior temporal gyrus and the left angular gyrus, as well as the inferior
frontal gyrus (IFG), have been implicated as being engagedr Nauchi and Sakai r

TABLE I. Demographic details of each group

N
Age
Range
Mean  SD
AOE
Range
Mean  SD
DOE
Range
Mean  SD
LQ
Range
Mean  SD

High-school students

Adult students

78 (43 females)

17 (9 females)

14–18
15  1.4

20–41
28  5.6

12–13
13  0.3

6–19
11  4.0

1.7–4.7
2.6  1.4

6–28
17  6.7

29–10081  16

60–10087  14

whether there is also an anatomical basis for individual
differences in the acquisition of syntactic knowledge, probably involving the left IFG such as F3t and F3O.
In this study, we used the same English stimuli andtasks of Syn and Spe. We acquired high-resolution MR
images from 95 nonnative speakers of English in two
groups: Japanese high-school students and adult international students. The latter group was added to exclude thepossibility that the results were dependent on particularage or L1 backgrounds (Tables I and II). To examine any
difference between these two groups is not, however,within the scope of this study. By examining the performance of the linguistic tasks, as well as all possible factors
including age, gender, and handedness throughout bothgroups, truly biologically relevant individual variability on
syntactic abilities will be elucidated in the brain.

N, number of participants; AOE, age of ﬁrst exposure to English;
DOE, duration of exposure to English; LQ, laterality quotient ofhandedness.

in syntactic processes during sentence comprehension[Caplan et al., 2001; Friederici et al., 2003; Meyer et al., 2000].
Given this uncertainty about the regional speciﬁcity, thedata from VBM studies are expected to shed new light on
the critical roles of these cortical regions in syntactic processes. Therefore, we employed the VBM technique to clarify
which regions are actually related to the individual differences of syntactic abilities in L2.
In our recent functional magnetic resonance imaging(fMRI) study for L2 learners, who were in two groups
with different age of ﬁrst exposure (AOE) to English(mean: 12.6 and 5.6 years for late and early learners, respectively), we examined the cortical activations involved inprocessing English sentences containing either syntactic orspelling errors, where the testing ages and task performances of both groups were matched [Sakai et al., in press].
Two forced-choice error-detection tasks were contrasted
using the same set of English sentences: a syntactic (Syn)task and a spelling (Spe) task. The Syn task directly tested
the correct use of English verbs in sentences [Levin, 1993],
whereas the Spe task served as a control not only for theword-level knowledge and the reading abilities, but forthe overall developmental and educational differences(e.g., experiences and exposures in L2). We found distinct
activation patterns in two regions of the left IFG that correlated differentially with the performances of the late andearly learners. Speciﬁcally, activations of the triangularpart (F3t, Brodmann’s area (BA) 45) of the left IFG correlated positively with the accuracy of the Syn task for thelate learners, while activations of the left ventral F3t correlated negatively with the accuracy for the early learners. In
contrast, activations of the orbital part (F3O, BA 47) of theleft IFG correlated positively with the reaction times (RTs)of the Syn task for the late learners, whereas those activations correlated negatively with the RTs for the early learners. These results provide a functional basis for individual
differences in L2 acquisition. The next goal is to examiner

MATERIALS AND METHODS
Participants
We recruited 95 healthy nonnative English speakers in
two groups. The high-school students (N ¼ 78) were
native speakers of Japanese, who had passed an entrance
examination at the age of 12, and they were in the second
or ﬁfth academic years. They had studied English as L2
only in Japan and the age at which they had begun studying English was 13 years; they had never studied a third
language (L3). The adult international students (N ¼ 17)
had L1 backgrounds other than English (e.g., Bulgarian,
Chinese, Croatian, Indonesian, Lithuanian, Mongolia, Persian, Philippine (Cebuano and Tagalog), and Turkish), andthey had studied English as L2 in their non-English speaking countries at least until 15 years old. They also varied
TABLE II. Participants’ behavioral data for each group
Task
Syn
Accuracy (%)
Range
Mean  SD
RTs (ms)
Range
Mean  SD
Spe
Accuracy (%)
Range
Mean  SD
RTs (ms)
Range
Mean  SD

High-school students

Adult students

41–90
59  1160–91
77  122,832–5,804
4,651  578

3,809–5,557
4,496  515

48–98
77  1375–98
90  7.1

2,875–5,716
4,371  604

3,614–5,100
4,273  534

Only trials with correct responses were used for reaction times(RTs). The accuracy of Syn for the high-school students was signiﬁcantly higher than the chance level at 50 % (t(77) ¼ 7.7, P <0.0001).

3626 rr Brain Lateralization and Syntactic Abilities r

in their skills of the Japanese language as L3. All participants of these two groups were right-handed and their laterality quotients of handedness (LQs) were above 20
according to the Edinburgh inventory [Oldﬁeld, 1971].
Informed consent was obtained from all participants, aswell as from the parents/guardians of the high-school students, and the study was approved by the Secondary Education School attached to the Faculty of Education of the
University of Tokyo and by the review board of The University of Tokyo, Komaba.

Stimuli and Tasks
We selected 42 high-frequency English verbs (20 transitive and 22 intransitive, including 12 unergatives and 10
unaccusatives [Yusa, 2003]), and made 100 sets of sentence
stimuli using these verbs, as listed previously [Sakai et al.,in press]. Each set consisted of a key sentence and its associated sentence, which was either syntactically normal or
anomalous. The syntactic errors used in the Syn task werebasically related to argument structures of English verbs.
For instance, as in the example of ‘‘Do you often meet
Mary? - Yes, I often meet.’’, L2 learners tend to make a mistake of omitting an object. This is because objects of transitive verbs can be omitted quite freely in many languages
other than English [Cole, 1987; Park, 2004]. Similarly, thenull-subject (pro-drop) is allowed in Japanese, as well asin Spanish and Italian [Hyams, 1989], and Spanish speakers often accept English sentences without overt subjects[White, 1985]. Even if these aspects of English grammar
are normally taught at school, such syntactic knowledge ishard to acquire for the students. Because the present paradigm explicitly requires judgment on the grammaticalityof sentences, the acquisition of argument structures andtheir associated syntactic knowledge will be properly
assessed. In the Spe task, on the other hand, a typographical error was included in each set for half of the same sets,
to test the English orthography of words.
All behavioral data were acquired outside the MR scanner. At the initiation of every trial of 7 s, a cue, indicating
whether the task was Syn or Spe, was shown for 400 ms,
followed by a set of two English sentences for 6,400 ms.
The participants were instructed to read the two sentencessilently from ﬁrst to last before responding, and they indicated whether or not the sentences contained an error bypushing one of two buttons. In a single session, there were
two Syn and two Spe task blocks (ﬁve trials each), and eachsession was repeated ﬁve times. The order of these two task
blocks was counterbalanced across each participant. In calculating the accuracy of each task, we included trials withno responses as incorrect ones, and excluded trials withpremature responses (button press within 2 s); no further
adjustment for correct or incorrect responses was made.
The high-school students received 10 brief training sessions from their English teachers as a part of the normal
lessons, in which the correct usage of English verbs wastaught with the 100 sets. During the training, each set con-rsisted of a key sentence followed by its associated two sentences, one of which contained a syntactic error in somecases. The students ﬁrst tried to guess their grammaticality, and a teacher then provided them with the correct
answers and a brief explanation. After the training sessions, 100 new sets of sentences with the same English
verbs were used for the Syn and Spe tasks to ensure
whether they had actually acquired the knowledge of syntactic structures, rather than merely memorizing the sentence examples used for the training. The accuracy of Syn
improved signiﬁcantly after the training (paired-t test:
t(77) ¼ 7.7, P < 0.0001), and we used these data (Table II)
for the present analyses, together with the MRI data alsoacquired after the training.

MR Image Acquisition and Analyses
Using a 1.5-Tesla MRI system (STRATIS II, Premium;Hitachi Medical Corporation, Tokyo, Japan), high-resolution T1-weighted images of the whole brain (160 axial slices; 1.0  1.0  1.0 mm3) were acquired with a radio
frequency spoiled steady-state acquisition with a rewoundgradient echo (RF-Spoiled SARGE) sequence (repetitiontime, 30 ms; echo time, 8.0 ms; ﬂip angle, 60 ). MR images
were ﬁrst skull-stripped with a Brain Extraction Tool (BET)[Smith, 2002] in MRIcro software [Rorden and Brett, 2000](http://www.sph.sc.edu/comd/rorden/ mricro.html), andthe data were further analyzed with SPM5 software [Friston et al., 1995] (http://www.ﬁl.ion.ucl.ac.uk/spm). A
symmetrical GM template was made by averaging GM
maps of the standard brain and its mirrored image [Luders
et al., 2004]. The VBM preprocessing [Ashburner and Friston, 2005] (http://dbm.neuro.uni-jena.de/vbm/) combined
bias correction, spatial normalization with the symmetrical
template, and segmentation with a hidden Markov random
ﬁeld model [Cuadra et al., 2005]. The results presented
below were replicated also with a conventional asymmetrictemplate, but the symmetric template is more appropriate
to use in the present study for comparing the corresponding regions in the left and right hemispheres.
To evaluate the absolute volume of GM, the segmented
GM images were further modulated by multiplying thevoxel values by the relative voxel volumes (i.e., the Jacobian determinants of the deformation ﬁeld derived fromspatial normalization) [Ashburner and Friston, 2000]. The
modulated GM images were then smoothed with an isotropic Gaussian kernel of 12 mm at full-width half-maximum (FWHM) [Lee et al., 2007]. To avoid possible edge
effects (partial volume effects) around the border of theGM, voxels with a value greater than 0.05 (maximum, 1.0)
were used for analyzing the modulated GM images. Using
the same procedures, we also examined volumes of thewhite matter (WM) across the whole brain. For the anatomical identiﬁcation of cortical regions, we used the automated anatomical labeling (AAL) method [TzourioMazoyer et al., 2002] on SPM5.

3627 rr Nauchi and Sakai r

Figure 1.
The overall lateralization of cortical regions (N ¼ 95). Cortical used as an inclusive mask. The cross hairs denote the position
regions with the signiﬁcantly positive regional asymmetry index of the anterior commissure (x ¼ y ¼ 0). Note that both lateral(AI) are shown (from red to yellow) on the axial slices (z coor- and medial frontal regions show rightward lateralization,
dinates are denoted) of the symmetrical standard brain, which whereas the deeper frontal structures show leftward
was normalized to the symmetrical template (L, left). The sym- lateralization.
metrical gray matter (GM) template (GM value > 0.05) was also
The voxel-based asymmetry of the regional GM was estimated by calculating the asymmetry index (AI) for a pairof original and mirrored GM images:
AI ¼ 2  (original GM – mirrored GM)/(original GM þ
mirrored GM)
The modulated GM images were used for this calculation, and the resultant AI images were then smoothedwith a 12-mm FWHM kernel [Luders et al., 2004]. The positive AI in the left and right hemispheres correspond to
leftward and rightward lateralization, respectively.

standardized AI at this locus and the standardized valueof this factor to conﬁrm the selective and reliable correlation. To fully characterize the lateralization of this locus,
we need to clarify whether this correlation emerges
because of the regional GM in one hemisphere, thereby
employing both multiple regression and partial correlation
analyses. We will then proceed to the separate analyses ofeach group using the same procedures, followed by theexamination for any effects of age.

RESULTSThe Overall Lateralization of Cortical Regions

Here we set out our main line of analyses by explaining
the motivation of each analysis and the method used tocarry it out. First, we characterize the AI in the wholebrain to show the overall left or right lateralization of cortical regions. We then present the results of the AI analyses
for all participants, employing a multiple regression analysis to examine the effects of ﬁve standardized factors on
the AI: the accuracy of Syn, the accuracy of Spe, age, gender, and LQ (Fig. 2B). In this analysis, no particular correlation between the AI and the global volume is expected.
If any locus shows a signiﬁcant correlation with one factor,
we further perform a partial correlation analysis with the

Figure 1 shows the overall lateralization of corticalregions with the signiﬁcantly positive AI (P < 0.05, false
discovery rate (FDR) corrected for multiple comparisons).
It is notable that both lateral and medial frontal regions, aswell as the superior and middle temporal regions, showed
rightward lateralization. In contrast, leftward lateralization
was observed in the deeper frontal structures including
IFG and the insula, as well as lateral and medial occipitalregions. The AAL method indicated that the regions withleftward lateralization included most of putamen, thalamus, and the Heschle gyrus as well. The general patternof volume differences between left and right hemispheresr3628 rr Brain Lateralization and Syntactic Abilities r

are consistent with previous reports [Luders et al., 2004;
Toga and Thompson, 2003].

The Structural Basis for Individual Syntactic
Abilities in L2
According to a multiple regression analysis on the AI,
we found a signiﬁcant correlation between the accuracy of
Syn and the AI in a focal region of the left F3t (x ¼ 32,
y ¼ 31, z ¼ 12; 554 voxels; Z-score ¼ 5.0; P ¼ 0.013, FDR
corrected), which was one and only region in the wholebrain (Fig. 2A). At this locus, the AI was signiﬁcantly positive, ranging from 0.23 to 0.41 (mean  SEM: 0.067 
0.012; t ¼ 5.7, P < 0.0001). Remarkably, this region is justmedial to the functionally critical region of the Syn task(three loci: x ¼ 42, y ¼ 27, z ¼ 0; x ¼ 57, y ¼ 24, z ¼
15; x ¼ 51, y ¼ 27, z ¼ 24) indicated by our fMRI study
using the same paradigm [Sakai et al., in press]. At thelocus of the left F3t in this study, the regression coefﬁcients of the AI were signiﬁcant for the accuracy of Syn(0.077  0.014, P < 0.0001) and age (0.031  0.013, P ¼
0.016) only (other coefﬁcients, P > 0.28) (Fig. 2C). It isstriking to note that the accuracy of Syn is one and only
factor with a signiﬁcantly positive correlation. The selective contribution of syntactic abilities is thus clear fromthis signiﬁcant interaction between the AI in the left F3t
and the ﬁve factors, because the AI can be predicted by
the accuracy of Syn alone, independently of the accuracyof Spe, gender, and LQ. Indeed, there was no signiﬁcantcorrelation (i.e., neither positive nor negative correlation)
between the accuracy of Spe and the AI in the whole brain(corrected P > 0.05).
By using the standardized AI at this locus of the left F3t,
we also performed a partial correlation analysis with thestandardized accuracy of Syn, after the effects of all otherfactors had been removed from each of these two parameters. The standardized AI was signiﬁcantly correlated withthe standardized accuracy of Syn (r ¼ 0.50, P < 0.0001)(Fig. 2D). In contrast, the standardized AI was not correlated with the standardized accuracy of Spe at all (r ¼
0.008, P ¼ 0.9) (Fig. 2E), even when both parameters
were standardized in the same manner as the case of Syn.
These results clearly demonstrate that the leftward lateralization of the F3t is speciﬁc and critical for the performanceof the Syn task.
To fully characterize the leftward lateralization of theF3t, which correlated signiﬁcantly with the accuracy ofSyn, we need to show whether this correlation emerges
because of a relatively larger volume of the regional GM
in the left hemisphere and/or a smaller volume of the regional GM in the right hemisphere. We thus employed amultiple regression analysis to examine the effects of six
standardized factors on the regional GM: the accuracy ofSyn, the accuracy of Spe, age, gender, LQ, and the total
GM. In this analysis, the positive correlation between theregional GM and the total GM is expected. We found ar

signiﬁcant correlation between the accuracy of Syn and theregional GM in the left F3t (x ¼ 35, y ¼ 27, z ¼ 11; Zscore ¼ 3.0; P ¼ 0.039, FDR corrected) when a small volume correction (SVC) (5.5-mm radius sphere at x ¼ 32,
y ¼ 31, z ¼ 12) was applied. At the locus of the left F3t(x ¼ 32, y ¼ 31, z ¼ 12), the regression coefﬁcients of theregional GM were signiﬁcant for the accuracy of Syn(0.012  0.005, P ¼ 0.011) and the total GM (0.025  0.004,
P < 0.0001) (Fig. 3A). Moreover, the standardized regional
GM in the left F3t was signiﬁcantly correlated with thestandardized accuracy of Syn (r ¼ 0.23, P ¼ 0.023) (Fig.
3B). In contrast, at the locus of the right F3t (x ¼ 32, y ¼
31, z ¼ 12), the regression coefﬁcients of the regional GM
were signiﬁcant for the total GM (0.026  0.005, P <0.0001), but not for the accuracy of Syn (0.008 0.005,
P ¼ 0.10) (Fig. 3C). The standardized regional GM in theright F3t was not signiﬁcantly correlated with the standardized accuracy of Syn (r ¼ 0.18, P ¼ 0.080). These results
suggest that the larger volume of the left regional GM contributes more to the selective correlation between syntactic
abilities and the AI in the left F3t. Regarding the regional
WM, there was no signiﬁcant correlation with the accuracyof Syn or Spe (corrected P > 0.05).

The Structural Basis for Individual Syntactic
Abilities in L2 for the High-School Students
Next we examined the data from the high-school students alone (N ¼ 78) to exclude the possibility that theobserved effects were due to the inclusion of the adultinternational students, who widely varied in age, durationof exposure (DOE) to English, L1 background, and skillsof the Japanese language. Note, however, that for the adultgroup (N ¼ 17) none of the regression coefﬁcients of the
AI in the left F3t (x ¼ 32, y ¼ 31, z ¼ 12) were signiﬁcant(P > 0.3). The absence of signiﬁcance for this group would
be due to the smaller sample size, as well as the narrower
range of the accuracy of Syn (Table II). Using exactly thesame procedures of analyses described above, we further
checked whether all of the main ﬁndings were robust andexactly replicated even for the high-school students alone,
who were relatively homogeneous individuals withrespect to age, AOE, DOE, and L1 background (Table I).
According to a multiple regression analysis to examine
the effects of the same ﬁve standardized factors on the AI,
we found a signiﬁcant correlation between the accuracy of
Syn and the AI in a focal region of the left F3t (x ¼ 33,
y ¼ 32, z ¼ 11; 579 voxels; Z-score ¼ 5.1; P ¼ 0.009, FDR
corrected), which was one and only region in the wholebrain. At this locus of the left F3t, the AI was signiﬁcantly
positive, ranging from 0.26 to 0.27 (0.063  0.012; t ¼ 5.1,
P < 0.0001), and the regression coefﬁcients of the AI weresigniﬁcant for the accuracy of Syn (0.069  0.012, P <0.0001) alone (other coefﬁcients, P > 0.17) (Fig. 4A). There
was no signiﬁcant correlation between the accuracy of Speand the AI in the whole brain (corrected P > 0.05).

3629 rFigure 2.
The structural basis for individual syntactic abilities in L2 (N ¼ (B) Design matrix used for a multiple regression analysis. The
95). (A) The left F3t with a signiﬁcant correlation between the ﬁve columns denote the ﬁve regressors of the accuracy of Syn,accuracy of Syn and the AI. The left (L) lateral surface (horizon- the accuracy of Spe, age, gender, and the laterality quotient oftal cross hairs at z ¼ 0, 12, 24) and axial sections of the sym- handedness (LQ). (C) Regression coefﬁcients of the AI in themetrical standard brain are shown for the locus of the left F3t left F3t for the ﬁve regressors. Error bars indicate the SEM ofwith a signiﬁcant correlation (red), together with three foci of participants, and asterisks denote the signiﬁcance level of P <the left F3t (green) identiﬁed by our fMRI study [Sakai et al., in 0.05. (D,E) A partial correlation between the standardized AI inpress]. The vertical cross hair on the lateral surface and the hor- the left F3t and the standardized accuracy of Syn (D) or Spe (E),izontal cross hair on the axial sections denote y ¼ 31, whereas after removing the effects of all other factors.
the vertical cross hairs on the axial sections denote x ¼ 32.

r Brain Lateralization and Syntactic Abilities r

According to a partial correlation analysis, the standardized AI at this locus of the left F3t was also signiﬁcantly
correlated with the standardized accuracy of Syn (r ¼ 0.56,
P < 0.0001) (Fig. 4B). In contrast, the standardized AI was
not correlated with the standardized accuracy of Spe at all(r ¼ 0.02, P ¼ 0.9) (Fig. 4C).
We also employed a multiple regression analysis to
examine the effects of the same six standardized factors on
the regional GM. There was a signiﬁcant correlation
between the accuracy of Syn and the regional GM in theleft F3t (x ¼ 34, y ¼ 27, z ¼ 11; Z-score ¼ 2.6; P ¼ 0.049,
FDR corrected) when a SVC (5.5-mm radius sphere at x ¼
33, y ¼ 32, z ¼ 11) was applied. At the locus of the left
F3t (x ¼ 33, y ¼ 32, z ¼ 11), the regression coefﬁcients of
the regional GM were signiﬁcant for the accuracy of Syn(0.011  0.005, P ¼ 0.023) and the total GM (0.026  0.005,
P < 0.0001). Moreover, the standardized regional GM in
the left F3t was signiﬁcantly correlated with the standardized accuracy of Syn (r ¼ 0.23, P ¼ 0.042) (Fig. 5A). In
contrast, at the locus of the right F3t (x ¼ 33, y ¼ 32, z ¼11), the regression coefﬁcients of the regional GM weresigniﬁcant for the total GM (0.030  0.005, P < 0.0001), but
marginally signiﬁcant for the accuracy of Syn (0.009 
0.005, P ¼ 0.059). It should be noted that the standardized
regional GM in the right F3t was signiﬁcantly correlatedwith the standardized accuracy of Syn (r ¼ 0.23, P ¼
0.043) (Fig. 5B). These results suggest that the larger volume of the left regional GM, as well as the smaller volumeof the right regional GM, contributes to the selective correlation between syntactic abilities and the AI in the left F3t.
Regarding the regional WM, there was no signiﬁcant correlation with the accuracy of Syn or Spe (corrected P >0.05).

The Effects of Age
Finally we examined the effects of age, independently ofother factors. Regarding the AI images, we conducted thegroup comparison between the high-school students (N ¼
17 with higher Syn scores) and adult international students(N ¼ 17) matched for proﬁciency (t(32) ¼ 1.0, P ¼ 0.3), butthere was no signiﬁcant difference (corrected P > 0.05).
According to a multiple regression analysis for all

Figure 3.
The correlation between the regional GM in the F3t and syntactic abilities in L2 (N ¼ 95). (A) Regression coefﬁcients of the regional GM in the left F3t for the accuracy of Syn, the accuracyof Spe, age, gender, LQ, and the total GM. Error bars indicate
the SEM of participants, and asterisks denote the signiﬁcancelevel of P < 0.05. (B) A partial correlation between the standardized accuracy of Syn and the standardized regional GM in theleft F3t, after removing the effects of all other factors. C:
Regression coefﬁcients of the regional GM in the right F3t forthe six regressors.

r

3631 rr Nauchi and Sakai r

participants, there was no signiﬁcant correlation (i.e., neither positive nor negative correlation) between age andthe regional GM, but the regional WM showed a signiﬁcantly negative correlation with age in the bilateral coronaradiata (x ¼ 28, y ¼ 48, z ¼ 17; 14,815 voxels; Z-score ¼
4.7; P ¼ 0.017, FDR corrected) (Fig. 6A). In this analysis,
the positive correlation between the regional WM and thetotal WM is expected. At this locus of the right coronaradiata, the regression coefﬁcients of the regional WM

Figure 4.
The structural basis for individual syntactic abilities in L2 for thehigh-school students (N ¼ 78). (A) Regression coefﬁcients of
the AI for the ﬁve regressors. (B,C) A partial correlation
between the standardized AI in the left F3t and the standardized
accuracy of Syn (B) or Spe (C).

r

Figure 5.
The correlation between the regional GM in the F3t and syntactic abilities in L2 (N ¼ 78). (A,B) A partial correlation between
the standardized accuracy of Syn and the standardized regional
GM in the left F3t (A) or right F3t (B).

3632 rr Brain Lateralization and Syntactic Abilities rwere highly signiﬁcant for both age (0.0271  0.005, P <0.0001) and the total WM (0.068  0.005, P < 0.0001) (Fig.
6B). This age-dependent negative correlation in the bilateral corona radiata is consistent with the result reported
previously [Good et al., 2001].
It is interesting to note that the structural basis for syntactic abilities is consistent over a wide range of ages,
namely 14–41 years in the present study. Because the DOEof each participant was highly correlated with age (r ¼
0.96, P < 0.0001) (see Fig. 7), the result was also robust no
matter how short or long the DOE was. The correlation
between age and DOE indicates that it is difﬁcult toapportion variance between these variables, not that they
are equivalent. In our previous fMRI study, we conductedJapanese (L1) versions of the Syn and Spe tasks, which
resulted in the mean accuracy of more than 80% for bothtasks [Sakai et al., in press]. Individual differences in L1,
as well as age-dependency in L1, are thus difﬁcult toassess with these tasks, and it is another challenging issue
for future research.

DISCUSSION
Here we showed that the leftward lateralization of theF3t selectively correlated with the performance of the Syntask, that is, syntactic abilities in L2, independently of lexical knowledge in L2 as tested by the Spe task (Figs. 2 and
4). Moreover, this positive correlation was independent ofage or DOE, as well as of gender and handedness. We
conﬁrmed that the larger volume of the left regional GM,
as well as the smaller volume of the right regional GM,

Figure 6.
The effects of age on the white matter (WM) (N ¼ 95). (A)The bilateral corona radiata with a signiﬁcantly negative correlation between age and the regional WM. Coronal (y ¼ 48), sagittal (x ¼ 28), and axial (z ¼ 17) slices of the symmetrical WM
template are shown. Note the extension of the signiﬁcant voxels
along the ﬁber bundles. (B) Regression coefﬁcients of the regional WM in the right corona radiata for the accuracy of Syn,the accuracy of Spe, age, gender, LQ, and the total WM.

rFigure 7.
A correlation between the DOE to English and age for eachparticipant.

3633 rr Nauchi and Sakai rcontributes to the selective correlation between syntactic
abilities and the AI in the left F3t (Figs. 3 and 5). On theother hand, an age-dependent correlation on the regional
WM was observed only in the sensory pathway of thebilateral corona radiata, suggesting that the languagedependent variance in the regional GM might be independent of the general architecture of cortical networks forbasic sensory-motor functions. Although these correlation
data alone cannot allow the causal interpretation, the correspondence of the left F3t between the present anatomical
study and our previous functional study using the same
paradigm is striking. Given that the syntactic processing inboth L1 and L2 is specialized in the left F3t, as shown previously by our fMRI studies [Sakai et al., 2004, in press],the present results further suggest that the anatomical basis for syntactic abilities generally lies in the speciﬁcity ofthe same region.
Accumulating evidence has indicated that the left F3t is
specialized in syntactic processing, using various syntactic
decision tasks with sentence stimuli [Hashimoto and Sakai,
2002; Iijima et al., 2009; Kinno et al., 2008; Momo et al.,2008; Sakai et al., in press]. The adjacent opercular part(F3op, BA 44) has been also implicated in the syntactic aspect of single words (content or function words) and thecomplexity of sentences [Friederici et al., 2000, 2006].
Indeed, activation has been sometimes found just on thevertical ramus of the Sylvian ﬁssure, thus covering boththe left F3op and F3t, when sentence-level syntax wascompared with other linguistic factors including semantics, spelling, unreal rules, and phonology [Dapretto andBookheimer, 1999; Embick et al., 2000; Musso et al., 2003;
Suzuki and Sakai, 2003]. We have previously demonstrated that these regions showed prominent activation for
syntactic decision tasks even when they were directly compared with verbal short-term memory tasks [Hashimotoand Sakai, 2002]. The activation of the left F3op/F3t is
thus related to the process of analyzing syntactic structures, which cannot be explained either by task difﬁculty
or by verbal short-term memory components. These results
consistently indicate an essential and universal role of theleft F3op/F3t in syntactic processing. This region can bethus regarded as the ‘‘grammar center’’ [Sakai, 2005]. Weshould note, however, that all of these syntactic tasks
involve executive processes as a part of decision-making
component of the tasks. If those executive processes are
general in linguistic decisions, our control task of Spe also
critically involved the same decision-making component,
and thus the Syn-speciﬁc leftward lateralization of the F3tcannot be explained by such general executive processes.
The involvement of speciﬁc linguistic executive processes,
such as syntax-semantics interface, should be further
examined in the future functional and anatomical studies.
We observed a signiﬁcantly negative correlation
between age and the AI in the left F3t (Fig. 2C), suggestingthat this region tends to show more reduced left lateralization when the participant becomes older. Because the ages
were not uniformly distributed among the participants inrthis study, more extensive studies are needed to establish
this tendency. A previous cytoarchitectonic study has indicated the opposite direction, such that asymmetry tended
to increase with age throughout life, which was signiﬁcantin BA 45, but not in BA 44 [Amunts et al., 2003]. Because
the lateralization itself becomes reversed between the lateral and deeper structures within the F3op/F3t (see Fig.
1), the age-dependent lateralization may be affected by thelocation of a targeted region and by a proportion of lateraland deeper structures.
One possible explanation for the signiﬁcance of leftward
lateralization of the grammar center is that the larger the
AI is, the less the inhibition from the right homologous
region becomes, which is controlled through commissuralﬁbers. As a result, the capacity or ﬂexibility of the left F3tactivation increases when compared with more symmetrical or right-dominant brain regions. A recent fMRI study
has reported that participants with a larger corpus callosum showed more left-lateralized activation in inferior
frontal and posterior temporal regions for lexico-semantic
tasks [Josse et al., 2008]. It is possible that the relationshipbetween the corpus callosum size and functional lateralization also depends on the location of a targeted region andon speciﬁc tasks used. According to an intriguing
cytoarchitectonic study, one ‘‘language genius’’ (E.K.), whospoke ﬂuently more than 60 languages in his life, showed
the largest asymmetry in the left F3t, when compared with
control brains [Amunts et al., 2004]. Our large-scale studyof high-school students and adults further suggests thatthe variable asymmetry of the left F3t is a crucial factor for
explaining individual differences on syntactic abilities in
L2. Such information about the speciﬁc brain structure
might be utilized for effectively predicting an individual
aptitude for multiple languages.

ACKNOWLEDGMENTS
We thank T. Tsumoto for his encouragement, Y. Muraishi, K. Hirano, M. Fukushima, N. Narafu, and Y. Tanabe
for assisting with the high-school students, Y. Ochi, K.
Shiota, M. Chiba, T. Katsuragi, and A. Miyata for assistingwith the classroom training in English, N. Komoro and N.
Saeki for technical assistance, and H. Matsuda and S. Matsukura for administrative assistance.

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