ORIGINAL RESEARCH
published: 23 May 2017
doi: 10.3389/fpsyg.2017.00829

Differential Signatures of Second
Language Syntactic Performanceand Age on the Structural Propertiesof the Left Dorsal Pathway
Kayako Yamamoto 1,2 and Kuniyoshi L. Sakai 1,3*
1Department of Basic Science, Graduate School of Arts and Sciences, The University of Tokyo, Tokyo, Japan, 2 Japan
Society for the Promotion of Science, Saitama, Japan, 3 Japan Agency for Medical Research and Development – Core
Research for Evolutional Science and Technology, Tokyo, Japan

Edited by:Niels O. Schiller,
Leiden University, Netherlands
Reviewed by:
Bencie Woll,
University College London,
United Kingdom
Yang Zhang,
University of Minnesota, United States*Correspondence:
Kuniyoshi L. Sakai
sakai@mind.c.u-tokyo.ac.jp
Specialty section:
This article was submitted toLanguage Sciences,a section of the journal
Frontiers in Psychology
Received: 09 December 2016
Accepted: 08 May 2017
Published: 23 May 2017
Citation:
Yamamoto K and Sakai KL (2017)
Differential Signatures of Second
Language Syntactic Performanceand Age on the Structural Propertiesof the Left Dorsal Pathway.
Front. Psychol. 8:829.
doi: 10.3389/fpsyg.2017.00829

In adult second language (L2) acquisition, individual differences are considerably large
even among people with similar experiences. The neural mechanisms underlying thisvariability would include structural plasticity of language-related pathways. To elucidate
such neuroplasticity, we focused on the transitional period of adolescence, which is
associated with certain plasticity toward maturation following the sensitive period of
language acquisition (≤12 years old). The adolescent brain would thus be influenced byage-dependent factors, as well as performances in L2. Here, we examined individual
differences in L2 performances controlling the duration of experience to reveal thedifferential signatures of performances and age on the plasticity of structural properties
in major language-related pathways. We recruited Japanese students at two ages, i.e.,junior (age: 13–14) and senior (age: 16–17) high-school students, all of whom started to
expose to English at age 12 or 13. We divided them into subgroups, so that either
L2 performance [Junior (High)/Senior (Low)] or age [Senior (Low)/Senior (High)] wasmatched in group comparisons; the duration of L2 experience was also controlled
between the Senior (Low) and Senior (High) groups. We then examined the thickness
and fractional anisotropy (FA) of the dorsal and ventral pathways, i.e., the arcuate
fasciculus (Arcuate) and inferior fronto-occipital fasciculus (IFOF), respectively, usingsemi-automatic methods for selecting regions without branches. Regarding FA in theleft Arcuate, the Senior (High) group showed significantly higher FA than the other twogroups, indicating performance-related group differences. Further, FA in the left Arcuate
was selectively correlated with the accuracy of a syntactic task. Regarding the thicknessof the left Arcuate, the Senior (High) and Senior (Low) groups showed significantly
larger thickness than the Junior (High) group, indicating age-related group differences.
These differential performance-related and age-related signatures were evident on theleft Arcuate alone, in contrast to the right Arcuate that showed only mild differencesin thickness, and to the bilateral IFOF that lacked either signature. Our results suggestthat the left dorsal pathway continued to develop to adolescence, and that performancedifferences in a syntactic task can be predicted by its FA, independent of age and theduration of experience.
Keywords: diffusion MRI, white matter, dorsal and ventral pathways, language acquisition, syntax

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exposure (DOE) represent other factors in L2 acquisition (Liet al., 2014). In the present study, we controlled AOE inorder to examine any group differences related to the current
ages of participants (hereafter, age-related group differences),and therefore recruited students at two ages, i.e., junior (age:
13–14) and senior (age: 16–17) high-school students. TheirAOE to English was 12 or 13, and they attended the sameschool where English classes were based on the curriculum
guidelines determined by MEXT (Ministry of Education, Culture,
Sports, Science and Technology). The temporal factor of L2experience, as represented by the DOE, was also controlled andeliminated from the performances for the students at the sameage. Even among such students, large individual variations in
L2 performance were observable. Given that Japanese students
tend to make similar mistakes in English, such as applying
the null-subject (pro-drop) allowed in Japanese, we examinedparticipants’ syntactic abilities in English by a syntactic errordetection task (Syn) that we previously developed with highschool teachers (Sakai et al., 2009). Orthographic knowledge inEnglish was also examined by using a spelling error-detection
task (Spe) with basically the same sets of sentences. Based on thetask performances, the junior and senior students were separately
divided into subgroups. As a result, the task performances of the
Junior (High) and the Senior (Low) groups matched, while thoseof the Senior (High) group were significantly better. We thencompared these three groups, with either age or L2 performance
being fixed. After the group division, we identified the dorsal
and ventral language-related pathways, two major routes thatcombine multiple language areas (Hickok and Poeppel, 2007;
Friederici, 2011). The dorsal and ventral pathways correspond to
the fronto-temporal segment of the arcuate fasciculus (Arcuate)
and the inferior fronto-occipital fasciculus (IFOF), respectively.
We identified these pathways using our previously establishedsemi-automatic methods of defining seeds for tractography in adiffusion magnetic resonance imaging (diffusion MRI) analysis(Yamamoto and Sakai, 2016). We focused on two distinct
structural properties, i.e., the thickness (or the volume of a tract)and fractional anisotropy (FA—the degree of myelination and/or
fiber organization), to examine how age and L2 performance arereflected in these properties of the dorsal and ventral pathways ineach hemisphere.
Several diffusion MRI studies have suggested that the dorsal
pathways mature later than the ventral pathways in both infants
and children. A diffusion MRI study with tractography hasreported that one of the two dorsal pathways, the one connecting
the inferior frontal gyrus (IFG) and the temporal cortex, was nottrackable in 2-day-old newborns; in contrast, the IFOF of theventral pathways, as well as the other dorsal pathway connecting
the premotor cortex and the temporal cortex, was already present(Perani et al., 2011). In a study with 7-year-old children, both
the dorsal and ventral pathways were trackable, but FA of thesepathways was significantly lower than that of adults (Brauer et al.,2013), suggesting that the language-related pathways were notfully mature at this age. Regarding the adolescent ages, it has beensuggested that the dorsal pathway was still under development,
and that the ventral pathway showed less prominent development(Lebel and Beaulieu, 2011). FA in the dorsal pathway has been

INTRODUCTION
Second language (L2) acquisition shows considerably large
individual differences, especially when the L2 is acquired in
adulthood. Even among people with similar L2 experiences(e.g., taking the same classes or lessons on a foreign language),some improve their L2 performances in a relatively shortperiod of time, while others do not improve as well. This
is in marked contrast to first language (L1) acquisition, in
which linguistic abilities are similar among individuals despite
highly variable experiences. However, individual differences in
L1 do emerge when effortful language use is imposed. By using
verb-, rhyme-, and opposite word generation tasks in L1 for
9-year-old children and adult participants, previous studies havereported that distinct regions in the left frontal and occipital
cortices showed age-related or performance-related activations(Schlaggar et al., 2002; Brown et al., 2005). These studies haveindicated the importance of employing subgroups, in which
either age or performance was matched, thereby fixing one of
the two factors in group comparisons. Individual differences
would also be revealed when people learn to read or write
even with their own languages through educational training ofspecific skills. A previous study has reported that the structuralproperty of a white matter pathway connecting the left temporaland parietal language areas may have plasticity associated withliteracy experience even for adults, by comparing three groupsof illiterates, ex-illiterates who learned to read during adulthood,and literates (Thiebaut de Schotten et al., 2014). Long andintensive experiences are required also in L2 acquisition, which
may be supported by the structural plasticity of language-related
pathways. To elucidate such neuroplasticity, it is of interest to
focus on the transitional period of adolescence, which occurs
after the sensitive period of language acquisition (≤12 yearsold). Indeed, adolescence has been suggested to involve certain
plasticity toward maturation (Fuhrmann et al., 2015). The total
cerebral volume has been reported to show a gentle inverted-U
trend, with a peak age different among genders (girls: 10.5 years,
boys: 14.5 years) (Lenroot et al., 2007). While the gray mattervolume gradually decreases in adolescence, after peaking at later
years in higher order association areas (Gogtay et al., 2004;
Lenroot et al., 2007), the white matter continues to increase until
the twenties or later with some regional differences (Westlye
et al., 2010). Moreover, developments in white-matter pathways
are accompanied by large individual differences. A previous
longitudinal study showed that some show increases in volume,
while others show decreases, even at similar ages (Lebel andBeaulieu, 2011). The white matter in the adolescent brain
would be influenced by multiple factors depending on theparticipants’ ages (e.g., biological maturation), as well as on
the attainment of cognitive/motor abilities. More specifically, inmajor language-related pathways, the independent factors of age
and performances after intensive L2 experiences may be reflectedin the plasticity of different structural properties.
Given the large individual differences in L2, many complicatedissues should be tackled in examining the neural plasticity
related to L2 acquisition. In addition to participants’ current
age, the age of first exposure (AOE) and the duration of

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defining seeds in tractography and selecting regions of interest(ROIs) (Yamamoto and Sakai, 2016). In this previous study,
we reported that the thickness of the left Arcuate, averaged
in a one-dimensional ROI, was clearly larger than that of
the right Arcuate; such laterality was evident neither for the
thickness of the IFOF, nor for FA in the Arcuate or IFOF.
In the present study, recruiting a larger number of adolescentparticipants, we confirmed that the leftward laterality of theArcuate was consistent among the three groups. We further
examined the correlation with individual accuracy of Syn/Spe
to clarify which particular aspects of L2 abilities were related tothe structural properties that showed any performance-relatedgroup differences. Our results should thus help to elucidate theneuroanatomical basis of language acquisition after the sensitive
period.

reported to increase during adolescence, mainly associated withincreases in parallel diffusivity, which may reflect the increases inaxon diameters (Giorgio et al., 2010). FA in the language-related
pathways may increase with linguistic experiences, as previous
longitudinal studies reported that FA of the left ventral pathwayof bilinguals was higher than that of monolinguals, possiblyreflecting differences in semantic aspects (Mohades et al., 2015).
However, it remains less clear how these structural developments
can be correlated with behavioral measurements. The relatively
slow development of the dorsal pathway suggests the interesting
possibility that this pathway may be more strongly influenced bylanguage experiences. As suggested by a native language neuralcommitment theory (Kuhl, 2004), neural networks develop under
the coding of L1 inputs from early ages, further influencing theacquisition of L2 in later ages. Indeed, L2 abilities have beenreported to be correlated with L1 abilities, for instance in reading
proficiency (van Gelderen et al., 2007). Given that improvements,
as well as individual differences, in L1 during adolescence become
smaller than those in L2, examining the relationships between L2
acquisition and the structural properties would be of worth inunderstanding the neural plasticity of language-related pathways
in adolescence.
We have performed the following functional and structural
studies on adolescent students. In our previous functional
magnetic resonance imaging (fMRI) study, we identified corticalregions involved in syntactic processing using the same English
tasks as in the present study, and showed a positive correlation
between the individual activations of the left IFG and theperformance accuracy of the Syn task (Sakai et al., 2009). Our
voxel-based morphometry (VBM) study further clarified that
individual leftward lateralization of a single region in the IFG
also showed a correlation with the accuracy of Syn (Nauchi andSakai, 2009). Moreover, in our recent diffusion MRI study wereported that individual FA in the left Arcuate was correlatedwith the accuracy of Syn (Yamamoto and Sakai, 2016), suggesting
the importance of the left dorsal network including the IFG and
the Arcuate in syntactic processing. More specifically, among
the Arcuate and IFOF in both hemispheres, we revealed that
FA in the left Arcuate alone was positively correlated with theperformance, i.e., accuracy of the Syn task, but not with that ofSpe or with L1 verbal fluency. Further, within monozygotic twinpairs, neither the accuracy of Syn nor FA in the left Arcuate weresignificantly correlated between the twins, in spite of the highinter-twin correlation for the thickness of the left Arcuate. Given
these results, syntactic abilities in L2 and FA in the left Arcuate
may thus have been sensitive to non-shared environmental
factors by which the twins were individually affected, while
the thickness was dependent on shared genetic/environmental
factors. Based on these points, we made two further hypotheses.
First, FA in the left Arcuate should show performance-relatedgroup differences that would be observable even among thestudents with the same DOE, because larger variances within
the monozygotic twin pairs were observed for FA than for the
thickness. Second, the thickness of the left Arcuate should show
age-related group differences, as a similar thickness was observed
for monozygotic twin pairs. We tested these hypotheses usingsemi-automatic methods, which we developed previously for

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MATERIALS AND METHODS
Participants
Junior high-school students (age: 13–14) and senior highschool students (age: 16-17) were recruited from the Secondary
School attached to the Faculty of Education, the Universityof Tokyo. Twin pairs were included among the participants;
this school has performed educational as well as twin research.
The following accumulative inclusion criteria were employed in
the present study: (i) right-handedness, i.e., a positive laterality
quotient (LQ), which was assessed using the Edinburgh inventory(Oldfield, 1971), (ii) with neither hearing/visional problems nor
history of neurological/psychiatric diseases, (iii) native Japanese
speakers who started to acquire English in formal education
at the age of 12 or 13 (this condition was met by most of
the students in this school), and (iv) reaction times (RTs)for Spe within the presentation time (6400 ms) for morethan 90% of the trials including incorrect responses. To avoid
including monozygotic/dizygotic twin pairs with potentiallysimilar characteristics, the one with the higher score in Spe wasanalyzed for each pair who met these criteria. As regards thefirst criterion, 8 junior and 11 senior students, who showed anegative LQ or reported a potential history of left-handedness,were dropped. As a result, the population showed relatively
strong right-handedness (LQ > 35). One participant each for thesecond and fourth criterion, and two participants for the third
criterion, were dropped.
For the senior high-school students, we employed three
additional criteria: (v) an accuracy of Spe higher than 65% (i.e.,“mean – 1.5 SD”), (vi) no worse outliers in each task (i.e., higher
than the “mean – 2 SD” for the accuracy, and shorter than the“mean + 2 SD” for the RTs), and (vii) shorter RTs for easier
Spe than for Syn. Given that most Japanese students learn analphabetic writing system at the age of 12–13, and that the seniorhigh-school students had been studying English for about 4 years,
the fifth criterion was necessary to exclude the potential effects
of poor reading abilities and precisely assess individual syntactic
abilities; five senior high-school students were dropped for thisreason. Two students were dropped because they did not meetthe sixth criterion, and two more students because they did not3

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meet the seventh criterion. As a result, we enrolled a total of 39
junior and 38 senior high-school students.
We divided the junior high-school students into two groups:
a group of 14 students [the Junior (High) group] who scoredhigher than 65% in Spe (this was identical to the fifth criterion
employed for senior high-school students), and a group of 25
students [the Junior (Low) group] with scores lower than 65%
in Spe, which were too low to assess their L2 abilities andrelated structures further. In regard to the senior high-school
students, we first divided the 38 students into two groups using
K-means cluster analysis (R software)1 on the accuracy of Syn
and Spe tasks. This analysis yielded a group of 15 participants
with higher L2 abilities [the Senior (High) group], as well asa group of 23 participants with lower L2 abilities. Because
the performances of the group with lower L2 abilities did notmatch those of the Junior (High) group for the accuracy and
RTs of Spe (one-sided t-tests, P < 0.05), we further performeda hierarchical cluster analysis using Ward’s method in the R
software1 based on the accuracy and RTs of Spe for the 23
students with lower L2 abilities. As a result, we divided thesestudents into two groups: a group of 5 students with the higher
accuracy and shorter RTs of Spe [the Senior (Middle) group],
and a group of 18 other students [the Senior (Low) group]. The
accuracy/RTs of both tasks for the Senior (Low) group matchedthose for the Junior (High) group (one-sided t-tests, P > 0.05).
Because our purpose was to examine the differences between
the performance-matched groups with different ages, as well
as between age-matched groups with different L2 abilities, we
focused on the Junior (High), Senior (Low), and Senior (High)groups, dropping the other groups. All participants in the Senior(High) group, as well as seven participants in the Senior (Low)group, were included in our previous study (Yamamoto andSakai, 2016), in which we analyzed participants with an accuracyof Spe ≥ 80% (Experiment I); moreover, these former participants
were the subset of the same 38 senior high-school students
mentioned above. Participants in the Junior (High) group were
newly recruited for the present study. All participants in thethree groups were scanned with the same diffusion MRI protocol.
Demographic details of participants in these three groups, such1

as age, AOE, DOE, and LQ, are shown in Table 1. We obtained
written informed consent for this research from all the students
and their guardians. This study was approved by the Institutional
review board of the University of Tokyo (Komaba) and by theSecondary School.

Stimuli and Tasks
All the students performed English syntactic (Syn) and spelling(Spe) error-detection tasks (50 trials each for Syn and Spe tasks),
as well as a verbal fluency task in Japanese (for three initial lettersin hiragana). The tasks were the same as those we employedin our previous studies (Nauchi and Sakai, 2009; Sakai et al.,2009; Yamamoto and Sakai, 2016); the stimuli for Syn are listed
in Sakai et al. (2009). In the Syn task, we tested argument
structures and related syntactic knowledge, which are difficultfor L2 learners to acquire. For instance, as objects of transitive
verbs are freely omitted in Japanese as well as other languages,
Japanese students tend to accept incorrect (∗ ) English sentences,such as “Do you often meet Mary? – ∗ Yes, I often meet” [seeSakai et al. (2009) for further information on other types ofsyntactic errors]. Because ungrammatical sentences in the Syntask cannot be judged as incorrect by semantic information alone(e.g., by internally translating English sentences into Japanese),
the accuracy of the Syn task reflected individual syntactic abilities
appropriately.

Magnetic Resonance Image Acquisition
and Data Analyses
Magnetic resonance images were acquired with the same
protocols and parameters as in our previous study (Yamamotoand Sakai, 2016). With the same semi-automatic procedures
described in this previous study, we identified the Arcuate and
IFOF in each individual hemisphere. In the present study withgroup comparisons, all the tracts were normalized and analyzed
after the tracking in individual brains; in our previous study,
tracts were analyzed in the native space to focus on individual
variabilities of structural indices (Yamamoto and Sakai, 2016).
Using the affine and non-linear transformation with FLIRT and
FNIRT, all the tracts were spatially normalized to the Montreal
Neurological Institute (MNI) space, and were binarized with thehttps://www.r-project.org/

TABLE 1 | Demographic details of the participants in each group.
N
Junior (High)

Senior (Low)

Senior (High)

Age

AOE

DOE

LQ

vf

Female714 ± 0.5

12.7 ± 0.3

1.5 ± 0.3

82 ± 2024 ± 3.7Male

7

14 ± 0.3

12.6 ± 0.3

1.4 ± 0.2

86 ± 1320 ± 2.6

Total

14

14 ± 0.4

12.6 ± 0.3

1.5 ± 0.3

84 ± 1622 ± 3.6

Female1017 ± 0.3

12.6 ± 0.3

4.4 ± 0.2

82 ± 2124 ± 5.6Male

8

17 ± 0.3

12.7 ± 0.4

4.4 ± 0.2

92 ± 1621 ± 5.0

Total

18

17 ± 0.3

12.7 ± 0.3

4.4 ± 0.2

86 ± 1923 ± 5.4

Female917 ± 0.4

12.5 ± 0.4

4.5 ± 0.2

82 ± 1626 ± 6.5Male

617 ± 0.3

12.6 ± 0.3

4.5 ± 0.2

83 ± 1629 ± 5.3

Total

15

17 ± 0.4

12.6 ± 0.3

4.5 ± 0.2

83 ± 1527 ± 6.0

Data are shown as the means ± SD for the number of participants (N), age, age of first exposure (AOE) to English, duration of exposure (DOE) to English, laterality quotient(LQ), and the number of words produced in the verbal fluency task (vf).

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20 mm, and slid the segment. We selected the segment with aminimal SD as an ROI.
In order to avoid the potential uncertainty of FA near
the peripheral regions of fiber tracts, we set the thresholding(FA ≥ 0.2) in accordance with previous literature. The resultant
FA maps were normalized using the affine and non-linear
transformation with FLIRT and FNIRT. Within each ROI, we
calculated the mean FA for each group, and examined the groupdifferences. Statistical analyses were performed using R software.
We used the packages cocor3 for comparing correlations, ppcor4
for partial correlations, and pwr5 for power analyses, as well as
lme46 and car7 for linear mixed-effects models (Koerner andZhang, 2017).

fslmaths function of FSL software. While FLIRT and FNIRT areconventional volume-based registration algorithms using voxellevel information, a method of combining volume-based andsurface-based registration (Zöllei et al., 2010), as well as an
improved voxel-based registration (Schwarz et al., 2014), hasbeen proposed for better alignment. We overlaid the binarizedtracts across the participants for each pathway, thereby producing
population probability maps, in which voxel values represented
the number of participants. The population probability maps
with thresholding (at least half of the participants) were smoothedand shown using MRIcroN software2 .

ROI Selection
We basically followed the ROI selection procedures in ourprevious study (Yamamoto and Sakai, 2016); we determined
one-dimensional ROIs (in an antero-posterior direction) at the
portion with the most uniform thickness, and showed that theappropriate length, i.e., ROI size, minimizing the individual
variances of thickness was 20 and 15 mm for the Arcuate and
IFOF, respectively. We defined the thickness of a pathway as
the number of voxels at a coronal section (voxel size, 1 mm2 ),because the relatively straight portions of these two pathways(i.e., the portions without branches) were nearly horizontal.
We first measured the thickness of each participant’s Arcuate
for the length of 35 mm (y = −40 ∼ −6; the candidate
region for ROI), excluding the branching or curved portions.
Within these candidate regions, we then calculated the standard
deviation (SD) of the thickness across a tract segment of 20 mm,
and slid the segment. At each position, the averaged SD was
obtained among all the participants of the three groups. We
selected the segment with a minimal averaged SD as an ROI ineach hemisphere, thereby extracting the region with the most
uniform thickness across participants. Using these procedures, we
objectively selected ROIs at the same position in the MNI space,
thereby minimizing individual variabilities in the ROI selection.
In regard to the IFOF, we set a candidate region with a lengthof 70 mm and selected a 15-mm-long ROI in each hemisphere, in
accordance with our previous study. We measured the thicknessof each participant’s IFOF for y = −75 ∼ −6, excluding thebranching or curved portions. Within these candidate regions,
we calculated the SD of the thickness across a tract segment of
15 mm, and slid the segment. At each position, the averaged SD
was obtained among all the participants. We selected the segmentwith a minimal averaged SD as an ROI in each hemisphere.
We next examined the correlation with individual accuracy of
Syn/Spe to clarify which aspects of L2 abilities were related to thestructural property that showed any performance-related groupdifferences. For the analyses within a single group, we aimed to
examine individual variances in a pathway, thereby employing
individually selected ROIs on the normalized tracts. We selected
ROIs where the thickness was most uniform for the tract of eachparticipant in the MNI space. As described above, the thickness of
the Arcuate was measured for the candidate region with a lengthof 35 mm (y = −40 ∼ −6). Within these candidate regions,
we calculated the SD of the thickness across a tract segment of2

RESULTS
Behavioral Data
Task performances of Syn and Spe in the Junior (High), Senior(Low), and Senior (High) groups are shown in Figure 1.
Regarding the accuracy (Figure 1A), a two-way repeatedmeasures analysis of variance (rANOVA) [group × task (Syn,Spe)] showed significant main effects of group [F(2,44) = 47,
P < 0.0001] and task [F(1,44) = 169, P < 0.0001] without
interaction [F(2,44) = 0.4, P = 0.6]. A linear mixed-effects
model analysis [fixed effects: group, task; random effects:
subject] confirmed significant effects of group [χ2 (2) = 68,
P < 0.0001] and task [χ2 (1) = 219, P < 0.0001]. Regarding
RTs (Figure 1B), an rANOVA showed significant main effects
of group [F(2,44) = 6.3, P < 0.005] and task [F(1,44) = 116,
P < 0.0001] with a significant interaction [F(2,44) = 4.2,
P < 0.05]. A linear mixed-effects model analysis confirmed
significant effects of group [χ2 (2) = 13, P < 0.005] andtask [χ2 (1) = 102, P < 0.0001]. One-way ANOVAs did notshow a significant effect of gender for the accuracy or RTs ofeither task [F(1,45) < 0.2, P > 0.7]. According to the t-tests(Bonferroni-corrected for three comparison pairs, significancelevel at α = 0.017), we confirmed that the Senior (High) group
had significantly higher accuracy and shorter RTs than the othertwo groups in both tasks (effect size: d > 0.90, statistical power:
1 – β > 0.73), indicating that the Senior (High) group had bettersyntactic abilities and word knowledge than the other two groups.
If a behavioral parameter reflected factors commonly involvedin both Syn and Spe, such as reading proficiency and taskdifficulty, that parameter would be correlated between Syn andSpe among the participants (see Yamamoto and Sakai, 2016). For
instance, RTs of a slow reader would be relatively long among theparticipants for both tasks. Conversely, if a behavioral parameter
was not correlated between the two tasks, that parameter would
reflect, at very least, factors distinctly required in each task.
Thus we analyzed the correlations among accuracy of the two
3

https://cran.r-project.org/web/packages/cocor/
https://cran.r-project.org/web/packages/ppcor/
5
https://cran.r-project.org/web/packages/pwr/
6
https://cran.r-project.org/web/packages/lme4/
7
https://cran.r-project.org/web/packages/car/4

http://people.cas.sc.edu/rorden/mricron/index.html

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FIGURE 1 | Behavioral data of Syn and Spe tasks for the three groups. (A) The accuracy of Syn and Spe tasks for the three groups of high school students,
Junior (High), Senior (Low), and Senior (High), are indicated by bars with white, gray, and black shades, respectively. Error bars indicate the standard error of themean (SEM) for the participants, and asterisks denote the significant differences (Bonferroni-corrected P < 0.05). (B) The reaction times (RTs) of the Syn and Spetasks for the three groups are indicated by dots corresponding to the white, gray, and black shades in (A). The Senior (High) group showed significantly higher L2
abilities, i.e., higher accuracy and shorter RTs, while the Junior (High) and Senior (Low) groups showed no significant difference in the accuracy or RTs in either task.
(C,D) Independence of the accuracy of the Syn and Spe tasks. Individual behavioral parameters were plotted to compare the two tasks, as shown by the plotted
dots, whose groups correspond to the shades in (A). The dotted line indicates an inclusion criterion of Spe. The accuracy of Syn and Spe showed no significant
correlation (C), while the RTs of Syn and Spe were highly correlated (D).

tasks, as well as among RTs. The accuracy of Syn and Spe was
not significantly correlated (r = 0.27, P = 0.07; Figure 1C);
it showed a week correlation among the three groups, as the
Senior (High) group showed the higher accuracy of Syn/Spe thanthe other two groups, but when examined in each group, suchsignificant positive correlation between the accuracy of Syn and
Spe was not observed in any of the three groups (P > 0.3). These
results suggest that the accuracy of Syn and Spe mainly reflectedabilities distinctly required for each task. In contrast, the RTsof Syn and Spe were highly correlated (r = 0.82, P < 0.0001;
Figure 1D). Indeed, the RTs of Syn and Spe were positively
correlated in all three of the groups (r > 0.7, P < 0.005). These
results indicate that the RTs of each participant were related togeneral cognitive processes common to both tasks. Moreover,the correlation coefficient between RTs of Syn and Spe wassignificantly larger compared to that between the accuracy of Syn
and Spe (Z = 4.4, P < 0.005), confirming the differential natures

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of these two behavioral measurements. These results suggestthat a participant’s accuracy of each task reflected individual
abilities employed for each task. On the other hand, RTs were
metrics that reflected more general cognitive abilities, such as
reading proficiency. Once a structural property which showed
any group difference related to L2 acquisition was found, we
further examined its correlation with the accuracy of Syn or
Spe to reveal which ability was dominantly reflected. Moreover,
we also examined its correlation with the RTs to reveal if thisstructural property was related to general cognitive abilities.
We also examined the verbal fluency data in L1, andfound a consistent trend among groups with the Syn and Spe
performances. Behavioral data of the verbal fluency task areshown in Table 1. A one-way ANOVA showed a significant effectof group [F(2,44) = 4.0, P < 0.05]. The Senior (High) groupproduced significantly larger numbers of words than the Junior(High) group [t(23) = 2.8, P < 0.005, d = 1.1, 1 – β = 0.82],

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hemisphere, and found that FA of the left Arcuate in the Senior(High) group was higher than those of the other two groups,
especially in the anterior regions, as indicated by the nonoverlapping error bars (Figure 3B). In contrast, FA of the right
Arcuate did not show such clear group differences. In regard to
the IFOF, however, no clear group difference was observed. In
these ROIs, FA in the Arcuate showed some modulations, while
FA in the IFOF showed relatively sharp antero-posterior changes.
Nevertheless, the overall tendency of thickness or FA was similar
among the three groups throughout the candidate regions in bothhemispheres.

surviving Bonferroni correction for the three comparison pairs(significance level at α = 0.017); the Senior (High) group also
produced larger numbers of words than the Senior (Low) group[t(31) = 2.0, P = 0.03, d = 0.7, 1 – β = 0.52]. For the
performance-matched groups, i.e., the Junior (High) group andthe Senior (Low) group, there was no significant difference[t(30) = 0.8, P = 0.2]. To examine how syntactic abilities in L2
were related to overall proficiency in L1, we further examined thecorrelations between the verbal fluency in L1 and the accuracy of
Syn for each group. While correlations were not significant for
the Senior (High) (r = 0.23, P = 0.4) and Senior (Low) (r = 0.10,
P = 0.7) groups, a significant positive correlation was present for
the Junior (High) group (r = 0.68, P < 0.01). These results suggestthat syntactic abilities in L2 may depend on L1 proficiency inearly acquisition stages (DOE ≈ 1.5 years), but this relationshipbecame weaker in later acquisition stages (DOE ≈ 4.5 years).

Distinct Group Differences in the
Structural Properties of the Left Arcuate
For all the participants, the ROIs were placed at the same
position of each pathway in the MNI space. Within these
ROIs, we calculated the mean thickness of the Arcuate, andconfirmed the leftward laterality (Figure 2). A two-way rANOVA[group × hemisphere (left, right)] indicated significant main
effects of group [F(2,44) = 4.9, P = 0.01] and hemisphere[F(1,44) = 27, P < 0.001], without an interaction [F(2,44) = 0.3,
P = 0.7] (Figure 4A). Considering the potential relationships
between the thickness in the left and right hemispheres of thesame participants, we used a linear mixed-effects model analysis[fixed effects: group, hemisphere; random effects: subject],confirming significant effects of group [χ2 (2) = 9.8, P = 0.007]
and hemisphere [χ2 (1) = 28, P < 0.0001]. Indeed, in all of
the three groups, the mean thickness in the ROI of the Arcuate
was significantly larger in the left than in the right hemisphere(P ≤ 0.02) (one-sided t-tests). As regards the group differences,the mean thickness of the left Arcuate for the Senior (High) groupwas significantly larger than that of the Junior (High) group[t(27) = 3.1, P = 0.002, d = 1.2, 1 – β = 0.94] (one-sided t-tests);
the mean thickness for the Senior (Low) group was also larger
than that of the Junior (High) group [t(30) = 1.8, P = 0.04,
d = 0.7, 1 – β = 0.59]. There was no significant difference
between the Senior (High) and Senior (Low) groups [t(31) = 0.86,
P = 0.2]. Regarding the mean thickness of the right Arcuate,
the thickness for the Senior (High) group was significantly larger
than that for the Junior (High) group [t(27) = 3.0, P = 0.003,
d = 1.2, 1 – β = 0.93]. There was no significant difference
between the Senior (Low) and Junior (High) groups [t(30) = 1.3,
P = 0.10] or between the Senior (High) and Senior (Low) groups[t(31) = 1.6, P = 0.06]. No significant effect of gender wasobserved in either hemisphere, according to one-way ANOVAs[F(1,45) < 0.4, P > 0.5].
Based on the results of FA shown in Figure 3B, we focusedon group differences in the left Arcuate. For all voxels (withFA values of 0.2 or higher) within the tract at the ROI of
the left Arcuate, we calculated the mean FA, which was clearlyhigher in the Senior (High) group than in the other two groups(Figure 4B). A one-way ANOVA for FA in the left Arcuate
indicated a significant main effect of group [F(2,44) = 3.3,
P < 0.05]. More specifically, FA in the left Arcuate for the Senior(High) group was significantly higher than that for the Junior(High) group [t(27) = 2.2, P = 0.016, d = 0.9, 1 – β = 0.75];

Group Differences along the Tract of theArcuateThe Arcuate and IFOF were successfully tracked in bothhemispheres for every participant, and the tracking was basicallysimilar among groups. In all groups, the Arcuate connected
the frontal and temporal regions with a similar curvature, andthe IFOF connected the frontal and occipital/temporal regions
through a narrower portion near the external capsule (Figure 2).
While these overall characteristics were the same for the left
and right hemispheres, the left Arcuate was thicker than theright Arcuate. From both lateral and top views, the Arcuate wasconsistently thicker and extended more anteriorly in the left
hemisphere. The Arcuate of the Senior (High) and Senior (Low)groups was thicker than that of the Junior (High) group, which
was evident from both views. Such group differences were notobserved for the IFOF in either hemisphere.
To examine the overall profile while excluding highly variable
regions among individuals, we first set the candidate regions
for ROI selection: the region of 35 mm for the Arcuate(y = −40 ∼ −6), and the region of 70 mm for the IFOF
(y = −75 ∼ −6) (Figure 2). As regards the Arcuate, the candidate
region was selected where the pathway was relatively straight,
excluding the curved or branching portions. The candidate
region for the IFOF was also selected where the pathway
was straight, excluding the narrower portion near the external
capsule, resulting in a longer candidate region than for the
Arcuate. The thickness of the Arcuate in the Senior (High)and Senior (Low) groups was significantly larger than that of
the Junior (High) group throughout the candidate region inboth hemispheres, as indicated by the non-overlapping error
bars (mean ± SEM) (Figure 3A). In contrast, for the thicknessof the IFOF, no clear group difference was observed in either
hemisphere. For most of the candidate regions in the Arcuate and
IFOF, the thickness was basically uniform in both hemispheres.
We selected one-dimensional ROIs, where the thickness wasmost uniform (see the “Materials and Methods” section). Because
the thickness was independent of FA, our ROIs were free fromsampling bias of extracting regions with particularly higher orlower FA. We also plotted FA in the same regions in each

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FIGURE 2 | The Arcuate and IFOF reconstructed with diffusion MRI. The probability maps of population for the Arcuate and IFOF in the MNI space. The
pathways were thresholded to show the results of the tracking present in more than half of the participants in each group. The color scales denote the number ofparticipants (%): black–red to yellow–white for the Arcuate, and blue to green for the IFOF. Note that the Arcuate in the Senior (High) and Senior (Low) groups wasclearly thicker than that in the Junior (High) group, which was evident from both left lateral (top row) and top (middle row) views. Similar tendency was observed in theright hemisphere from the right lateral (bottom row) view. To examine the overall profile while excluding highly variable regions among individuals, we first set
candidate regions for selecting regions of interest (ROIs): a region of 35 mm for the Arcuate (y = –40 ∼ –6), and a region of 70 mm for the IFOF (y = –75 ∼ –6). The
right-most panel shows the candidate regions, which are bounded by the pairs of black lines. We further selected ROIs at the portion with the most uniform
thickness in each pathway to quantify the Arcuate and IFOF (see the “Materials and Methods” section), as shown in Figure 3.

FA in the left Arcuate for the Senior (High) group was also higher
than that for the Senior (Low) group [t(31) = 2.2, P = 0.019,
d = 0.8, 1 – β = 0.72]. There was no significant difference
between the Senior (Low) and Junior (High) groups [t(30) = 0.02,
P = 0.5]. Regarding FA in the ROI of the right Arcuate, a oneway ANOVA did not show a significant main effect of group[F(2,44) = 2.0, P = 0.15]. No significant effect of gender wasobserved for FA in either hemisphere, according to one-way
ANOVAs [F(1,45) < 0.2, P > 0.7].
In regard to the IFOF, neither the mean thickness nor mean
FA in the ROI showed a group difference (Figures 4C,D). A oneway ANOVA for the thickness did not show a significant main
effect of group in either hemisphere [F(2,44) < 1.7, P > 0.8].
In addition, a one-way ANOVA for FA in the IFOF did notshow a significant main effect of group in either hemisphere[F(2,44) < 2.6, P > 0.05]. Major structural properties, i.e., theFrontiers in Psychology | www.frontiersin.org

thickness and FA, in the ROI of IFOF in both hemispheres weresimilar among the three groups.

FA in the Left Arcuate Was Selectively
Correlated with the Accuracy of Syn
For FA in the left Arcuate, which showed group differences
between the Senior (High) and the other two groups (seeFigure 4B), we examined what aspect of L2 abilities was actuallyrelated to FA. We performed the following analyses for the Senior(High) group, whose task performances were higher and thus
most reliable for dissociating the linguistic abilities required by
Syn or Spe. ROIs were selected for each participant as describedin the “Materials and Methods” section. We performed partial
correlation analyses between the standardized accuracy of Syn
and the standardized FA in the left Arcuate, removing the effects

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FIGURE 3 | Profiles of the thickness/FA of the dorsal and ventral pathways in each group. (A) The profiles of thickness for the Arcuate and IFOF. (B) The
profiles of FA for the Arcuate and IFOF. The thickness and FA were averaged among the participants in each of the Junior (High), Senior (Low), and Senior (High)groups, as shown in blue, green, and red, respectively. Data are shown for the range of y = –40 ∼ –6 for the Arcuate and y = –75 ∼ –6 for the IFOF (bounded by thepairs of black lines in Figure 2) in the MNI space. Note that the thickness of the Arcuate in the Senior (High) group is larger than that in the Junior (High) group in
both hemispheres. Moreover, FA in the left Arcuate in the Senior (High) group is higher than those in the other two groups. No clear group difference was found forthe IFOF in either hemisphere. The SEMs in each group are shown as shaded bands in each color. The positions of ROIs are indicated by the black lines above theaxes. A, anterior.

FIGURE 4 | Group differences in the structural properties of the left Arcuate. (A) Age-related group differences on the thickness of the left dorsal pathway.
(B) Performance-related group differences on FA in the left dorsal pathway. (C,D) The ventral pathway without group differences. The Junior (High), Senior (Low), andSenior (High) groups are indicated by bars/dots with white, gray, and black shades, respectively. Error bars indicate the SEM for the participants, and asterisks
denote statistical differences at P < 0.05 (post hoc t-test after ANOVA).

(r = 0.40, P = 0.2), according to the partial correlation analysis
removing the effects of the accuracy of Syn, LQ, and gender(Figure 5B). In addition, no significant correlation was foundbetween FA in the left Arcuate and verbal fluency in L1 (r = 0.24,

of the accuracy of Spe, LQ, and gender. Regarding the accuracy ofSyn, we found a significant correlation with FA in the left Arcuate(r = 0.61, P = 0.03) (Figure 5A). In contrast, the accuracy of
Spe was not significantly correlated with FA in the left Arcuate

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P = 0.6), according to a partial correlation analysis removing
the effects of the RTs of Spe, LQ, and gender. These results
indicate that increased FA in the left Arcuate for the Senior (High)group was related mainly to the enhanced syntactic abilities in
L2, irrespective of L1 performances or other general measures
examined here.

DISCUSSION
In the three groups of high school students, we obtained thefollowing results. First, performance-related group differenceswere found only for FA in the left Arcuate. More specifically,
the Senior (High) group, who had higher L2 abilities, showed
higher FA in the left Arcuate than the Senior (Low) and Junior(High) groups (Figures 3B, 4B). Moreover, the mean FA in
the ROI of the left Arcuate of the Senior (High) group was
significantly correlated with the accuracy of Syn (Figure 5A),
but not with the accuracy of Spe (Figure 5B) or with verbal
fluency in L1, indicating that increased FA in the left Arcuate
was related mainly to the enhanced syntactic abilities in L2.
Secondly, age-related group differences were found for the
thickness of the left Arcuate. The thickness for the Senior (High)and Senior (Low) groups was larger than that for the Junior(High) group (Figures 3A, 4A), indicating that the left Arcuate
was still developing in adolescence. Thirdly, these differential
performance-related and age-related signatures were evident on
the left Arcuate alone, in contrast to the right Arcuate that showed
only mild differences in thickness (Figures 3A, 4A), and to thebilateral IFOF that lacked either signature (Figures 3, 4C,D).
To the best of our knowledge, our study is the first to reportthat plasticity during the adolescent years was markedly different
between the dorsal and ventral language-related pathways, theformer of which was related to syntactic abilities. In summary, we
showed that the left dorsal pathway, which has been reported tobe more immature than the ventral pathway from early infancy,
continued to grow thicker with increasing age at least until
the adolescent years. Further, by showing the group difference
between the Senior (High) and Senior (Low) groups, whose DOEs
were the same, we revealed that performance differences werereflected in the FA in the left dorsal pathway, independent of age
and the duration of experience. These results indicate that the left
dorsal pathway is a major neural network supporting syntactic
abilities.
Within the same part of the left dorsal pathway, we observed
the dissociated performance-related and age-related groupdifferences on FA and the thickness, respectively. These results
provide new insights into the plasticity of these two distinct
structural properties in the left Arcuate. FA and the volume of
the Arcuate have been reported to change during the adolescentyears (Lebel and Beaulieu, 2011), but it has remained unclear
whether or not these properties change in accordance with thedevelopment of specific abilities. Our present results suggest that
not age or maturation per se but the gradual improvement of
performances in syntactic abilities during adolescence was related
to FA. The increased FA in accordance with certain learning or L2
exposure has been reported also in other pathways. For instance,

FIGURE 5 | FA in the left Arcuate was selectively correlated with theaccuracy of Syn. (A) The scatter plots of the standardized accuracy of Syn
and the standardized mean FA in the left Arcuate. The ROIs in the left Arcuate
were determined for each participant in the Senior (High) group. The effects ofthe standardized accuracy of Spe, gender, and laterality quotient (LQ) were
removed. (B) The scatter plots of the standardized accuracy of Spe and thestandardized mean FA in the left Arcuate. The effects of the standardized
accuracy of Syn, gender, and LQ were removed. FA in the left Arcuate wascorrelated with the accuracy of Syn, but not with the accuracy of Spe.

P = 0.4) in the partial correlation analysis removing the effects of
LQ and gender. Moreover, no significant correlation was foundbetween FA in the left Arcuate and the RTs of Syn (r = 0.17,

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associated with age, which may reflect biological maturation, as
well as common and specific experiences that students underwent
during the ages of 13–17. A recent longitudinal study reported
that children’s structural connectivity, which was obtained before
they learned to read (i.e., before age 5), predicted the spatial
profile of functional activations in the Visual Word Form Area
(VWFA) after they learned to read (i.e., after age 8), suggestingthat connectivity precedes the functional development (Saygin
et al., 2016). These results raise an interesting hypothesis thatexperience interacts with the micro-structural development ofa pathway whose structural connectivity has already developed.
A more detailed picture of the developmental mechanism of
language-related structures would be provided by closely linking
the development of linguistic abilities and that of white matter
pathways, as well as the structures of connected cortical regions,which can be examined by such methods as VBM and the
myelin mapping technique (Glasser and Van Essen, 2011). Ourpresent study showed both age-related and performance-relatedgroup differences in adolescent participants, suggesting theimportance of future longitudinal studies with various structuraland functional measurements.
In addition to the fronto-temporal segment examined here,
the arcuate fasciculus is also composed of the fronto-parietal
and temporo-parietal segments (Catani et al., 2005). Thiebaut de
Schotten et al. (2014) have suggested that the temporo-parietal
segment has plasticity associated with learning even in adults,
based on their finding that its FA was higher in a group of
ex-illiterates, who lacked access to schools during childhood
for social reasons and learned to read during adulthood, in
contrast to a group of illiterates, who never learned to read.
They also showed that FA was correlated with activations in
the two regions, i.e., the left VWFA and planum temporale,connected to the angular/supramarginal gyri by this segment.
As the authors of this study discussed in their subsequent paper(Dehaene et al., 2015), these results might have been influenced
by multiple factors, including the motivations, self-confidence,socioeconomic status, and professions of the participants. Indeed,differences in FA between ex-illiterates and illiterates might bepresent before ex-illiterates voluntarily begin to learn reading.
Future studies should attempt to verify whether or not “learning
to read improves the structure” or not. To examine such causal
changes in the brain, longitudinal studies that track neural indicesand behavioral measures, together with multiple regression
analyses that de-correlate confounding variables, would becritical (Galván, 2010; Dehaene et al., 2015). Note that ourpresent study does not intend to suggest causal influences of
L2 acquisition on structural properties. Rather, we demonstrated
here that the performance-related group differences, which wereseparated from the duration of L2 experience (i.e., DOE) as well
as from the age-related group differences, were predicted by FA
in the left dorsal pathway.

an increase in FA in the genu of the corpus callosum wascorrelated with the overall L2 performances after a 9-monthintensive course of spoken and written Chinese (Schlegel et al.,2012). Moreover, an increase in FA in the white matter underlying
the right IFG was correlated with vocabulary test scores after a
16-week period of vocabulary training in English (Hosoda et al.,2013). In our previous study, focusing on students with better
orthographic knowledge (80% or higher accuracy in the Spe task),
we showed that individual differences in the accuracy of Syn
were reflected in FA in the left Arcuate (Yamamoto and Sakai,2016). In the present study, analyzing students with a wider
range of L2 abilities and ages, we demonstrated that FA in theleft Arcuate was higher in students with higher L2 abilities thanin students with lower abilities at the same age, whose FA wasnot significantly different from performance-matched younger
students. Further, we showed that FA in the left Arcuate of the
Senior (High) group was positively correlated with the accuracyof the syntactic task, but not with the accuracy of the spellingtask. These results indicate that the higher FA in the left dorsal
pathway was mainly related to the higher syntactic abilities in
L2. As described in the “Materials and Methods” section, theSyn task was designed to test argument structures and related
syntactic knowledge in English, and cannot be correctly answeredby semantical/pragmatic cues, or by internally translating English
sentences into Japanese. Indeed, the accuracy of Syn and L1 verbal
fluency was not significantly correlated in the Senior (High) andSenior (Low) groups. Future studies with tasks that can accurately
assess individual syntactic abilities in L1 will be needed to reveal
how L1 syntactic abilities, as well as neural networks supportingthese abilities, facilitate (or hamper) the acquisition of a new
language. Moreover, it would be also important to elucidate how
the development in other aspects of linguistic abilities is related
to the plasticity in the left dorsal pathway.
Another important issue is whether non-cognitive abilities are
related to the development of the language-related structures.
A previous study on L2 learning in infants indicated the impact
of social interaction, by showing that infants who received “liveperson” sessions on Mandarin performed significantly better on
Mandarin phonetic perception tests, compared to infants who
received the identical information via television or audiotape but
showed no learning effects (Kuhl et al., 2003). These social factors,
as well as other non-cognitive factors such as motivation and selfconfidence, may have impacts on L2 acquisition in adolescentstudents and adults as well (Dörnyei, 2003; Gardner, 2010).
One of the directions of future studies would be to investigate
how such individual traits affect one’s acquisition experience,
which may further modify functional and structural networks. It
would also be important to dissociate the effects of non-cognitive
abilities on language-related networks from those of cognitive
abilities on the left dorsal pathway, whose critical involvement
in linguistic information processing has been shown by previous
studies (Ohta et al., 2013; Yamamoto and Sakai, 2016), andconfirmed in the present study.
Here, we showed that the thickness of the left Arcuate waslarger in the Senior (High) and Senior (Low) groups than in
the Junior (High) group, indicating age-related group differences.
This macro-structural property of the left Arcuate had plasticity

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AUTHOR CONTRIBUTIONS
All authors listed have made substantial, direct and intellectual
contribution to the work, and approved it for publication.

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FUNDINGACKNOWLEDGMENTS

This work was supported by AMED-CREST (Japan Agency
for Medical Research and Development – Core Research for
Evolutional Science and Technology) grant and by a Grant-inAid for the Japan Society for the Promotion of Science (JSPS)
Fellows (15J09382).

We thank R. Kinno and S. Ohta for their helpful discussions,N. Komoro for the technical assistance, H. Matsuda forthe administrative assistance, and all participating students,
guardians and teachers for their support of the present
study.

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Yamamoto and Sakai

Neuroanatomy of Second Language Acquisition

Copyright © 2017 Yamamoto and Sakai. This is an open-access article distributed
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use, distribution or reproduction in other forums is permitted, provided theoriginal author(s) or licensor are credited and that the original publication inthis journal is cited, in accordance with accepted academic practice. No use,
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Zöllei, L., Stevens, A., Huber, K., Kakunoori, S., and Fischl, B. (2010). Improved
tractography alignment using combined volumetric and surface registration.
Neuroimage 51, 206–213. doi: 10.1016/j.neuroimage.2010.01.101
Conflict of Interest Statement: The authors declare that the research was
conducted in the absence of any commercial or financial relationships that could
be construed as a potential conflict of interest.

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