Cortical activation in the processing of passive sentences in L1 and L2: An fMRI study

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NeuroImage 30 (2006) 570 – 579

Cortical activation in the processing of passive sentences

in L1 and L2: An fMRI study

Satoru Yokoyama,a,b,* Hideyuki Okamoto,b,d Tadao Miyamoto,a Kei Yoshimoto,a Jungho Kim,f

Kazuki Iwata, b,c Hyeonjeong Jeong, a,b Shinya Uchida, b,e Naho Ikuta, b,c Yuko Sassa, b,c

Wataru Nakamura,a Kaoru Horie,a Shigeru Sato,a and Ryuta Kawashimab

aGraduate School of International Cultural Studies (GSICS), Tohoku University, Kawauchi, Aoba-ku, Sendai-shi, Miyagi-ken, 980-8576, JapanbNew Industry Creation Hatchery Center, Tohoku University, 6-6-10, Aoba, Aza, Aramaki, Aoba-ku, Sendai-shi, Miyagi-ken, 980-8579, JapancLBC Research Center, Tohoku University 21st Century Center of Excellence Program in Humanities, Kawauchi, Aoba-ku, Sendai-shi,

Miyagi-ken, 980-8576, JapandGraduate School of Medicine, Tohoku University, Seiryo-cho, Aoba-ku, Sendai-shi, Miyagi-ken, 980-8574, JapaneDepartment of Radiology and Nuclear Medicine, IDAC, Tohoku University, Seiryo-cho, Aoba-ku, Sendai-shi, Miyagi-ken, 980-8574, JapanfGraduate School of Arts and Letters, Tohoku University, Kawauchi, Aoba-ku, Sendai-shi, Miyagi-ken, 980-8576, Japan

Received 19 May 2005; revised 29 September 2005; accepted 29 September 2005

Available online 21 November 2005

The question of whether the bilingual brain processes a first and second

language (L1 and L2, respectively) differently is a central issue in many

psycholinguistic and neurolinguistic studies. This study used functional

magnetic resonance imaging (fMRI) to investigate whether late

bilinguals process structurally complex sentences in L1 and L2 in

different cortical networks. For this purpose, we directly compared

brain activity during the processing of active and passive sentences in

both L1 and L2. We asked 36 healthy subjects to judge whether or not a

presented sentence was semantically plausible. Both L1 andL2 activated

the left hemispheric language-related regions such as the left inferior

frontal, superior/middle temporal, and parietal cortices. However, we

found different activation patterns between L1 and L2 in the processing

of passive sentences. Passive sentences elicited greater activation than

their active counterparts in the left pars triangularis, the premotor area,

and the superior parietal lobule in Japanese, but not in English.

Furthermore, there was a significant interaction between sentence type

(active versus passive) and language (Japanese versus English) in the left

pars orbitalis. The results of this study indicate that late bilinguals use

similar cortical regions to comprehend both L1 and L2. However, when

late bilinguals are presented with structurally complex sentences, the

involvement of these regions differs between L1 and L2. These results

suggest that, in addition to age of L2 acquisition and L2 proficiency,

differences in grammatical construction affect cortical representation

during the comprehension of L1 and L2.

D 2005 Elsevier Inc. All rights reserved.

Keywords: Bilingual; Sentence comprehension; Passive sentence; fMRI

1053-8119/$ - see front matter D 2005 Elsevier Inc. All rights reserved.

doi:10.1016/j.neuroimage.2005.09.066

* Corresponding author. Graduate School of International Cultural

Studies (GSICS), Tohoku University, Kawauchi, Aoba-ku, Sendai-shi,

Miyagi-ken, 980-8576, Japan. Fax: +81 22 795 4088.

E-mail address: [email protected] (S. Yokoyama).

Available online on ScienceDirect (www.sciencedirect.com).

Introduction

Many psycholinguistic and neurolinguistic studies have inves-

tigated the question of how the bilingual brain processes a first and

second language (L1 and L2, respectively). For example, based on

their study of aphasics, Albert and Obler (1978, p. 254) have argued

that L2 is represented more globally than L1 and that the right

hemisphere plays an important role in L2 representation. Other

researchers have presented evidence that following brain injury,

multilinguals exhibit different degrees of damage (Fabbro and

Paradis, 1995) and recovery (Junque et al., 1995). Furthermore, in an

experiment using electrical cortical stimulation during brain surgery,

Ojemann and Whitaker (1978) showed that L2 is more broadly

represented in epileptic bilingual patients than in their monolingual

counterparts. Although these studies did not lead to the same

conclusions, the combined evidence suggests that different cortical

areas are involved in the comprehension of L1 and L2. Neuro-

imaging studies, however, have yielded inconsistent results on this

question. Some imaging studies have found different activation

patterns for L1 and L2 (e.g., Klein et al., 1994; Perani et al., 1996;

Dehaene et al., 1997), while others have reported no difference in

activation between L1 and L2 (e.g., Klein et al., 1995; Illes et al.,

1999). In this paper, we report on a functional magnetic resonance

imaging (fMRI) study that investigates how the bilingual brain

processes L1 and L2.

Previous studies of bilinguals have considered various facets of

language processing, including phonological, lexical, and sentential

processing. Recent neuroimaging studies on bilingual sentence

comprehension have yielded relatively consistent results. In

previous studies on bilinguals, age of acquisition and proficiency

level have been considered to be the main factors that cause different

brain activation patterns between L1 and L2. In an fMRI study of

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http://dx.doi.org/10.1016/j.neuroimage.2005.09.066

(3) John-ga Mary-wo home-ta.

John-NOM Mary-ACC praise-PAST

‘‘John praised Mary.’’

(4) Mary-ga John-ni home-rare-ta.

Mary-NOM John-DAT (by) praise-PASS-PAST

‘‘Mary was praised by John.’’

S. Yokoyama et al. / NeuroImage 30 (2006) 570–579 571

early Mandarin-to-English bilinguals acquiring the two languages

simultaneously, Chee et al. (1999) investigated whether the

bilinguals showed identical activation patterns for L1 and L2 in a

visually presented sentence comprehension task. The study revealed

no significant difference in activation patterns for L1 and L2. By

contrast, in a study of late Mandarin-to-English bilinguals acquiring

L2 later than L1, Luke et al. (2002) found that compared to

Mandarin, English produced greater activation in the left frontal

region during a syntactic error detection task; and greater activation

in the superior temporal region during a semantic error detection

task. Wartenburger et al. (2003) compared Italian-to-German

bilinguals on syntactic and semantic error detection tasks. The

subjects varied in age of acquisition and proficiency; the three

groups were high-proficiency early bilinguals, high-proficiency late

bilinguals, and low-proficiency late bilinguals. Early bilinguals

showed no significant difference between L1 and L2 in either the

syntactic or the semantic error detection task. By contrast, among

late bilinguals, L2 elicited greater activation in the left frontal and

parietal areas than L1, regardless of proficiency level. Furthermore,

Wartenburger et al. (2003) found that low- versus high-proficiency

late bilinguals showed different activation patterns. Based on these

observations, wemay assume that age of acquisition and proficiency

are the main factors that determine the pattern of brain activation in

L1 and L2 processing among bilinguals.

However, a recent neuroimaging study on bilingual sentence

comprehension (Hasegawa et al., 2002) lets us speculate that

sentence complexity may be an additional factor affecting differ-

ences in activation between L1 and L2. Hasegawa et al. (2002) based

their study on the findings of Carpenter and Just (1975) and

Carpenter et al. (1999), who reported that a negative sentence

requires more processing than its affirmative counterpart. Hasegawa

et al. (2002) compared the comprehension of negative versus

affirmative sentences among Japanese-to-English late bilinguals.

They reported that English (L2) negative sentences showed greater

activation than their affirmative counterparts in the left inferior

frontal, superior/middle temporal, and parietal cortices. Interesting-

ly, however, Japanese (L1) negative sentences produced no more

activation than Japanese affirmative sentences, suggesting that

structurally complex sentences may be processed differently in L1

and L2.

In the present study, we compared late bilinguals’ processing of

structurally simple versus complex sentences in Japanese (L1) and

English (L2). For this purpose, we compared brain activity during

the processing of active and passive sentences within each language.

We chose to compare active and passive sentences because the

Japanese direct passive semantically parallels the English passive

(Shibatani, 1990). Furthermore, as explained in detail below, the

syntactic differences between active and passive sentences in both

English and Japanese are similar.

Most languages mark the passive by a change in both the verb

form and the relative order of the agent and the theme (cf. Shibatani,

1990; O’Grady and Dobrovolsky, 1996). As shown in (1) and (2)

below, the English passive sentence has three distinct properties

(‘‘AUX’’, ‘‘PAST’’, and ‘‘PASS’’ are abbreviations for auxiliary, past

tense, and passive, respectively).

(1) John praised Mary.

praise-PAST

(2) Mary was praised by John.

AUX-PAST praise-PASS

First, a passive sentence contains some form of the auxiliary

verb ‘‘be’’, together with a verb in the past participle form, which is

normally marked by the suffix -ed or -en. Second, the order of the

agent and the theme is reversed in passive sentences relative to

active sentences. While the agent precedes the theme in active

sentences, the theme precedes the agent in passive sentences. The

final property of the English passive is that the agent occurs as an

oblique in a by-phrase.

The analogous situation occurs with the Japanese direct passive

sentence. As shown in (3) and (4) below, the Japanese direct

passive has three defining properties that are similar to those of the

English passive (‘‘NOM’’, ‘‘ACC’’, and ‘‘DAT’’ are abbreviations

for nominative, accusative, and dative, respectively).

First, a direct passive sentence encodes the passive voice with a

morpheme (ra)re on the verb. Second, the relative order of

thematic roles is reversed. Third, the agent occurs as part of a noun

phrase with an oblique case, which is marked by -ni in direct

passive sentences (cf. Shibatani, 1985). Thus, a Japanese direct

passive sentence is very similar to an English passive sentence.

It is important to note, however, that English and Japanese

passives differ in a number of ways. For example, Japanese has

three passive constructions: the direct passive, the indirect passive,

and the possessive passive; while English has only one passive

construction. Also, English uses psychological verbs in the passive

form (e.g., I am frightened), while Japanese does not. Keeping

these differences in mind, in our study, we restricted our stimuli to

Japanese direct passive sentences and English passive sentences

without psychological verbs.

In the present study, we compared brain activity during the

processing of active and passive sentences within each language to

determine whether the comprehension of structurally complex

sentences differs in L1 and L2. If we find different activation

patterns for Japanese and English, our hypothesis that structurally

complex sentences are processed differently in L1 and L2 will be

supported.

In addition, we statistically excluded the effect of task difficulty

as a confounding covariate in the analysis of covariance

(ANCOVA) when we directly compared the comprehension of

L1 and L2. We took this measure to address the points raised by

Hasegawa et al. (2002), who suggested that task difficulty or

workload generates different cortical representations during the

comprehension of L1 versus L2. Based on Hasegawa et al. (2002),

we speculate that when the effect of task difficulty is statistically

excluded, there will be no difference in the activation pattern of the

left hemispheric language-related regions in the comprehension of

L1 and L2.

Materials and methods

Participants

Thirty-six university students (30 males and 6 females; aged

between 18 and 29 years; the mean age of the participants was 21.1

S. Yokoyama et al. / NeuroImage 30 (2006) 570–579572

years) participated in this study. All participants were native

Japanese speakers, and all were right-handed, as assessed by the

Edinburgh Handedness Inventory (Oldfield, 1971). None of the

participants displayed any signs, or had any previous history of,

medical or neurological diseases. We obtained written informed

consent from each participant in accordance with the guidelines

approved by Tohoku University and the Helsinki Declaration of

Human Rights, 1975. The mean age and length of acquisition of

English (L2) for these participants were 11.8 (range = 8–13, SD =

1.4) and 9.2 years (range = 6–17, SD = 2.6), respectively. Thus, all

participants were late bilinguals. We assessed the participants on the

basis of the pre-level 2 English Language Proficiency test, which

was prepared by the Society for Testing English Proficiency. This

test, which includes listening and reading components, is generally

used to assess the proficiency of English as a foreign language in

Japan. The test has seven grades: one, pre-one, two, pre-two, three,

four, and five; five refers to the lowest level of proficiency, and one

to the highest. At pre-level 2 proficiency, the level selected for the

participants in this study, speakers are assumed to have a sufficient

level of comprehension and production to participate in daily life in

English. The mean scores in the listening and reading sections of the

proficiency test were 66.9% (range = 60.0–92.5, SD = 13.4) and

90.1% (range = 80–100, SD = 6.9), respectively. The mean total

score for the test was 78.6% (range = 66–92, SD = 8.4).

Materials

The experimental stimuli were 72 short sentences, half of which

were Japanese, and half English. For each language, 12 sentences

were semantically plausible, 12 sentences were semantically

implausible, and the remaining 12 were control stimuli. Of the

plausible and implausible sentences, half were active and half were

passive. All sentences consisted of three phrases: two noun phrases

and one verb phrase. We used translation equivalents in both

languages to ensure a comparable lexical level. Table 1 contains

some examples.

We composed the stimulus sentences as follows. For the

English sentences, we chose nouns and verbs generally used at

the junior high school level to ensure the participants’ familiarity

with them. We then translated the selected words into Japanese

and checked and controlled for frequency using the database

developed by Amano and Kondo (1999). Prior to the fMRI

experiment, we performed a lexical decision screening test to

eliminate any lexical items that would be difficult for learners of

English as a second language to process. Ten additional healthy

right-handed subjects (aged between 20 and 26 years; the mean

age of the participants was 22.3 years) participated in this test.

The mean reaction time (SD) for selected words was 1248 (258)

ms. The control stimuli consisted of three nouns or verbs that

were included in the stimulus sentences. We did not present the

Table 1

Examples of stimuli used in the present experiment

Sentence type Example

Plausible active sentence The hunter/shot/the deer

Plausible passive sentence The deer/was shot/by the hunter

Implausible active sentence The deer/shot/the hunter

Implausible passive sentence The hunter/was shot/by the deer

Control stimulus The deer/the hunter/the deer

control stimuli in a sentential context. While half of the stimuli

were identical, the remaining half were not.

Task procedure

We presented the stimuli visually in a phrase-by-phrase

manner on a black projection screen. Fig. 1 illustrates this

procedure. Following an initial resting period (12 s), the stimuli

were presented in epochs lasting 28 s (18 epochs, pseudo-

randomized), followed by a 28-s resting period, during which a

fixation cross was presented. Prior to each epoch, an instruction

word was presented for 1 s (e.g., ‘‘bun’’, which means ‘‘sentence’’

in Japanese, for the sentence epoch; or ‘‘tan’’, which means

‘‘word’’ in Japanese, for the control epoch). Each epoch contained

four randomized trials. Each phrase was presented for 1 s.

Intervals for switching screens were inserted between phrases.

Plausible and implausible sentences were presented in the

sentence epoch. Immediately after the presentation of the third

phrase of a sentence, a fixation cross was displayed for a period

of 3.8 s. During this period, subjects were asked to press the left

button with their index finger if the sentence was plausible, and

the right button with their middle finger if the sentence was

implausible. Therefore, the intervals between the subject’s

response and the start of the next trial varied in relation to the

subject’s reaction time. In the control epoch, three noun phrases

or verb phrases were sequentially presented in a randomized

order. These phrases did not comprise a sentence. After the

presentation of the third phrase of these stimuli, a fixation cross

lasting 3.8 s was displayed. Subjects were then asked to press the

right button if the presented phrases were identical, and the left

button if the phrases were not identical. This control condition

was intended to control for the effects of visual input, working

memory, word recognition, and motor output. The order of the

conditions, such as the Japanese active, passive, and control, and

the English active, passive, and control conditions, was pseudo-

randomized and counterbalanced across subjects. We conducted a

brief practice session before performing the fMRI in order to

familiarize the participants with the task involved in the study.

This practice session consisted of 10 trials that were similar to the

task performed in this study.

fMRI data acquisition

We performed the fMRI on a 1.5 T Siemens Symphony

scanner (Siemens, Erlangen, Germany) at Tohoku University.

Head motion was minimized by placing pillows and cushions

around the head. Forty-two axial slices (thickness, 3 mm; FOV,

192 mm; data matrix, 64 � 64 voxels; in-plane resolution, 2 �2 mm) were acquired every 4 s during functional measurements

(BOLD-sensitive gradient EPI sequence; TR = 4000 ms; TE =

50 ms; flip angle = 90-). The seven initial scans were dummy

scans that were used to equilibrate the state of magnetization

and were excluded from the analysis. After the functional

imaging, anatomical images of T1-weighted MDEFT images

(thickness, 1 mm; FOV, 256 mm; data matrix, 192 � 224; TR =

1900 ms; TE = 3.93 ms) were also acquired from all

participants.

The accuracy rate and response time for all tasks used as

behavioral data were collected using a Windows-based com-

puter, which was used in the presentation of the stimuli for the

tasks.

Table 2

Behavioral data

Accuracy

rate (%)

SD Reaction

time (ms)

SD

Japanese active 95.5 21 1435 631

Japanese passive 94.9 17 1659 709

English active 91.6 26 1492 761

English passive 88.8 32 1692 902

Fig. 1. Procedure followed in the present experiment.


Data analysis

The fMRI time-series data were analyzed using SPM99

implemented on MATLAB (The Mathworks Inc., Natick, MA).

The data were realigned, spatially normalized to the standard brain

space, and smoothed with an isotropic Gaussian kernel of 9 mm

full width at half maximum using a standard SPM method (Friston

et al., 1995), and a high-pass frequency filter (128 s) was applied.

The time series were modeled using box-car regressors for each

epoch and convolved with the hemodynamic response function.

For each subject, we computed contrasts among (a) Japanese active

sentences; (b) Japanese passive sentences; (c) English active

sentences; (d) English passive sentences; (e) the Japanese control

task; and (f) the English control task.

We computed group effects using these contrast images with

the random effect model. Since the reaction time and the

accuracy rate exhibited significant statistical differences among

conditions (see Results), we included these values as a

confounding covariate in the ANCOVA in order to compensate

for the effect of task difficulty. Although there is a confound

involved in the different time intervals between the presentation

of active and passive sentences in both English and Japanese, we

assume that this confound corresponds to reaction time. An

anatomical location was identified using a template created by

Talairach and Tournoux (1988). In the contrasts of L1 plus L2

versus their controls and in the comparisons between L1 and L2,

a threshold was set at P < 0.05, corrected. In the comparisons of

task versus control conditions and task versus task conditions, a

threshold of P < 0.001, uncorrected, was established. Although

we did not perform correction for multiple comparisons in these

task versus task comparisons, we believe that the statistical results

were nevertheless conservative since these analyses employed the

random effect model.

However, we also performed ROI analyses to confirm statistical

significance and to determine the characteristics of each activated

area. In order to compare the intensity of activation, we defined

ROIs as the significantly activated clusters when contrasting

‘‘Japanese passive’’ versus ‘‘Japanese active’’ and ‘‘English

passive’’ versus ‘‘English active’’ (cf. Miura et al., 2005). Mean

percent signal changes were calculated in each ROI for each

subject in each condition. ANOVAs were conducted for all

conditions, and a post hoc multiple comparison (Bonferroni

method) was performed.

The data regarding accuracy rate and response time for all tasks

were analyzed by the analysis of variance (ANOVA). The data

were analyzed by ANOVA, and a post hoc multiple comparison

(Bonferroni method) was performed. When there was a significant

difference among conditions in the behavioral data, we performed

correlation analysis between the values of percent signal changes in

each ROI and the behavioral data, in order to confirm whether

there was a significant correlation between behavioral data and

brain activity for each ROI.

Results

Behavioral data

Table 2 summarizes the accuracy rate and reaction time. The

difference in the accuracy rates between the active and passive

sentence conditions was not statistically significant (P > 0.1), but

there was a significant difference between the Japanese and

English conditions (P < 0.001). In the post hoc analysis, there

was a significant difference between Japanese and English in both

the active and passive sentence conditions (P < 0.01 and P < 0.001

for active and passive sentences, respectively). The difference in

Table 4

Brain regions activated in the comparison between Japanese as L1 and

English as L2

L/R Anatomical region T x y z

Japanese versus control condition

L Inferior frontal gyrus 6.44 �42 24 �18L Inferior frontal gyrus 4.99 �56 26 �2L Premotor area 7.72 �42 24 18

L Premotor area 7.72 �42 24 18

L Superior temporal gyrus 8.28 �56 �38 �2L Middle temporal gyrus 8.28 �56 �38 �2L Inferior parietal lobule 6.58 �48 �56 48

L Inferior parietal lobule 6.5 �40 �58 30

L Lingual gyrus 5.69 �12 �102 0

R Posterior lobule of the cerebellum 5.57 14 �84 �30R Posterior lobule of the cerebellum 4.69 34 �78 �30

English versus control condition

L Inferior frontal gyrus 6.41 �50 26 20

L Inferior frontal gyrus 6.24 �50 20 �4L Premotor area 7.24 �46 6 30



L Lingual gyrus 7.02 �10 �92 �6R Posterior lobule of the cerebellum 8.23 14 �80 �16R Posterior lobule of the cerebellum 8 48 �68 �28

Japanese versus English

No data obtained

English versus Japanese

L Fusiform gyrus 4.09 �28 �92 �8L Posterior lobule of the cerebellum 4.99 �6 �82 �28L Posterior lobule of the cerebellum 3.91 �32 �76 �22Details are the same as those provided in Table 3.


the response times between Japanese and English was not

statistically significant (P > 0.1). There was a significant difference

between the active and passive sentence conditions (P < 0.001). In

the post hoc analysis, there was a significant difference between the

active and passive sentences for both the Japanese and English

conditions (P < 0.001 for each).

Imaging data

Table 3 summarizes the results of each language versus control

condition, direct comparisons between L1 and L2, and the contrast

of L1 plus L2 versus their controls. Table 4 summarizes the results

of each language versus control condition and the direct

comparison between the active and passive sentence conditions

for each language. As shown in Table 3 and Fig. 2, the activation

pattern in the left and right hemispheric regions did not differ; a

similar cortical network was used to comprehend L1 and L2.

However, as shown in Table 4 and Fig. 3, the left cerebellum and

the fusiform gyrus were more activated during the comprehension

of L2 compared to L1.

Table 5 and Fig. 4 show significant brain activations in

contrasts of the direct comparison. When compared to the Japanese

active sentence condition, the Japanese passive sentence condition

activated regions in the left premotor area, insula, pars triangularis,

and superior parietal lobule. Since these regions were activated in

the contrasts of the Japanese active and passive sentence conditions

versus the control condition, we can say that these regions were

more active during the processing of passive sentences than active

sentences. Compared to the English active sentence condition, the

English passive sentence condition activated regions in the left

inferior frontal gyrus and the right cuneus. Since these regions

were among those that were activated in the contrast of the English

active and passive sentence conditions versus the control condition,

we can say that they were more active during the processing of

English passive sentences than English active sentences. In both

Japanese and English contrasts, then, we found that passive

sentences elicited greater activation than active sentences, while

the reverse contrast showed no significant activation.

ROI analysis

We conducted ROI analysis for five regions of the brain; Fig. 5

shows the results of this analysis. In the ROI of the left pars orbitalis,

there was a significant interaction (P < 0.05) and a marginally

Table 3

Common activation pattern during comprehension of L1 and L2


Japanese and English versus their control conditions


L Medial aspect of the superior frontal gyrus 9.33 �6 8 56

L Inferior frontal gyrus 10.2 �44 46 �10L Middle temporal gyrus 7.26 �60 �38 �4L Inferior parietal lobule 13.4 �34 �58 46

R Superior frontal gyrus 10.2 6 16 52

R Inferior frontal gyrus 11 44 46 �18R Inferior parietal lobule 10.5 34 �58 46

R Posterior lobule of the cerebellum 9.7 12 �80 �26R and L indicate right and left hemispheres, respectively. x, y, and z

represent Talairach and Tournoux coordinates (Talairach and Tournoux,

1988).

significant main effect for the active and passive contrast (P < 0.1),

but not for the Japanese and English contrast (P = 0.55).With respect

to the multiple comparison results, we found a significant effect only

for the English passive and English active contrast.

In the left pars triangularis, there was a significant main effect

for the active and passive contrast (P < 0.05) and a marginally

significant effect for the interaction (P < 0.1), but not for the

Japanese and English contrast (P = 0.59). The multiple compar-

isons show that signal intensity was significantly lower during the

Japanese active sentence condition compared to the three other

conditions.

In the left premotor area, there was a significant main effect for

the active and passive contrast (P < 0.05), but not for the Japanese

Fig. 2. Brain activation indicating all conditions versus their control

conditions (Japanese active and passive as well as English active and

passive sentence conditions with the exception of Japanese and English

control conditions). Left and right indicate the left and right hemi-

spheres, respectively.

Fig. 3. Brain activation indicating the difference between Japanese and

English (the English active and passive sentence conditions with the

exception of Japanese active and passive sentence conditions). The figure

on the left side indicates the left hemisphere. In the figure on the right side,

the left side indicates the left hemisphere.

Table 5

Brain regions activated in the comparison among Japanese active, Japanese

passive, English active, and English passive sentence conditions


Japanese active versus control condition

L Inferior frontal gyrus 6.44 �42 24 �18L Inferior frontal gyrus 5.85 �44 22 �32L Inferior frontal gyrus 4.99 �56 26 �2L Premotor area 4.45 �40 22 22


L Middle temporal gyrus 5.75 �54 �38 �2L Superior temporal sulcus 3.94 �58 �50 12


L Intraparietal sulcus 4.4 �40 �64 38

R Posterior lobule of the cerebellum 5.57 14 �84 �30R Posterior lobule of the cerebellum 4.69 34 �78 30

Japanese passive versus control condition

L Inferior frontal gyrus 6.87 �44 28 �18L Middle frontal gyrus 5.85 �42 22 28

L Middle frontal gyrus 5.88 �54 30 10




L Superior frontal gyrus 3.86 �6 6 68


R Medial aspect of the superior frontal gyrus 3.99 4 32 48

L Middle temporal gyrus 5.8 �62 �42 0

L Middle temporal gyrus 4.06 �56 �28 �10L Insula 4.37 �32 28 �12L Fusiform gyrus 3.99 �40 �56 �12L Inferior parietal lobule 7.57 �42 �58 30

L Superior parietal lobule 6.39 �38 �70 48


R Posterior lobule of the cerebellum 9.39 14 �82 �32R Posterior lobule of the cerebellum 4.58 34 �82 �26


and English contrast (P = 0.15) and the interaction (P = 0.33). The

multiple comparisons show a significant difference only for the

Japanese passive and Japanese active contrast.

In the left insula, there was a significant main effect for the

active and passive contrast (P < 0.01), but not for the Japanese and

English contrast (P = 0.92) and the interaction (P = 0.47). The

multiple comparisons show a significant difference only for the

Japanese passive and Japanese active contrast.

In the left superior parietal lobule, there was a significant main

effect for both the active and passive contrast (P < 0.05) and the

Japanese and English contrast (P < 0.05), but not for the interaction

(P = 0.18). The multiple comparisons show that signal intensity is

significantly lower during the Japanese active sentence condition

compared to the three other conditions.

In the analysis of the correlation between the behavioral data

and the % signal change for each ROI, there was no significant

correlation for any of the ROIs in terms of accuracy rates or

response time. Table 6 summarizes the results of the correlation

analysis.

English active versus control condition

L Inferior frontal gyrus 4.45 �50 22 �2L Premotor area 4.21 �50 8 46


L Precentral gyrus 4.12 �36 0 40

L Middle temporal gyrus 3.86 �52 �40 �2R Posterior lobule of the cerebellum 4.02 32 �74 �32R Posterior lobule of the cerebellum 3.87 8 �82 �26L Posterior lobule of the cerebellum 3.68 �4 �82 �24

English passive versus control condition

L Inferior frontal gyrus 4.63 �44 24 �6L Inferior frontal gyrus 4.41 �46 22 �18L Premotor area 3.61 �48 6 38

L Superior frontal gyrus 4.4 �4 6 68

L Cuneus 3.91 �8 �88 �2R Posterior lobule of the cerebellum 5.5 12 �84 �22

Japanese passive versus active


L Inferior frontal gyrus: pars triangularis 3.9 �52 34 14


L Insula 3.62 �32 18 �4

English passive versus active

L Inferior frontal gyrus: pars orbitalis 3.91 �50 20 �10R Cuneus 4.48 �6 �88 0

Details are the same as those provided in Table 3.

Discussion

In this study, we directly compared late bilinguals’ processing

of Japanese (L1) and English (L2). We found that the language-

related regions were commonly activated during the processing of

both L1 and L2; and that when the effect of task difficulty was

statistically excluded, there was no difference in the activation

pattern of the hemispheric regions related to language function.

Thus, our fMRI experiment indicates that late bilinguals use a

similar neural basis to comprehend both L1 and L2. In contrast, we

compared the processing of Japanese direct passive sentences with

English passive sentences and found different activation patterns

between L1 and L2. These results support our hypothesis that late

bilinguals use language-related regions of the brain differently

when processing structurally complex sentences in L1 versus L2.

We discuss these results in more detail below.

Difference between L1 and L2

In contrast to previous neuroimaging studies, we found no

difference between L1 and L2 in the activation pattern of the

hemispheric regions related to language function, such as the left

inferior frontal, superior/middle temporal, and the parietal regions

(see Table 4 and Fig. 3). As described in the Introduction, previous

studies have reported greater activation in these areas for L2

compared to L1. Our study suggests that such results may be

Fig. 4. The upper figure shows the surface rendering of brain activation

during the processing of Japanese passive sentences when compared with

active sentences. The lower figure shows the surface rendering of brain

activation during the processing of English passive sentences when

compared with active sentences. In both the upper and lower figures, left

and right indicate the left and the right hemispheres, respectively.


attributable to task difficulty, as hypothesized in Hasegawa et al.

(2002). Hasegawa et al. (2002) suggested that greater activation in

the language-related regions during the comprehension of L2 is

related to task difficulty, which in turn is related to differences in

speakers’ fluency and/or proficiency in L1 and L2. In this study,

we attempted to exclude the effect of task difficulty by using

ANCOVA; as a result, we found no difference between L1 and L2

in the activation pattern in the language-related regions. Further-

more, as shown in Fig. 2, the language-related regions were

commonly activated during the comprehension of both L1 and L2.

These results support our hypothesis that task difficulty elicits

greater activation during sentence comprehension in L2 than in L1.

Taken together, the results of this and previous studies suggest that

among both late and early bilinguals, L2 is essentially processed in

similar left hemispheric language-related regions, and that cortical

representation reflects task difficulty in sentence comprehension.

Although we found no difference between L1 and L2 in the

activation patterns of the language-related regions, other factors

may account for the conflicting results of this and previous studies.

The first possible factor is that we used relatively easy sentences as

stimuli. As explained in Materials and methods, we used very high

frequency words. Additionally, the stimuli consisted of three

phrases– two noun phrases and one verb phrase. If we had used

more complex words and sentences as stimuli, we may have

obtained different results. The second factor is that while we

statistically excluded the effect of task difficulty, we did not control

it. Thus, further studies are necessary to determine if late bilinguals

process L1 and L2 differently when the effect of task difficulty is

controlled.

In this study, direct comparisons of L1 and L2 showed that L2

produced greater activation in the left cerebellum than L1, as

shown in Table 4 and Fig. 3. Although the role of the cerebellum

has traditionally been consigned to motor function, previous

neuroimaging studies on bilinguals have reported activation in

this region (Pillai et al., 2004). In subsequent studies, late Spanish-

to-English bilinguals were asked to perform semantic and

phonological tasks. The results showed greater activity in the left

cerebellum for L2 as compared to L1. As explained by Pillai et al.

(2004), the left cerebellum may have a language-related function, a

possibility that is also suggested by Lechtenberg and Gilman

(1978), who reported that lesions of the left cerebellum cause

muscular speech control. However, we cannot identify the role of

the left cerebellum in late bilinguals’ comprehension of L2, since

relatively few data are available to document its activity in this

context.

Difference between the processing of passive sentences in L1 and

L2

In this study, we found different activation patterns between

L1 and L2 in the processing of passive versus active sentences

(see Fig. 5). These results support our hypothesis that

structurally complex sentences produce a different pattern of

involvement in L1 versus L2 in language-related brain regions.

We observed significant interaction between sentence type

(active versus passive) and language (Japanese as L1 versus

English as L2) in the left pars orbitalis; and significantly greater

activation in the left pars triangularis and parietal cortex during

the processing of Japanese passive versus active sentences. We

did not find this pattern of activation for English. We discuss

these results below.

First of all, it is reasonable to consider whether differences in

sentence length were partially responsible for the different cortical

activation patterns found for active and passive sentences, given

that passive sentences are longer than active sentences in both

Japanese and English. However, if sentence length was a factor, we

would expect the same regions to be activated in comparisons of

both the Japanese active and passive sentences, and the English

active and passive sentences. In this study, we observed different

activation patterns in these two comparisons and no regions which

were commonly activated. Thus, while we cannot completely

exclude the effect of sentence length, it is unlikely that the different

activation patterns we found are attributable to this factor.

Second, in our ROI analysis, we found a significant interaction

between sentence type and language in the left pars orbitalis. In

addition, this region was more active during the comprehension of

English passive sentences compared to their active counterparts,

while Japanese active and passive sentences showed no such

difference. Thus, the left pars orbitalis is sensitive to the difference

between an active and passive sentence in English, but not in

Japanese. It could be, as suggested by Devlin et al. (2003), that the

activation in the left orbitalis is associated with semantic

processing. However, if this is so, the same activation patterns

would have been observed in comparisons of active and passive

sentences in both Japanese and English, since the Japanese direct

passive semantically parallels the English passive. Our finding

obviously eliminates this possibility. It is possible that the

activation in the left pars orbitalis is related to morphological

Fig. 5. Results of ROI analysis. ‘‘JA’’, ‘‘JP’’, ‘‘EA’’, and ‘‘EP’’ are abbreviations for Japanese active, Japanese passive, English active, and English passive

sentence conditions, respectively. The yellow and red bars in the graphs show the results of percent signal change of intensity in the active and passive sentence

conditions, respectively. The figure showing surface rendering of brain activation and the transversal slice show the regions of interest. The regions of the left

premotor area, insula, and pars triangularis were detected in a direct comparison between the Japanese passive versus Japanese active conditions. The region of

the pars orbitalis was detected in a direct comparison between the English passive versus English active conditions.


processing of the auxiliary ‘‘be.’’ Unlike their active counterparts,

English passive sentences require an auxiliary verb; conversely,

Japanese active and passive sentences do not contrast in their use

of auxiliary verbs. The auxiliary ‘‘be’’ requires morphological

processing related to subject–verb agreement in person and

number. Thus, morphological processing likely accounts for the

different activation patterns found in the left pars orbitalis for

Japanese and English. This view is in line with previous neuro-

imaging studies, which reported that processing of morphological

agreement activates the left inferior frontal cortex (e.g., Moro et al.,

2001; Miceli et al., 2002).

Table 6

Results of correlation analysis between behavioral data and % signal

change

ROI Response time

and % signal change

Error rate and

% signal change

Orbitaris P = 0.84 P = 0.87

Triangularis P = 0.69 P = 0.95

Premotor P = 0.85 P = 0.77

SPL P = 0.93 P = 0.88

Insula P = 0.6 P = 0.99

Orbitaris, Triangularis, Premotor, and SPL denote pars orbitaris, pars

triangularis, Premotor area, and superior parietal lobule, respectively.

Third, we found greater activation in the left pars triangularis

and parietal regions during the processing of Japanese passive

sentences relative to their active counterparts, but no significant

difference for English (see Fig. 4). These different activation

patterns may be explained by differences in thematic role

assignment in head-initial versus head-final languages. In a

head-final language like Japanese, the head (e.g., the verb) is

placed at the end of a clause or sentence. In a head-initial

language like English, the head (e.g., the verb) does not appear

at the end of a clause or sentence (it does not necessarily

appear initially; however, it appears earlier in the clause or

sentence than it would in a head-final language). According to

the incremental processing model (Inoue and Fodor, 1995;

Mazuka and Itoh, 1995; Kamide and Mitchell, 1999; Miyamoto,

2002), clauses and sentences are processed incrementally, based

on the local information that becomes available with the

appearance of each word. In comparing Japanese and English,

we may assume that Japanese passive sentences require greater

reanalysis of thematic role assignment than English passive

sentences. In a Japanese active sentence, the noun phrase with

the agent role is generally assigned nominative case (i.e., the

agent is usually the subject), but in a passive sentence, it is the

patient role that receives nominative case. The incremental

processing model would predict, therefore, that passive senten-

ces require thematic role reanalysis (Mazuka and Itoh, 1995). In


addition, Japanese passive sentences require thematic role

reanalysis for all the components that appear before the head,

since the head verb appears at the end of the clause or sentence.

In contrast, in English passive sentences, only the subject

requires thematic role reanalysis, since the verb is preceded by

only one noun phrase. This difference between Japanese and

English is reflected in our data. We found that the left

triangularis and the parietal region were more active during

the comprehension of Japanese passive sentences compared to

their active counterparts, while the comparison of English

passive and active sentences showed no difference in activation

in these regions. If we assume that the left pars triangularis and

parietal cortex are both involved in thematic role assignment,

then our results are compatible with the incremental processing

model’s predictions with respect to thematic processing.

Accordingly, our results are consistent with the findings that

the left pars triangularis (Newman et al., 2003) and the parietal

region (Inui et al., 1998) are involved in thematic processing.

Fourth, the different activation patterns observed in our study

may be attributable not only to the differences in grammatical

construction discussed above, but also to participants’ L2

proficiency. The participants in our study were late bilinguals,

with greater proficiency in L1 than L2. They may have found it

difficult to learn L2 grammatical properties that were not present in

their L1. Thus, the different activation patterns we found may stem

from the interaction between differences in grammatical construc-

tion between L1 and L2 and the participants’ L2 proficiency.

Fifth, it must be noted that between-language interference may

occur in a study design like ours, where sentences in the same

language continue in a block. Although we counter-balanced the

order of blocks across subjects, we cannot completely exclude the

effects of between-language interference. To address this issue, in

future studies of bilingual sentence comprehension, an event-

related or ‘‘odd ball’’ paradigm may be preferable.

Conclusion

In this study, we used fMRI to investigate whether the

comprehension of structurally complex sentences generates differ-

ent activation patterns in L1 and L2. First, our results indicate that

L1 and L2 are processed in similar language-related regions, such

as the left inferior frontal, superior/middle temporal, and parietal

regions, and that there is no difference in the activation pattern in

these regions between L1 and L2 when the effect of task difficulty

is statistically excluded. These results suggest that late bilinguals

use a similar neural basis to comprehend both L1 and L2.

However, we also found different activation patterns for the

processing of passive sentences in L1 versus L2. Passive sentences

elicited greater activation than their active counterparts in the left

pars triangularis, the premotor area, and the superior parietal lobule

in Japanese, but not in English. Furthermore, we found a

significant interaction between sentence type (active versus

passive) and language (Japanese versus English) in the left pars

orbitalis, indicating that structurally complex sentences generate a

different pattern of involvement in these regions for L1 and L2. We

attribute this contrast in cortical representation to an interaction

between differences in grammatical construction between L1 and

L2, and L2 proficiency. Therefore, further neuroimaging studies on

late bilinguals’ comprehension of L1 and L2 should take into

account not only age of acquisition and L2 proficiency, but also

task difficulty and differences in grammatical construction between

L1 and L2.

Acknowledgments

We thank Professor Noriaki Yusa of Miyagi Gakuin

Women’s University and Associate Professor Masatoshi Koi-

zumi of Tohoku University for their helpful comments. We also

thank two anonymous reviewers for their helpful comments.

This study was supported by JST/RISTEX, R&D Promotion

Scheme for Regional Proposals Promoted by TAO, and the 21st

Century Center of Excellence (COE) Program (Ministry of

Education, Culture, Sports, Science and Technology) entitled ‘‘A

Strategic Research and Education Center for an Integrated

Approach to Language and Cognition’’ (Tohoku University).

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Cortical activation in the processing of passive sentences in L1 and L2: An fMRI study