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OPEN Neural underpinning of Japanese

particle processing in non‑native
speakers
Chise Kasai1,3,6, Motofumi Sumiya2,6, Takahiko Koike3,4, Takaaki Yoshimoto3,5, Hideki Maki1 &
Norihiro Sadato3,4,5*

Grammar acquisition by non-native learners (L2) is typically less successful and may produce
fundamentally different grammatical systems than that by native speakers (L1). The neural
representation of grammatical processing between L1 and L2 speakers remains controversial. We
hypothesized that working memory is the primary source of L1/L2 differences, by considering working
memory within the predictive coding account, which models grammatical processes as higher-level
neuronal representations of cortical hierarchies, generating predictions (forward model) of lower-
level representations. A functional MRI study was conducted with L1 Japanese speakers and highly
proficient Japanese learners requiring oral production of grammatically correct Japanese particles.
We assumed selecting proper particles requires forward model-dependent processes of working
memory as their functions are highly context-dependent. As a control, participants read out a visually
designated mora indicated by underlining. Particle selection by L1/L2 groups commonly activated the
bilateral inferior frontal gyrus/insula, pre-supplementary motor area, left caudate, middle temporal
gyrus, and right cerebellum, which constituted the core linguistic production system. In contrast, the
left inferior frontal sulcus, known as the neural substrate of verbal working memory, showed more
prominent activation in L2 than in L1. Thus, the working memory process causes L1/L2 differences
even in highly proficient L2 learners.

Although a growing body of research has been investigating the similarities and differences in linguistic process-
ing between native (L1) and non-native (L2) speakers, the issue still remains controversial. Some studies have
shown that the acquisition of grammar by late learners is typically less successful and produces less uniform, and
perhaps even fundamentally different grammatical systems than with L1 ­acquisition1,2. These studies argue that
the rule systems developed by late L2 learners do not necessarily conform to the principles that constrain native
grammar ­learners2–5. Conversely, evidence from several experimental studies indicates that late L2 learners can
achieve native-like ­processing6–9.
Two principal hypotheses have been expounded regarding L2 grammatical processing of sentence comprehen-
sion. Clahsen and Felser’s4,5 influential shallow structure hypothesis postulates that L2 learners adopt “shallow”
parsing with reduced sensitivity to grammatical information; thus, a different parsing process occurs from L1.
The second hypothesis assumes that L1/L2 parsing processing is similar and explains the differences therein,
in terms of inefficient lexical access routines or an increased burden on capacity-limited cognitive resources
such as working memory in L ­ 210–12. By specifying working memory function as memory retrieval, C ­ unnings13
argued that “a primary source of L1/L2 differences (in the grammatical process) lies in the ability to retrieve
information-constructed processing from memory”.
Working memory involves holding information in the mind and mentally working with i­ t14. "Working mem-
ory is critical for making sense of anything that unfolds over time, for that always requires holding in mind what
happened earlier and relating that to what comes later. Thus, it is necessary to make sense of written or spoken
language, whether it is a sentence, a paragraph, or longer"14. Working memory is a core executive function and
is defined as "a collection of top-down control processes used when going on automatic or relying on instinct or

1
Faculty of Regional Studies, Gifu University, Yanagido 501‑1193, Japan. 2Research Center for Child Mental
Development, Hamamatsu University School of Medicine, Hamamatsu 431‑3192, Japan. 3Division of Cerebral
Integration, National Institute for Physiological Sciences, Okazaki 444‑8585, Japan. 4Department of Physiological
Sciences, SOKENDAI (The Graduate University for Advanced Studies), Hayama 240‑0193, Japan. 5Research
Organization of Science and Technology, Ritsumeikan University, Kusatsu 525‑8577, Japan. 6These authors
contributed equally: Chise Kasai and Motofumi Sumiya. *email: [email protected]

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intuition would be ill-advised, insufficient, or impossible"14. Other core executive functions are inhibition and
cognitive ­flexibility14.
One approach to studying the issue of L1/L2 differences is by using a functional neuroimaging technique,
such as functional MRI (fMRI) or PET. Previous studies have indicated that L2 syntax requires a high processing
load and is represented in language-related ­areas8,15. For L1, the neural substrates of grammatical processing
comprise the frontal and posterior superior temporal regions and their connections via dorsal fiber ­pathways16–23.
However, recent neuroimaging and lesion studies suggest that grammar is inseparable from other aspects of
language comprehension (lexico-semantic processing)24,25. Thus, the study of L2 grammatical processing of
sentence comprehension requires a procedure that is able to investigate and manipulate the grammatical com-
ponent within sentence comprehension.
In this study, we investigated the mechanism of L2 grammar processing using Japanese particles. Japanese
is a head-final language with a subject-object-verb (SOV) word order, in which, particles are crucial in provid-
ing a thematic role to nouns within the sentence (e.g., agent, patient, location, goal)26,27. A particle is a suffix
represented by a Japanese hiragana character and is normally added to the end of a noun. As the head (verb)
is not stated until the end of the sentence, Japanese sentences are incrementally processed before the head is
­inputted28,29. As the information contained in a particle affects the prediction or anticipation of subsequent
­elements30,31, selecting the correct particle is essential for creating a comprehensible and grammatically accept-
able sentence in Japanese. To articulate such a sentence, speakers must select the appropriate particle. However,
the treatment of particles is difficult. Unlike English, in which the word order determines the grammatical role
of the noun in a sentence, in Japanese, the grammatical function is signaled through postpositional p ­ articles32.
For example, by adding the nominative case particle ga, the noun becomes a subject, and the accusative particle
o indicates that a noun is an object in a sentence. Although Japanese is an SOV language, the order is free because
the word order is not essential for assigning grammatical roles. Thus, a speaker needs to assign a correct particle
to assign a thematic role to the nouns. What makes particle selection especially difficult for L2 learners is that
the same particle is used for different purposes. For example, wa has two functions: to mark a theme or to mark
a contrasting element in a s­ entence33. Furthermore, in a colloquial form, particles are often o ­ mitted34. The lower
35
the level of formality, the more acceptable the particle omission ­is , and particles can be dropped when adjacent
to a ­verb36. Although numerous studies have investigated particle omission, not much is known about which
particle is omitted the most. Such context-dependent operations make L2 learning more difficult. Inaccurate
use of particles is seen among both Japanese ­children37 and proficient learners with years of language-learning
­experience38,39. Thus, correct particles usage is a known bottleneck for non-native learners, and are simultane-
ously well-suited to experimentally control the grammatical structures; further, minimal effort is required to
replace or omit them since they are represented with one mora.
The neural substrates of particle processing were first examined by Inui et al.40 in a discrimination task in
which they showed particles and non-particles without any other sentence information to native Japanese partici-
pants (e.g., X ga (particle) or X nu (non-particle)) and asked to judge whether they were particles. They compared
the results with those from a phonological discrimination task to conclude that the left inferior frontal gyrus
(IFG) was responsible for particle discrimination in Japanese. While the involvement of the left IFG in particle
processing has also been reported by other ­researchers41,42, they did not test the processing of the retrieval and
selection of an appropriate particle, which is relevant for communication. Furthermore, the neural underpin-
nings of particle processing by non-native Japanese learners have never been reported.
The current study attempted to fill the gaps in previous studies and aimed to test two contradicting hypoth-
eses on L2 grammatical processing. We recruited highly proficient L2 Japanese learners of various nationalities
residing in Japan, whose ability to produce particles was tested; native Japanese speakers comprised the L1
control group. Highly proficient L2 participants were chosen as a proof that Japanese particles are bottle necks
for learning the Japanese language. All participants were assigned a sentence completion task in which they
were instructed to select an appropriate particle (Fig. 1) (Grammar condition) orally and to simply read out an
underlined Japanese phonetic letter (Letter condition). Unlike the previous studies, we aimed to examine the
process of the actual language production.
We hypothesized that working memory is a primary source of L1/L2 differences in the grammatical ­process13.
Specifically, we operationalized working memory and executive function within the predictive coding account,
which is the most popular explanation for neuronal message p ­ assing43–46. In this account, neuronal representa-
tions in higher levels of cortical hierarchies generate predictions (forward model) of representations in lower
­levels44,45,47. The comparison of top-down predictions with representations at the lower level forms a prediction
error that is passed back up the hierarchy to update higher representations. This recursive exchange of signals
suppresses the prediction error at each level and provides a hierarchical explanation for sensory inputs that
enter at the lowest (sensory) level. The neuronal activity of the entire hierarchy encodes beliefs (or probability
distributions) over states in the world that cause sensations (e.g., my visual sensations are (likely) caused by a
face)48. Thus, perceptual inference is accomplished by minimizing prediction errors by changing the top-down
prediction. Active inference, in contrast, minimizes prediction errors by changing sensory inputs through action,
such as ­utterance49. According to a theoretical analysis of the relationship between working memory and active
inference, working memory is considered a process of evidence accumulation to inform action choices through
active ­inferences50. In the current study, we asked participants to select the most suitable Japanese particle to
fulfill a blank in a stimulus sentence, which is a working memory process.
Participants were given the following phrases, serially (Fig. 1),

࣓࡛࢝ࣛࡍ ࡕࡕ㸦 㸧 (1)

They had to re-order the phrases mentally,

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Figure 1.  Sequence of events in the task. Each trial comprised two phases: preparation and production. In the
preparation phase, the participant observed and listened to the predicate portion (Camera is). In the production
phase, the subject (This) my father was presented. Two conditions were prepared in this phase: when an empty
line was shown, the participant was required to utter a particle (Grammar condition). In this particular case,
no (the possessive case) was the correct answer. When a Japanese letter was presented with an empty line, the
participant was required to read out the letter (Letter condition). Activities during the task were modelled
with boxcar functions for each phase, except for the rest condition. The English phrases in the figure is for
explanatory purposes, and were not presented during the experiment.

ࡕࡕ㸦 㸧 ࣓࡛࢝ࣛࡍ (2)

and utter the most appropriate particle in the context (2), that makes grammatical sense.

ࡕࡕ㸦ࡢ㸧 ࣓࡛࢝ࣛࡍ (3)

The comparison of top-down predictions (forward model) with representations at the lower level (Sentence
(3)) forms a prediction error. The exploration of particles for active inferences continues until the minimum
prediction error is reached. Thus, according to predictive coding theory, working memory includes the active
inference process that minimizes prediction error. This formalization first enables the plausible interpretation of
the behavioral differences between L1 and L2: a longer RT represents more iterative processing to minimize the
prediction error. Second, it provides the explicit hypothesis regarding the neural representation of L1/L2 differ-
ence: our working memory hypothesis predicts the activation difference of L1/L2 in the verbal working memory
region. Third, this formalization shows how immersion works for learning L2: optimization of the forward model
can be accomplished by sharing the forward model through mutual interaction with active i­ nference48. Specifi-
cally, working memory in the present task consists of.

(a) Mentally holding the serially presented phrases, (1)

(b) Re-ordering them, (2)
(c) Retrieving the particle according to a prior probability distribution, (3)
(d) Comparison of (3) with a forward model to generate the prediction error.

The whole process from (a) through (d) is regarded as working memory, leading to the decision to move on
to the second round by inhibiting the preceding results to explore other candidate’s particles. Thus, the active
inference is one of the possible mechanisms of working memory, that is, minimizing the prediction error, lead-
ing to the decision process that depends on other executive functions such as inhibition and cognitive flexibility.
Within this predictive coding schema, the forward model of L2 is assumed to be less optimized than that of
L1; we hypothesized that L2 requires a longer reaction time (RT), and more workload on the working memory
is reflected by the more prominent activation of the verbal working memory region in the left inferior frontal
sulcus. This hypothesis derives from the fact that the lexical processes of L1 are almost automatic whereas those
of L2 require effort, implying the recruitment of the executive function. This difference corresponds to the
prediction error in the predictive coding schema: the smaller the error, the smaller the number of iterations of
active inference to minimize it. Within the context given by the two phrases, the optimal forward model of L1
weighted a few candidates of the particle from a variety of contextual options. In contrast, a less optimal forward
model of L2 cannot limit the candidates’ number of particles, resulting in longer reaction times. If the shallow
structure hypothesis (postulating L2 learners adopt “shallow” parsing with reduced sensitivity to grammatical
information—a different parsing process from L1) is correct, activation patterns in the particle-related area and
the left ­IFG40 will differ, and the working memory-related areas will show similar activation patterns.
In the present study, we conducted an fMRI experiment involving 23 healthy non-native learners of Japanese
and 25 healthy native speakers among Japanese adult volunteers. We employed a task in which each participant
was required to read out a particle by filling in a blank or reading a letter on the screen within the MRI scan-
ner. To investigate our hypotheses, we compared the RTs and error rates used to produce particles or letters

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Figure 2.  Behavioral results. Non-native learners demonstrated significantly (A) longer reaction times and (B)
higher error rates than native speakers. Data are presented as box plots and violin plot datasets for each group.

between native and non-native participants, and the associated neural processing by focusing on similarities
and differences.

Results
Behavioral results. We measured the RT of the produced particles and letters, and eliminated RTs from
further analysis of two native participants whose raw RTs in both conditions were longer than 2 standard devia-
tions (SDs) from the native group average. This was done as longer RTs indicated misunderstanding of the task
(N = 23; total in the non-native learners’ group). We also eliminated from further analysis, the data of one non-
native participant whose utterance could not be recorded due to a recording error (N = 21; total in the native
learners’ group). The results of the linear mixed-effects modelling for RT indicated that the interaction between
conditions and groups was significantly associated with performance (estimate = 0.12, SE = 0.017, t = 6.874).
There was also a significant main effect of conditions (estimate = 0.056, SE = 0.011, t = 4.938) and groups (esti-
mate = 0.071, SE = 0.025, t = 2.903) (Supplementary Table S5 and Fig. 2A). In addition to Fig. 2A, which shows
raw values of RT, the figure showing the log-transformed RT is shown in Supplementary Figure S1.

Error rate. We checked the error rate in the produced particles and letters. Results of linear mixed-effects
modelling for accuracy indicated that the interaction of conditions and groups was significantly related to
performance (estimate = −2.406, SE = 0.607, t = −3.963). There was also a significant main effect of conditions
(estimate = −3.151, SE = 0.34, t = −7.905) and groups (estimate = −2.305, SE = 0.392, t = −5.886) (Supplementary
Table S5 and Fig. 2B).
All graphs were prepared using the RainCloudPlots R-script51, which provides a combination of box, violin,
and dataset plots. In the dataset plot, each dot represents a data point. In the boxplot, the line dividing the box
represents the median of the data, while the ends of the box represent the upper and lower quartiles. The extreme
lines show the highest and lowest values excluding outliers.

Correlation between immersion length and behavioral performance. To investigate the relation-
ship between the performance and the contribution of experience of staying or living in Japan, we conducted
the correlation analysis between each participant’s full-immersion duration and performance in the non-native
group. We found that, as the length of stay in Japan increased, a participant’s error rate significantly decreased
(r = −0.52, p = 0.015), although there was no such significant relationship in the RT (r = 0.22, p = 0.328).

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Figure 3.  Regions associated with correct grammar processing. Brain activation was associated with grammar
processing (grammar > letter) in (A) non-native learners, (B) native speakers, (C) the conjunction of non-native
learners and native speakers, (D) non-native learners greater than native speakers, and (E) native speakers
greater than non-native learners. The level of activation was set at a threshold p-value of < 0.05 and the FWE was
corrected for multiple comparisons over the whole brain, with the height threshold set at a p-value of < 0.001
(uncorrected).

Functional MRI results. The whole brain analysis with contrasts of (grammar > letter) revealed significant
activation in the bilateral IFG/insula and superior frontal gyrus (SFG) corresponding to the supplemental motor
area/middle cingulate cortex, caudate, left middle frontal gyrus (MFG)/precentral gyrus, left middle temporal
gyrus, and bilateral cerebellum in non-native learners (Fig. 3A and Table 1) and in the bilateral IFG/insula, SFG
(supplemental motor area)/middle cingulate cortex, caudate, left middle temporal gyrus, and bilateral cerebel-
lum in native speakers (Fig. 3B and Table 1).
The conjunction analysis with the contrasts of (grammar > letter) in native speakers and non-native learners
revealed significant activation in the bilateral IFG/insula, left SFG (supplemental motor area)/middle cingulate
cortex, left caudate, left middle temporal gyrus, and right cerebellum (Fig. 3C and Table 2).
In the comparison of (grammar > letter), non-native learners showed higher activation in the cluster includ-
ing the left IFG and MFG on the left inferior frontal sulcus (LIFS) (Fig. 3D and Table 3) than native speakers.

Discussion
In this study, we compared the role of working memory processes among native and highly proficient adult learn-
ers of Japanese. In terms of behavior, as expected, we found a longer RT and a higher error rate in non-native
learners than in native speakers when producing particles. According to predictive coding theory, a shorter RT
in native speakers (Fig. 2B) reflects faster processing of minimizing the prediction error. This may be related to
the forward model formation optimized to the context generated by the serially presented phrases. This process
may correspond to the context-dependent anticipation of correct particle candidates. C ­ unnings13 argued that the
primary difference in sentence processing between L1 and L2 was in the ability to retrieve lexical information,
known as lexical semantics, from memory. Thus, the differences may suggest that non-native learners acquired
sufficient lexical semantics to select particles correctly. Native speakers use a combination of the lexical semantics
of a noun phrase and its particles to anticipate upcoming arguments without awaiting the arrival of the v­ erb52.
As a forward model formation corresponds to the Bayesian inference with the prior ­probability53, native speak-
ers may predict the correct particles’ probability using a combination of the retrieved lexical semantics. Several
studies have suggested that L2 learners do not anticipate the upcoming arguments to the same extent as native
speakers ­do54–56. This does not necessarily mean they exhibit a lack of lexical semantics because the present

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MNI coordinates
Spatial extent test (mm) Location
Cluster size PFWE-corr x y z t value Side Area
In non-native learners
13,387 < 0.001 −3 8 64 5.95 L SFG
1 9 63 6.18 R SFG
−5 18 44 5.56 L mPFC
14 25 33 5.72 R MCC
23,272 < 0.001 − 34 −1 45 4.83 L Precentral gyrus
− 54 28 19 8.27 L IFG, triangular
− 46 15 6 5.92 L IFG, opercular
− 35 19 −1 6.75 L Insula
− 33 35 −2 5.12 L IFG, orbital
829 0.022 −3 − 15 13 3.70 L Thalamus
5112 < 0.001 40 26 7 4.97 R IFG, triangular
13 17 3 5.17 R Caudate
35 24 −1 5.96 R Insula
35 32 −5 4.07 R IFG, orbital
26 19 6 4.32 R Putamen
3748 < 0.001 − 50 − 41 7 4.99 L MTG
1013 0.008 − 11 12 7 5.54 L Caudate
− 11 6 0 4.77 L Pallidam
704 0.045 51 − 31 3 4.75 R STG
10,800 < 0.001 18 − 85 − 14 4.77 R Lingual gyrus
20 − 67 − 27 5.44 R Cerebellum VI
14 − 65 − 29 5.29 R Cerebellum Dentate
41 − 61 − 30 4.76 R Cerebellum Crus I
11 − 83 − 30 6.19 R Cerebellum Crus II
27 − 65 − 46 6.74 R Cerebellum VIIb
In native speakers
15,126 < 0.001 −9 21 46 6.50 L SFG
1 26 39 5.06 R mPFC
−3 26 38 5.29 L MCC
14 20 33 6.30 R MCC
− 12 28 29 4.97 L ACC​
21,757 < 0.001 − 55 27 18 6.31 L IFG, triangular
− 47 14 6 6.34 L IFG, opercular
− 33 19 −1 9.63 L Insula
− 46 17 −8 5.88 L IFG, orbital
− 46 20 − 15 5.83 L Temporal pole
12,286 < 0.001 38 19 13 4.55 R IFG, opercular
36 32 4 5.29 R IFG, triangular
37 22 −3 8.02 R Insula
48 24 − 10 4.79 R IFG, orbital
5067 < 0.001 3 −8 8 5.70 R Thalamus
− 11 9 5 4.82 L Caudate
11 13 4 4.93 R Caudate
7592 < 0.001 12 − 89 7 4.99 R Calcarine gyrus
−1 − 79 −7 4.29 L Lingual gyrus
21 − 87 − 13 5.92 R Lingual gyrus
13 − 82 − 34 5.95 R Cerebellum Crus II
1714 < 0.001 − 57 − 37 5 4.88 L MTG
1448 < 0.001 0 − 56 − 21 5.03 Cerebellum I−IV
5 − 55 − 26 4.52 R Cerebellum Fastigial
21 − 68 − 26 3.43 R Cerebellum VI
1 − 61 − 29 4.54 R Cerebellum Vermis VI
9 − 64 − 30 4.32 R Cerebellum Dentate
−1 − 59 − 32 4.38 L Cerebellum Vermis VIIIa
Continued

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MNI coordinates
Spatial extent test (mm) Location
Cluster size PFWE-corr x y z t value Side Area
744 0.036 34 − 67 − 23 3.95 R Cerebellum VI
45 − 57 − 29 4.04 R Cerebellum Crus I

Table 1.  Regions associated with processing in non-native learners and native speakers. Activation was set at
a threshold of p < 0.05 and FWE was corrected for multiple comparisons over the whole brain, with the height
threshold set at p < 0.001, uncorrected. The terms x, y, and z represent the stereotaxic coordinates (mm). R,
right hemisphere; L, left hemisphere; IFG, inferior frontal gyrus; SFG, superior frontal gyrus; ACC, anterior
cingulate cortex; MCC, middle cingulate cortex; mPFC, medial prefrontal cortex; MTG, middle temporal
gyrus; FWE, family-wise error; MNI, Montreal Neurological Institute.

study participants were highly proficient. Instead, the context-dependent forward model formation with lexical
semantics of L2 may not be as efficiently conducted as that of L1s. This notion is supported by the findings that
the staying experience of L2 in Japan significantly decreased the error rate. This finding is consistent with the
active inference account of communication. Friston and ­Frith57 argued that communication facilitates long-term
changes in the interacting individuals’ forward models by predicting and minimizing their mutual prediction
errors if these agents adopt the same forward model. Thus, the longer the stays within the areas where the L2 is
publicly used, the better adjusted the forward model is, resulting in lower error rates.
As for different brain regions for particle processing, when comparing non-native learners to native speak-
ers, the LIFS was more prominently activated. Note that the task difficulty of each test item within the group
was modelled (Fig. 3D). Thus, the differences in neural activation reflected differences in the processing of
sentence-building by selecting an appropriate particle between L1 and L2 participants, rather than its difficulty.
Furthermore, we focused on correct trials, excluding the incorrect response trials from the analysis. Thus, it is
unlikely that the additional brain regions recruited in the L2 group were related to error processing.
Several neuroimaging studies have reported separate functions within the inferior frontal c­ ortex58,59. As a core
region for grammar, the left IFG, and for non-grammar working memory, the LIFS, are dissociated from each
other within the inferior frontal cortex. For example, in the study by Makuuchi et al.59, an embedded sentence
structure was utilized to examine how multiple subject-noun phrases were stored before being processed. The
results provide direct evidence of dissociation, with the left pars opecularis (LPO) associated with core grammati-
cal computation and the LIFS associated with non-grammatical working memory. This finding was consistent
with a meta-analysis that determined that the mid-lateral prefrontal cortex clustering in and around the IFS is a
core region of the executive component of working m ­ emory60. Considering the slower response rate and lower
accuracy for grammatical processes among non-native learners in the present study, this group may have to select
the correct particle by going through multiple choices among all available particles, whereas native speakers have
fewer choices in the given context due to the accumulated prior experience and thus the choices are relatively
less complex. Although we did not directly show that L2 speakers went through multiple choices, through the
predictive coding schema, the elongated RT can be explained by the increased iteration of the retrieval. Thus,
the enhanced neural activity of the LIFS can be interpreted as the reflection of a larger prediction error and more
iterations of the retrieval. This is consistent with experience-based theories of the complexity difference of gram-
matical ­processes61–65, and our predictive coding account. Therefore, for non-native learners, the activation of
the LIFS may be associated with a greater workload on the working memory recruited for minimizing prediction
errors between the forward model and the retrieved particles. The LIFS is related to the post-retrieval selection
in resolving competition between simultaneously active r­ epresentations60,66.
In terms of common brain regions for particle processing, as compared to letter processing, the bilateral IFG/
insula, SFG/middle cingulate cortex, left caudate, left middle temporal gyrus, and right cerebellum were activated
in both native speakers and non-native learners, while selecting and uttering particles (Fig. 3C) that required
syntax computation and speech production. Our data confirmed that similar brain areas are recruited for particle
production as for grammatical p ­ rocessing67. The activation pattern is largely consistent with previous literature
indicating that these brain areas are fundamental to the processing of syntax ­production68,69.
Regarding grammatical processing, the previous studies are in agreement that the left IFG is particularly the
core ­region69–71 for hierarchical grammatical ­complexity72. Therefore, the activation of the left IFG for particle
processing could be interpreted by assuming a cognitive process that is routinely engaged when attempting to
comprehend linguistic input that is relatively challenging to understand due to its grammatical ­properties69.
Furthermore, although little activation of the right IFG has been reported for grammatical p ­ rocessing69, its
co-activation with the left IFG is observed in tasks that reflect linguistic expectations, that is, the prediction of
structural features of the expected linguistic i­ nput73–75. Therefore, in our task, which provides linguistic expecta-
tion and allows for retrieval of the particle as soon as the noun is presented, bilateral activation of the IFG may
be associated with grammatical surprise, reflecting the expectedness of the particle given its preceding context,
which allows the noun to be connected to the left c­ ontext74.
The activation of bilateral IFG included the activation of the bilateral insula within these clusters. A previ-
ous activation likelihood estimation (ALE) meta-analysis reported the involvement of the bilateral insula for
speech and language t­ asks76. For speech production, it has been suggested that the insula cortex functions as a
relay between the cognitive aspect of language and preparation for v­ ocalization77, particularly during difficult

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MNI coordinates
Spatial extent test (mm) Location
Cluster size PFWE-corr x y z t value Side Area
Non-native learners and Native speakers (conjunction analysis)
9040 < 0.001 2 14 60 5.26 R SFG
−4 19 45 5.51 L SFG
14 25 33 5.72 R MCC
13,334 < 0.001 −55 27 18 6.31 L IFG, triangular
−46 15 6 5.92 L IFG, opercular
−35 19 −1 6.75 L Insula
−33 35 −2 5.12 L IFG, orbital
711 0.043 −3 −15 13 3.70 L Thalamus
4416 < 0.001 40 26 7 4.97 R IFG, triangular
35 24 −1 5.96 R Insula
35 32 −5 4.07 R IFG, orbital
26 19 −6 4.32 R Putamen
879 0.016 −11 9 5 4.82 L Caudate
−11 6 1 4.60 L Pallidum
1308 0.002 −54 −36 5 4.56 L MTG
1764 < 0.001 18 −85 −14 4.77 R Lingual gyrus
20 −79 −20 3.46 R Cerebellum VI
17 −86 −28 3.84 R Cerebellum Crus I
13 −83 −32 5.32 R Cerebellum Crus II

Table 2.  Regions associated with grammar processing for non-native learners and native speakers. Activation
was set at a threshold value of p < 0.05 and FWE was corrected for multiple comparisons over the whole
brain, with the height threshold set at p < 0.001, uncorrected. The terms x, y, and z represent the stereotaxic
coordinates (mm). R, right hemisphere; L, left hemisphere; IFG, inferior frontal gyrus; SFG, superior frontal
gyrus; MCC, middle cingulate cortex; MTG, middle temporal gyrus; MNI, Montreal Neurological Institute.

Spatial extent test MNI coordinates (mm) Location

Cluster size PFWE-corr x y z t value Side Area
Non-native learners > Native speakers
752 0.034 −52 15 37 3.40 L MFG
−52 25 31 4.62 L IFG, opercular

Table 3.  Regions associated with more grammar processing in non-native learners or native speakers.
Activation was set at a threshold value of p < 0.05 and FWE was corrected for multiple comparisons over
the whole brain, with the height threshold set at p < 0.001, uncorrected. The terms x, y, and z represent the
stereotaxic coordinates (mm). R, right hemisphere; L, left hemisphere; IFG, inferior frontal gyrus; MFG,
middle frontal gyrus; MNI, Montreal Neurological Institute.

speech-language ­processing78. Therefore, for both native speakers and non-native learners, the bilateral insula’s
involvement in grammatical processing is attributed to an integrator of grammatical computation and speech
production through cooperation with other regions.
Another common region for native speakers and non-native learners was the pre-SMA, which is known to
be involved in word selection, encoding of word form, and control of syllable ­sequencing79,80. Furthermore,
the linguistic system relies on a bilateral dual ­structure23,81, while the pre-SMA is involved in the interaction
of right- and left-hemispheric function between prosodic representations of speech melody and rhythm in the
right hemisphere and the parsing of abstract grammatical constituents in the left ­hemisphere82. Therefore, the
pre-SMA may coordinate the activity of the bilateral IFG and insula to process an appropriate particle that needs
to be selected quickly. We also found activation in the left caudate and right cerebellum regions. In the planning
of speech production, the pre-SMA and basal ganglia such as the caudate is in concert with the cerebellum and
serve as a pacemaker to provide a basic temporal s­ tructure80.
As for the practical implications of the present study, our hypothesis was that proficiency in bilingualism
depends on the optimization of the forward model that can be accomplished by sharing it across individuals
through mutual communication. Thus, we found that the staying experience within Japan significantly decreased
the error rate. This finding is consistent with the active inference account of the communication. Friston and
­Frith57 argued that communication facilitates long-term changes in the interaction among an individual’s forward

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models by predicting that each could minimize their mutual prediction errors if these agents adopted the same
forward model. Thus, the longer the stay or experience in the areas where L2 publicly speaks the language, the
better adjusted is the forward model and the lower is the error rate. Thus, proficiency in bilingualism may be
understood as the optimized forward m ­ odel57 that can be improved by immersion in the L2-spoken region.
This study has some limitations. First, our task was not designed to test the predictive coding hypothesis per
se, and thus this study does not depict the complete structure of predictive codings, such as the representation of
the forward model which sends the top-down signals to the left IFS nor the lower representation of bottom-up
signals. Future study is warranted for the complete depiction of the hierarchical structure of the linguistic process.
In this task, we used seven types of particles containing one mora (one hiragana character), which were
selected from case particles, connecting particles, postpositional particles, conjunctive particles, as well as the
suffixes of adjectives and adverbs and parts of adverbs. The selection of the particles was based on the Mikiko
Iwasaki Systematic ­Japanese83, which focuses on the most effective method of teaching Japanese. Thus, the more
frequently the particle is used in our daily life, the more frequently the particle was tested in our experiment,
and for this reason, the number could not be controlled. Therefore, presentation of each type of stimuli was not
necessarily balanced. Thus, we could not examine differences in RT/error rates across different kind of particles,
which may reflect the difficulty associated with each type of particle for non-native participants.
We adopted an explicit particle comprehension task; thus, we could not infer any implicit processes. Within
the predictive coding schema, the implicit production of a particle implies applying a forward model without
active inference. Thus, we expect that the RT may be similar between L1 and L2. Conversely, the error rate
depended on the optimization of the forward model; thus, it was better in L1 than L2 participants. These expec-
tations can be tested in future studies.
In this study, because we did not intend to test any specific hypothesis regarding the L1 effects, the first lan-
guage of the L2 participants was not controlled and was varied (Table S1). The neural underpinning of L1 effects
on L2 performance warrants further study.
In conclusion, the Japanese particle selection task activated the LIFS, known as the neural substrate of verbal
working memory, and showed more prominent activation in L2 than in L1 subjects. In contrast, the core linguis-
tic production system of both L1 and L2 subjects was similarly activated. We conclude that the active inference
mediated by working memory causes differences in L1/L2 even among highly proficient L2 learners, supporting
the working memory hypothesis.

Methods
Participants. Twenty-three healthy non-native learners of Japanese aged between 19 and 44 years (9 men
and 14 women; mean age = 27.5 years; SD = 5.9 years) and 25 healthy native speakers of Japanese aged between
18 and 39 years (13 men and 12 women; mean age = 23.7 years; SD = 5.4 years) participated in the study (for
details, see Supplementary Tables S1and S2).
All subjects gave informed written consent to participate. The present study was approved by the ethics com-
mittee of Gifu University and the National Institute for Physiological Sciences and was in accordance with the
Declaration of Helsinki. All non-native learners who participated in the experiment had different demographic
background on self-reporting such as first language or length of stay in Japan (Supplementary Table S1). All
non-native learners had high Japanese proficiency. The majority had passed N1 level of the Japanese Proficiency
Test (JLPT), which is equivalent to the Common European Framework of Reference for Language (CEFR) C1
level. One participant had achieved the N2 level (CEFR B2), and another had achieved the N3 level (CEFR B1).
One participant undertook the Examination for Japanese University Admission (EJU) for International Stu-
dents, which assesses academic Japanese skills. Although the levels and types of tests differed, Japanese language
proficiency of the participants was ascertained to be sufficiently high for their participation in this experiment.
Their Japanese proficiency was verified just before the MRI experiment with the Minimal Test (M-Test;84) to
certify that they were able to complete the task. At this stage, one non-native participant was excluded due to
low score (lower than 2SD from the average within the non-native group) on the Japanese proficiency test. After
the elimination, we analyzed the data from 22 non-native participants aged 19–40 years (8 men and 14 women;
mean age = 26.8 years; SD = 4.8 years).
All participants were right-handed according to the Edinburgh Handedness ­Inventory85. None of the partici-
pant had a history of symptoms requiring neurological, psychological, or other medical care.

Experimental schedule. The study was conducted over two days for non-native participants, and one day
for native participants. We adopted a two-day schedule for non-native participants as they required more time to
understand instructions than native speakers. On day 1, the participants took the Japanese proficiency test, and
the experimental procedure was explained to them, which helped avoid withdrawal of participation in the actual
experiment on the day. The Japanese proficiency test was administered individually in a classroom setting with
an examiner present and lasted approximately 3 min. On day 2, the fMRI experiment was conducted. Before the
experiment, participants received experimental instruction. The fMRI experiment was divided into three runs.

Japanese proficiency test. We utilized the Minimal Test of participants’ Japanese p­ roficiency84 to certify
whether participants would be able to conduct our task. In this test, participants inserted one Japanese hiragana
character into a blank space in a sentence, while listening to a compact disc audio recording that narrated the
reading passages written on a test sheet; the whole procedure took approximately three minutes. The Minimal
Test contained 46 blanks, and the test sentences were created based on grammar items listed in the textbook,
Yookoso!86. The M-Test has shown correlations with traditionally used placement t­ ests84.

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Experimental task
Stimuli. Ninety Japanese sentences were selected as stimuli from material that was used for teaching Japa-
nese as a second ­language83 and each sentence was used twice in the grammar and letter conditions, respec-
tively (Supplementary Tables S3 and S4). In the grammar condition, participants were required to provide the
most appropriate particle to complete the sentence. Seven types of particles containing one mora (one hiragana
character) were selected from among case particles, connecting particles, postpositional particles, conjunctive
particles, as well as the suffixes of adjectives and adverbs, and parts of adverbs. Some sentences allowed several
alternatives as correct answers. For example, both wa and ga could be used as subject markers. Thus, as long as
the sentence was coherent, it was considered correct. In the letter condition, the participants were required to
simply read out a mora that was indicated by an underlined space.

Stimulus presentation. The participants lay in the MRI scanner with plugged ears and foam padding
around their heads. We used Presentation software (Neurobehavioral Systems, Albany, CA, USA) to present
visual and auditory stimuli and to record button responses. Visual stimuli were projected onto a half-transpar-
ent screen with a liquid–crystal display projector (CP-SX12000J; Hitachi Ltd., Tokyo, Japan). The participants
viewed stimuli via a mirror placed above the head coil. The viewing angle was sufficiently large for participants to
observe stimuli (13.1° [horizontal] × 10.5° [vertical] at maximum). The participants listened to auditory stimuli
through ceramic headphones (KIYOHARA-KOUGAKU, Tokyo, Japan). Their utterances were recorded with an
opto-microphone system (KOBATEL Corporation, Kanagawa, Japan) and their facial images were recorded with
an infrared camera (NAC Image Technology Inc., Tokyo, Japan). The video data were used to calculate the RT
and appropriateness of the particle produced.

MRI data acquisition. We used a 3 T whole-body scanner (Verio; Siemens Erlangen, Germany) with a
32-element phased-array head coil. To obtain T2*-weighted (functional) images in which a multiband echo-
planar imaging (EPI) sequence collected multiple EPI slices simultaneously and reduced the volume acquisi-
tion time (TA)87. We utilized the following sequences to cover the whole brain: repetition time (TR) = 5 s; echo
time (TE) = 30 ms; TA = 0.5 s; flip angle (FA) = 90°; field-of-view (FOV) = 192 mm × 192 mm; in-plane resolu-
tion = 3 mm × 3 mm; 42 3-mm axial slices with a 17% slice gap; and multiband factor = 6. We utilized a sparse
sampling design, in which the production phase was performed during the silences between image acquisitions,
to reduce effect of movement. A T1-weighted high-resolution anatomical image was obtained from each par-
ticipant (TR = 1.8 s; TE = 1.98 ms; FA = 9°; FOV = 256 mm × 256 mm; slice thickness = 1 mm) after the functional
imaging runs.

Task schedule. The participants performed three runs, each lasting 405 s (81 volumes per run). Each run
comprised 75 trials of 5 s each (375 s); the grammar and letter conditions were presented 30 times and the null
condition, which lasts for 5 s with a fixation, was presented 15 times in each run. We inserted a white cross for
15 s as a baseline before the first trial and for 15 s as a baseline after the last trial (375 + 30 = 405 s). Figure 1 shows
the task schedule for each trial. Each trial comprised two phases: preparation and production. In the preparation
phase, the predicate of the sentence was visually presented on the screen. At the same time, the stimulus sentence
was read aloud by the personal computer (PC). This phase lasted 1300 ms. In the production phase, an argument
(subject/object) required by the predicate or an adjunct, which did not conflict with the predicate, was presented
followed by a blank with a line that participants used to fill in with the correct particle in the grammar trial.
In the letter trial, the stimulus sentence was presented and contained an underlined letter (hiragana charac-
ter), indicating participants to read it out. The stimulus sentence was read aloud by the PC while being visually
presented on-screen. The audio lasted for approximately 308 to 889 ms. During this phase, the participants were
asked to produce the particle as soon as the audio finished. The participants were also required to either produce
a particle or read out an underlined letter by the time the next scan started. This phase lasted 3000 ms. The visual
stimuli changed into a cross fixation point after 1300 ms.

Behavioral data analysis. Error rate. We checked the error rate of the produced particles and letters
read out during the experiment, and double checked them after the experiment from the recorded video. For
the analysis, we used 30 sentences for each session to generate 90 sentences in total. Thus, 90 was the maximum
score for both the grammar and letter conditions.

RT. The RTs of the produced particles and readout letters were measured. The RT was set as the length of
time between the end of the PC sound and the onset of particle production/readout letter. Our video system
recorded both scanning sound and the participant’s voice while scanning. To calculate the RT, we first ordered
the two examiners to code the time between the end of the scan sound and the beginning of the participant’s
voice with Adobe Audition (Adobe Systems Inc., San Jose, CA, USA). Next, we automatically measured the
PC sound duration with an in-house script on MATLAB 2016b (MathWorks, Natick, MA, USA). Finally, we
determined the RT for each production from the average of times between two examiners by subtracting the two
components, the time of previous PC sound before production and the time between the sound and the end of
the scan sound (1500 ms, see Fig. 1). The reported time between these two examiners was highly reliable (inter-
rater reliability: kappa = 0.94). For the statistical analysis, we transformed the RT for each condition using log
transformation and calculated the differential value between them in each group, so that they would approach
a normal d ­ istribution88.

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Statistical analyses. Behavioral data, error rate, and RT were analyzed with linear mixed-effects modelling,
which allow for the inclusion of multiple participant-level and stimulus-level independent variables in a single
­analysis89. Analyses were conducted using mixed-effects models with crossed random effects for subjects and
items using the lme4 package (version 1.1–23) of R (version 3.6.0). P-values were determined using the lmerT-
est package, which employs the Saitterthwait approximation to compute degrees of freedom for the t-statistic
of fixed effects. The analysis included contrast-coded fixed effects for conditions (− 0.5 = Letter, 0.5 = Grammar)
and group (− 0.5 = Native, 0.5 = Non-native) in a 2 × 2 factorial design. Random effects were fit using a maximal
random-effects ­structure90. This included random intercepts for subjects and items, by subject random slopes for
conditions and by-item random slopes for group. Models were fit using a maximum likelihood technique. For
analysis, the RT was log transformed after adding one.

fMRI data analysis. Image processing and statistical analyses were performed using the Statistical Para-
metric Mapping package (SPM12; Wellcome Trust Centre for Neuroimaging, London, UK). The first functional
images were discarded in each run to allow the signal to reach a state of equilibrium. The remaining volumes
were used for subsequent analyses. To correct the participants’ head motions, we aligned the functional images
from each run to the first image and realigned them to the mean image once again after the first realignment.
Each participant’s T1-weighted anatomical image was co-registered with the mean image of all EP images for
each participant. The co-registered anatomical image was processed using a unified segmentation procedure
combining segmentation, bias correction, and spatial ­normalization91. Using the estimated normalized param-
eters, all functional images were spatially normalized to the template brain and resampled to a final resolution
of 1 × 1 × 1 ­mm3. The normalized EP images were filtered using a Gaussian kernel of 8 mm (full width at half-
maximum) in the x, y, and z axes.
Concerning fMRI data analysis, linear contrasts between conditions were calculated for individual partici-
pants and incorporated into a random-effects model to make inferences at the population ­level92.

Initial individual analysis. Following pre-processing, task-related activation was evaluated using a general
linear ­model93,94. The design matrix contained regressors of three fMRI runs. Each run included two regressors
of interest (grammar and letter) that were modelled at the onsets of the trial. The duration of each regressor was
5000 ms. These conditions were presented in a mixed sequence. Therefore, we adopted the event-related design.
The blood-oxygen level-dependent signal for all tasks was modelled with boxcar functions convoluted with the
canonical hemodynamic response function. We modelled the task difficulty of grammar processing that differs
between native and non-native groups. As task sensitivity is reflected in the error distribution, we added the
rate of incorrectness for each syntax within each group as the modulation term on the regressor of the grammar
condition. In addition, we only modelled correct trials for each participant to exclude the activation associated
with error (results from analysis with all trials were added and are reported in Supplementary Figure S2). Six
regressors of rigid-body head motion parameters (three displacements and three rotations) were included as
regressors of no interest. Two additional regressors, describing the intensities of the white matter and cerebrospi-
nal fluid were added to the model to account for image-intensity shifts attributable to the movement of the head
associated with utterance within the scanner. We also applied a high-pass filter with a cut-off of 128 s to remove
low-frequency signal components. Assuming a first-order autoregressive model, we estimated which serial auto-
correlation from the pooled active voxels with the restricted maximum likelihood (ReML) procedure to apply
to whiten the ­data95. No global scaling was performed. To calculate the estimated parameters, we performed a
least-squares estimation on the whitened data. The weighted sum of the parameter estimates in the individual
analyses constituted contrast images. The contrast images obtained from the individual analyses represented
the normalized task-related increment of the MR signal of each participant. To evaluate the neural substrates
involved in processing for grammar production, we compared the mean activation produced by particle produc-
tion and by letter production in all voxels in the brain (Grammar > Letter).

Subsequent random‑effects analysis. Contrast images from the individual analyses were used for the
group analysis. The contrast images obtained from the individual analyses represented the normalized task-
related increment of the MRI signal of each participant. In contrast (grammar > letter), a two-sample t-test was
performed between non-native and native participants for every voxel in the brain, to obtain population infer-
ences, with chronological ages different between the groups (t = 2.02, p = 0.049) as a covariate. The resulting set
of voxel values for each contrast constituted a statistical parametric map of the t-statistic (SPM {t}).
We evaluated the effects of grammar processing in both groups and the common brain activation between
groups as a conjunction of non-native learners and native speakers (conjunction-null hypothesis)95,96. We also
evaluated whether brain activation was higher in non-native learners than in native speakers for grammar pro-
cessing as (non-native > native). The SPM{t} threshold was set at t > 3.29 (equivalent to p < 0.001 uncorrected).
The statistical threshold for the spatial extent test on the clusters was set at p < 0.05 and was corrected for multiple
comparisons [family-wise error (FWE)] over the whole brain region 97.
We evaluated brain activation after excluding any activations outside the gray matter with the explicit masking
procedure. Brain regions were anatomically defined and labelled according to Automated Anatomical L ­ abeling98,
the SUIT t­ emplate99, and an atlas of the human ­brain100.

Data availability
The datasets used and/or analyzed during the current study are available from the corresponding author on
reasonable request.

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Received: 10 December 2021; Accepted: 31 October 2022

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Acknowledgements
This work was supported by the National Institute for Physiological Sciences ["the Cooperative Study Program”
(C.K.)]. Funding from the Japan Agency for Medical Research and Development (JP19dm0307005 to N.S.)
and the Grant-in-Aid for Scientific Research (15H01846 to N.S, 19K00877 to C.K.) is gratefully acknowledged.
The authors also wish to acknowledge Dr. Mako Hirotani of Carleton University for her help in validating the
methodology of this study, and proofreaders and editors of Editage.

Author contributions
Conceived of or designed study: C.K. and N.S. Performed research: C.K., M.S., T.K., and Y.Y. Analyzed data: M.S.
and T.K. Contributed new methods or models: H.M. Wrote the paper: C.K., M.S., and N.S.

Funding
Japan Society for the Promotion of Science, Japan Agency for Medical Research and Development.

Competing interests
The authors declare no competing interests.

Additional information
Supplementary Information The online version contains supplementary material available at https://​doi.​org/​
10.​1038/​s41598-​022-​23382-8.
Correspondence and requests for materials should be addressed to N.S.
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