rHuman Brain Mapping 29:1015–1027 (2008) r

Neural Correlates of Noncanonical Syntactic
Processing Revealed by a Picture-Sentence
Matching Task
Ryuta Kinno,1,2,3,4 Mitsuru Kawamura,2,3 Seiji Shioda,2,4
and Kuniyoshi L. Sakai1,2*
1

Department of Basic Science, Graduate School of Arts and Sciences, The Universityof Tokyo, Komaba, Tokyo, Japan
2
CREST, Japan Science and Technology Agency, Kawaguchi-shi, Japan3
Department of Neurology, Showa University School of Medicine, Hatanodai, Tokyo, Japan
4
Department of Anatomy, Showa University School of Medicine, Hatanodai, Tokyo, Japan

Abstract: It remains controversial whether the left inferior frontal gyrus subserves syntactic processing
or short-term memory demands. Here we devised a novel picture-sentence matching task involving
Japanese sentences with different structures to clearly contrast syntactic reanalysis processes. Using
event-related functional magnetic resonance imaging (fMRI), activations under three main conditions
were directly compared: a canonical/subject-initial active sentence (AS), a noncanonical/subject-initialpassive sentence (PS), and a noncanonical/object-initial scrambled sentence (SS). We found that activation in the dorsal region of the left inferior frontal gyrus (dF3t) was enhanced more by the noncanonical processing under the PS and SS conditions than by the canonical processing under the AS condition, and this enhancement was independent of domain-general factors, such as general memory
demands and task difﬁculty. Moreover, the left posterior superior/middle temporal gyrus (pSTG/
MTG) showed more enhanced responses to object-initial sentences under the SS condition than to subject-initial sentences under the AS and PS conditions, which were not signiﬁcantly affected by task difﬁculty. Furthermore, activation in the left lateral premotor cortex (LPMC) increased under the AS, PS,
and SS conditions, in that order. It is possible that task difﬁculty affects the left LPMC, but the three
distinct activations patterns suggest that these frontal and temporal regions work in concert to processsyntactic structures, with their respective contributions dynamically regulated by linguistic requirements. Hum Brain Mapp 29:1015–1027, 2008. V 2007 Wiley-Liss, Inc.
C

Key words: fMRI; frontal cortex; temporal cortex; sentence processing; syntax

Contract grant sponsor: Ministry of Education, Culture, Sports,
Science, and Technology of Japan; Contract grant number:
17022013; Contract grant sponsor: Japan Science and Technology
Agency (JST).
*Correspondence to: Dr. Kuniyoshi L. Sakai, Department of Basic
Science, Graduate School of Arts and Sciences, The Universityof Tokyo, Komaba, 3-8-1 Komaba, Meguro-ku, Tokyo 153-8902,
Japan. E-mail: sakai@mind.c.u-tokyo.ac.jp
C 2007 Wiley-Liss, Inc.
V

Received for publication 13 March 2007; Revised 5 June 2007;
Accepted 6 June 2007
DOI: 10.1002/hbm.20441
Published online 9 October 2007 in Wiley InterScience (www.
interscience.wiley.com).

r Kinno et al. r

INTRODUCTIONTABLE I. Sentences used in this study

Sentences convey not only lexico-semantic informationfor each word but also sentence meaning based on syntactic structures. In many languages, the same sentence meaning can often be expressed using different sentence structures. Even structurally complex sentences are sometimes
preferred to simple active sentences, especially when aparticular topic is intended to be emphasized in a certain
context. The more complex syntactic structures are, themore difﬁcult sentence comprehension generally becomes.
Previous functional magnetic resonance imaging (fMRI)
studies tested the effects of object-initial scrambled sentences in German and Hebrew, and reported enhanced activation in the left inferior frontal gyrus (IFG) and posterior
superior/middle temporal gyrus (pSTG/MTG) [Ben-Shachar et al., 2004; Bornkessel et al., 2005; Fiebach et al.,2005; Röder et al., 2002]. It is true that the sentences usedin many of these studies make it difﬁcult to know thecause of increased activation, since processing syntacticallycomplex sentences is inevitably confounded by task difﬁculty, which may simply explain the increased activation,
as indicated earlier. For example, Fiebach et al. (2005) haveconcluded that left IFG activation reﬂects ‘‘syntactic working memory load’’ (i.e., the maintenance of linguistic material that has not yet been integrated and is held active inshort-term memory) rather than syntactic integration costs(i.e., computational processes of integrating each incoming
word into the phrase structure representation); this conclusion was based on their observation that left IFG activation
was enhanced as a function of the distance between a dislocated verb phrase and its canonical position. It is not yet
clear, however, whether syntactic working memory is separable from general memory demands and task difﬁculty,
and the debate about the degree of specialization in language-related activity is still ongoing. Recent imaging
studies have shown that a part of the left IFG engages in
the processing of language-speciﬁc linearization rules that
include not only the rule of subject-before-object but therules of pronoun-before-nonpronominal argument [Greweet al., 2005] and animate-before-inanimate subject [Greweet al., 2006]. It would thus be necessary to clarify whether
the left IFG activation is modulated by syntactic processing
without the inﬂuence of domain-general factors if thisregion indeed specializes in syntactic processing.
The goal of the present study was to directly addressthese important issues, thereby equating domain-generalfactors among various types of canonical and noncanonicalsentences as much as possible. To minimize the effect ofgeneral memory demands, a whole sentence of a minimal
length (i.e., two nouns and one verb; see Table I) was visually presented for a longer time than was needed torespond, and the numbers of syllables and letters werestrictly controlled among all conditions. The sentences we
employed are thus more advantageous than those used inprevious studies with sequentially presented stimuli thatinvolve memorization. The task difﬁculty associated withr

Stimulus
Sentence control (SC) condition*-to h-ga neteiru*-to h-ga tatteru*-to h-ga aruiteru*-to h-ga hashitteru*-to h-ga koronderu*-to h-ga naiteru
Active sentence (AS) condition*-ga h-o hiiteru*-ga h-o oshiteru*-ga h-o shikatteru*-ga h-o ketteru*-ga h-o tataiteru*-ga h-o yonderu
Passive sentence (PS) condition
h-ga *-ni hikareru
h-ga *-ni osareru
h-ga *-ni shikarareru
h-ga *-ni kerareru
h-ga *-ni tatakareru
h-ga *-ni yobareru
Scrambled sentence (SS) condition
h-o *-ga hiiteru
h-o *-ga oshiteru
h-o *-ga shikatteru
h-o *-ga ketteru
h-o *-ga tataiteru
h-o *-ga yonderu

English translation* and h lie* and h stand* and h walk* and h run* and h tumble* and h cry* pulls h* pushes h* scolds h* kicks h* hits h* calls hh is affected by *’s pulling it
h is affected by *’s pushing it
h is affected by *’s scolding it
h is affected by *’s kicking it
h is affected by *’s hitting it
h is affected by *’s calling it
As for h,* pulls it
As for h,* pushes it
As for h,* scolds it
As for h,* kicks it
As for h,* hits it
As for h,* calls it

Only typical examples are shown here; other combinations among
the symbols *, h, and ~ were also used. ga, nominative marker;o, accusative marker; ni, dative marker; and to, conjunction ‘‘and.’’syntactically complex sentences might be also alleviated byproviding an appropriate context for each sentence.
Indeed, a self-paced reading study with Finnish sentences
showed that the processing of noncanonical/object-initialstructures was signiﬁcantly facilitated when the presenceof appropriate contexts alleviated the usual difﬁculty associated with noncanonical constructions [Kaiser and Trueswell, 2004]. In the present study, participants processed a
sentence based on a context provided by a picture. A picture representing an action consisted of two stick ﬁgures,
which were distinguished by ‘‘head’’ forms (without facial
expressions), each represented by a symbol: a circle (*), asquare (h), or a triangle (~) (Fig. 1). This picture further
excluded the involvement of pragmatic information about
word use (e.g., ‘‘An ofﬁcer chases a thief’’ is more acceptable than ‘‘A thief chases an ofﬁcer.’’). Half of the pictures
depicted action occurring from left to right, the other half
depicted action from right to left. The pictures were similar to those used in previous lesion studies [Maher et al.,
1995; Schwartz et al., 1980], but the simultaneous presentation of one picture and one sentence is unique and advantageous to the present study.
We tested the picture-sentence matching task under
three main conditions for event-related fMRI sessions (Fig.
1A–C): a canonical/subject-initial active sentence (AS), a
noncanonical/subject-initial passive sentence (PS), and a1016 rr Noncanonical Syntactic Processing in the Brain r

Figure 1.
The four sentence conditions used in the picture-sentence ‘‘h-o *-ga oshiteru’’; right, ‘‘~-o h-ga oshiteru’’). The sentence
matching task and the timing of slice acquisition. Each stimulus stimuli were all grammatical and commonly used in Japanese. An
consisted of one picture (top) and one sentence (bottom). Pic- identical picture set was used under the AS, PS, and SS conditures depicting actions consisted of two stick ﬁgures, and each tions. D: Under the sentence control (SC) condition, canonical/
stick ﬁgure was distinguished by one of three ‘‘head’’ symbols: a subject-initial active sentences with two agents and one verb
circle (*), a square (h), or a triangle (~). The participants were presented (left, ‘‘*-to h-ga hashitteru’’; right, ‘‘h-to ~-ga
judged whether or not the meaning of each sentence matched hashitteru’’). E: Each stimulus pair was presented for 3,800 ms
the action scene given in the corresponding picture. Two sam- with 200-ms interstimulus intervals. The trial events of the picples are shown for each condition. A: Under the active sentence ture-sentence matching task occurred with variable intertrial(AS) condition, canonical/subject-initial active sentences were intervals, in which four, ﬁve, or six visual control (VC) trials
presented (left, ‘‘*-ga h-o oshiteru’’; right, ‘‘h-ga ~-o oshiteru’’). were presented. The ﬁrst slice acquisition occurred 2,100 ms afBelow each example, a word-by-word translation in English is ter the stimulus onset, and the acquisition timing of each sliceshown. Nom, nominative case; Acc, accusative case; Dat, dative was corrected using the ﬁrst slice as a reference for the funccase. See Table I for the stimulus list. B: Under the passive sen- tional imaging data. A red-graded bar schematically denotes a catence (PS) condition, noncanonical/subject-initial passive senten- nonical homodynamic response function centered on the ﬁrst
ces were presented (left, ‘‘h-ga *-ni osareru’’; right, ‘‘~-ga h-ni slice (90% sensitivity at 61 s). The range of RTs (mean 6 SD) isosareru’’). C: Under the scrambled sentence (SS) condition, non- also shown under each of the SC, AS, PS, and SS conditions.
canonical/object-initial scrambled sentences were presented (left,

noncanonical/object-initial scrambled sentence (SS). The
same set of scenes depicted by pictures and sentences wasused under each of these three conditions. Under the AS
condition, transitive verbs were used with the SOV (S, subject; O, object; V, verb) canonical sentence type (e.g., ‘‘*-ga
h-o oshiteru’’; ‘‘* pushes h’’). Under the PS condition, noncanonical passive sentences were presented with the SOV
sentence type (‘‘h-ga *-ni osareru’’; ‘‘h is affected by *’srpushing it’’; this sentence type is further explained in thenext paragraph). Under the SS condition, object-initialscrambled sentences were presented with the OSV noncanonical sentence type (‘‘h-o *-ga oshiteru’’; ‘‘As for h,*pushes it’’). The OSV type is grammatical and frequently
used in conversation and writing in Japanese. Note thatthe sentences under the PS and SS conditions thus
required different types of noncanonical processing. More-

1017 rr Kinno et al. rover, sentence comprehension under these conditions explicitly required analysis of both dependency relations (i.e.,
which is the subject of a verb, and which is its object?) andsemantic (thematic) roles (i.e., who initiates the action, and
who is affected by it?). In Japanese syntax, the grammatical
relations are ﬁrst marked by case markers (e.g., nominative
and accusative), which in turn allow the assignment ofsemantic roles (e.g., agent and patient), whereas passivenessis also marked in the verb morphology.
The passive sentences in Japanese tested here are noncanonical/subject-initial and require syntactic reanalysis forthe following reasons. In most Japanese sentences, a nounphrase with the nominative case marker ga is associatedwith the semantic role of an agent (an initiator of an action,an actor), and a noun phrase with the accusative casemarker o is associated with the semantic role of a patient (aperson affected by an action). For passive sentences withni direct passive that were used in the present study, however, a noun phrase with the nominative case marker ga is
associated with the semantic role of an experiencer (a person experiencing a situation), and a noun phrase with thedative marker ni is associated with an agent [Hoshi, 1994;
Kuroda, 1992]. Actually, there are two types of passivization in Japanese: ni direct passive and ni yotte passive. The
following three examples indicate this distinction [Hoshi,
1994].

require the analysis of dependency relations in a sentence.
Thus, the SC condition is syntactically less complex andeasier to comprehend than other conditions. By using an
event-related fMRI, we focused on the ﬁnal process of syntactic reanalysis just before responses were produced (Fig.
1E; see MATERIALS AND METHODS). Direct comparisons among the AS, PS, and SS conditions reveal activations that represent syntactic reanalysis per se, which is
closely associated with different types of canonical andnoncanonical processing for sentence comprehension.

MATERIALS AND METHODS
Participants
Fourteen right-handed native Japanese speakers (tenmales and four females, aged 20–31 years) participated in
the present study. Handedness was determined by the
Edinburgh inventory [Oldﬁeld, 1971]. None of the participants had any neurological or psychiatric symptoms.
Informed consent was obtained from each participant after
the nature and possible consequences of the studies wereexplained. Approval for the experiments was obtained
from the institutional review board of the University ofTokyo, Komaba.

Stimuli(a) Mary-ga John-o nagutta.
‘Mary punched John.’(b) John-ga Mary-ni nagurareta. (ni direct passive)‘John was affected by Mary’s punching him.’(c) John-ga Mary-ni yotte nagurareta. (ni yotte passive)‘John was punched by Mary.’
According to Kuroda (1992), the ni direct passive form
carries the affective connotation and no noun-phrase (NP)movement takes place, while the ni yotte passive form
does not carry that connotation and NP movement occurs
as is the case in English. Therefore, the sentences with theni direct passive construction are noncanonical and subject-initial.
As stated earlier, the picture stimuli were exactly thesame under the AS, PS, and SS conditions. If the visual
analysis of pictures was also enhanced by noncanonicalprocessing, then activation in visual areas would beobserved. Visual factors alone cannot explain any condition-selective frontal and temporal activation without activation in the visual areas. Moreover, the pictures provided
the same additional contextual information for the three
conditions, and thus such semantic information cannot
explain any differential activation, either. To identify howtask difﬁculty potentially affects cortical activations in thepresent paradigm, we also included a sentence control(SC) condition with canonical/subject-initial active sentences in which intransitive verbs were used (Fig. 1D). The
SC condition basically required matching between words(symbols and verbs) and pictures alone, and it did notr

Each visual stimulus consisted of a picture at the top
and a Japanese sentence at the bottom as a single stimulusset (Fig. 1A–D). The sentences describing actions were
written in a combination of the ‘‘hiragana’’ and ‘‘kanji’’writing systems, and each sentence included two nounphrases and one verb. For example, a noun phrase (h-ga)
consisted of a symbol (h) and a hiragana (ga). Two sets ofJapanese verbs (six transitive verbs: pull, push, scold, kick,hit, and call; and six intransitive verbs: lie, stand, walk, run,tumble, and cry) were used, each of which, including thepassive forms, had either four or ﬁve syllables (Table I).
Note that the verb ‘‘call’’ is used as a transitive verb in Japanese. There was no signiﬁcant frequency difference
between the two sets of verbs (t-test, t(10) 5 0.68, P 50.52), according to the Japanese lexical database (NTTdatabase series, ‘‘Nihongo-no Goitokusei’’ (Lexical Properties of Japanese); Nippon Telegraph and Telephone Corporation Communication Science Laboratories, Tokyo, Japan,
2003). The pictures used in the AS, PS, and SS conditions
were identical (the number of lines used in a picture,mean 6 SD: 14 6 2.4, n 5 6), and equally complex pictures were used under the SC condition (14 6 2.5, n 5 6).
In the pictures, the use of symbols was also counterbalanced for both sides.
In each 4-s trial of the fMRI experiments, all stimuli
were presented visually in yellow against a dark background. Each stimulus was presented for 3,800 ms followed by a 200-ms blank interval (Fig. 1E). For ﬁxation, a
red cross was always shown at the center of the screen.

1018 rr Noncanonical Syntactic Processing in the Brain r

Stimulus presentation and behavioral data collection were
controlled using the LabVIEW software and interface(National Instruments, Austin, TX). The participants wore
earplugs and an eyeglass-like MRI-compatible display (resolution, 800 3 600, within the visual angle of 78)(VisuaStim XGA; Resonance Technology, Northridge, CA).

Tasks

TABLE II. Behavioral data for each task condition
Condition
SC
AS
PS
SS

Accuracy (%)

RT (ms)93.8 6 4.2
93.2 6 4.5
92.0 6 4.8
93.2 6 4.2

2010 6 289
2156 6 283
2166 6 308
2197 6 287

Data are shown as mean 6 SD.

Under the AS, PS, and SS conditions, all mismatchedsentences were made by exchanging two symbols in theoriginal sentences, e.g., ‘‘h pushes *’’ instead of ‘‘* pushesh’’. Under the SC condition, both symbol-mismatched sentences and action-mismatched ones were presented equallyoften, which required the sentences to be read completely
to arrive at a judgment. Under all of these conditions, theparticipants read a sentence covertly and judged whether
or not the sentence matched the action scene depicted by
the picture by pressing one of two buttons.
In addition to the picture-sentence matching task, weused a visual control (VC) task as a baseline control task,
which required neither word nor sentence processing. In
the VC task, the same sets of pictures used in the picturesentence matching task were presented, together with astring of jumbled letters taken from a single sentence (Fig.
1E, inset) in which the symbols and ‘‘kanji’’ appeared at
the same positions in the string as in the picture-sentence
matching task. The participants were asked to judge
whether or not all the symbols in a letter string were thesame as those in the picture, irrespective of the order ofthe symbols. General cognitive factors such as visual perception of the stimuli, response selection, and motor
response were controlled by the VC task.
A single run contained 12 ‘‘trial events’’ of the picturesentence matching task (three times each for the SC, AS,
PS, and SS conditions), with variable intertrial intervals of
16, 20, and 24 s (four, ﬁve, and six VC trials, respectively),
pseudorandomized within a run. Since letter strings were
presented throughout the VC task while sentences were
presented only in the trial events, the participants could
switch from the VC task to the trial events according to
the stimulus type. The order of the SC, AS, PS, and SS conditions was pseudorandomized in each run to prevent any
condition-speciﬁc strategy. Half of the stimuli consisted ofmatched picture-sentence pairs, and the other half consisted of mismatched pairs. Sixteen runs were tested in
two days, with eight runs per day, and the participants
did not encounter the same sentence twice in a single day.
The participants underwent practice sessions before scanning to become fully familiarized with the tasks.

fMRI Data Acquisition and Analyses
The fMRI scans were conducted on a 1.5 T scanner(Stratis II, Premium; Hitachi Medical Corporation, Tokyo,
Japan). We scanned 16 horizontal slices, each 6-mm thickand having a 1-mm gap, covering the range of z 5 249 tor

62 mm from the AC-PC line, with a gradient echo echoplanar imaging sequence (repetition time (TR) 5 4 s, acquisition time (TA) 5 1.85 s, echo time 5 50.5 ms, ﬂip
angle 5 908, ﬁeld of view 5 192 3 192 mm2, resolution 5
3 3 3 mm2). In a single scanning run, we obtained 77 volumes following three dummy images, which allowed forthe rise of the blood oxygenation-level-dependent signals.
We performed group analyses using SPM2 statisticalparametric mapping software [Friston et al., 1995] (Wellcome Department of Cognitive Neurology, London, UK),
on MATLAB (Math Works, Natick, MA). Because themean accuracy was more than 92% under all the conditions (Table II), all events including correct and incorrect
answers were used in the analyses. We realigned the functional volume data in multiple runs and removed runsthat included data with a translation of >2 mm in any of
the three directions and with a rotation of >1.48. The acquisition timing of each slice was corrected using the ﬁrst
slice as a reference. Each individual brain was spatiallynormalized to the standard brain space as deﬁned by theMontreal Neurological Institute (MNI) and was resampled
every 3 mm using sinc interpolation. These data were thensmoothed using an isotropic Gaussian kernel of 9 mm fullwidth at half maximum. Low-frequency noise and globalchanges in activity were further removed.
According to behavioral data, reaction times (RTs) under
the SC, AS, PS, and SS conditions were 2,100 ms (Fig. 1E,
Table II), indicating that there was little time to rehearse a
sentence more than once. Based on the pilot data, we set
the timing of the ﬁrst slice acquisition to 2,100 ms after the
stimulus onset, and the acquisition of 16 slices triggered
the presentation of a visual stimulus with a 50-ms delay.
The acquisition timing of each slice was corrected using
the ﬁrst slice as a reference for the functional imaging
data, thereby specifying both TR 5 4 s and TA 5 1.85 s in
the analyses. By using an impulse function for eventrelated hemodynamic responses, we focused on the ﬁnal
process of syntactic reanalysis just before responses were
produced. When one condition (e.g., AS) was comparedwith the VC task, one covariate was set that corresponded
to event-related responses from the baseline level of the
VC task. For random effects analyses, a contrast image
was generated for each participant and used for intersubject comparisons. The statistical threshold was set to P <0.05, corrected for multiple comparisons (false discovery
rate correction) in the entire brain with no cluster threshold. Among the signiﬁcantly activated regions under each1019 rr Kinno et al. rof the AS, PS, and SS conditions, further comparisons were
established at a Z-score > 3.1 (uncorrected P < 0.001) witha volume of more than ﬁve voxels. To exclude false-positive activations, we used a small volume correction (SVC)
at the level of corrected P 5 0.05 (9-mm radius) for SS–AS,(SS–AS) vs. (AS–SC), and PS–AS. The MNI coordinates (x,y, z) for the SVC were (254, 27, 21) and (257, 9, 9) for theleft IFG, (239, 3, 42) for the left lateral premotor cortex(LPMC) and (252, 246, 6) for the left pSTG/MTG, whichwere reported in the previous studies of syntactic processing [Fiebach et al., 2005; Hashimoto and Sakai, 2002;
Suzuki and Sakai, 2003]. For the anatomical identiﬁcationof activated regions, we used the Anatomical Automatic
Labeling method [Tzourio-Mazoyer et al., 2002].

RESULTS
Behavioral Data
Behavioral data on the accuracy and RT are shown in
Table II. The effect of context on the accuracy, together
with the differences between the conditions, was examinedby comparing the trials of matched and mismatchedsentences. A repeated-measures analysis of variance(ANOVA) with two factors (condition [SC, AS, PS, SS] 3
context [matched, mismatched]) showed that neither amain effect of condition (F(3, 39) 5 0.53, P 5 0.67) nor thatof context (F(1, 13) 5 2.9, P 5 0.11) was signiﬁcant, and aninteraction of condition by context was not signiﬁcant (F(3,39) 5 0.17, P 5 0.92), either. Regarding RTs, there was asigniﬁcant main effect of condition (F(3, 39) 5 15, P <0.001), while neither a main effect of context (F(1, 13) 5
2.5, P 5 0.13) nor an interaction of condition by context
was signiﬁcant (F(3, 39) 5 0.23, P 5 0.88). Paired t-tests
showed that the RTs were signiﬁcantly longer under theAS, PS, and SS conditions than under the SC condition (SCvs. AS: t(13) 5 3.0, P 5 0.011; SC vs. PS: t(13) 5 2.8, P 5
0.015; SC vs. SS: t(13) 5 3.7, P 5 0.0027), indicating that
the SC condition was easier than the other conditions.
Under the three main conditions, the RTs of AS and SS
alone were signiﬁcantly different (AS vs. PS: t(13) 5 0.44,
P 5 0.67; AS vs. SS: t(13) 5 3.0, P 5 0.0094; PS vs. SS: t(13)5 1.7, P 5 0.11). These results indicate that the SS condition was more demanding than the AS condition, while
the difﬁculty under the AS and PS conditions, as well asthat under the PS and SS conditions, was balanced.
The skewnesses of the accuracy distribution for the SC,
AS, PS, and SS conditions were 20.95, 20.70, 20.38, and20.46, respectively, and those of the RT distribution forthese conditions were 1.10, 0.52, 0.60, and 0.51, respectively.
The accuracy and RT distributions were more skewed
under the SC condition than under the other three conditions, indicating a ceiling effect under the SC condition.
Since there was no main effect of context among the four
conditions, we treated the trials of matched and mismatched sentences together in the following fMRI analyses.

rCommonalities and Differences in Cortical
Activation Among the Sentence Conditions
To examine the commonalities and differences in corticalactivation among the SC, AS, PS, and SS conditions, weﬁrst compared each condition with the VC task. As shownin Figure 2, the overall patterns of activation were similar
among the four conditions (see also Table III for activationfoci). These results showed the reproducibility and consistency of activation in the cortical language areas among
these conditions. Activations in the IFG (Brodmann’s areas(BAs) 44/45), LPMC (BAs 6/8/9), and pSTG/MTG (BAs
22/21/37) were most prominent and dominant in the left
hemisphere. The activation in the left IFG was localized in
the left pars opercularis (F3op, BA 44) and pars triangularis (F3t, BA 45) across the anterior vertical ramus, but thisregion (F3op/F3t) did not extend to the pars orbitalis(F3O, BA 47). Moreover, activation in the left dorsal F3t(dF3t) was more prominent under the PS and SS conditions than under the SC and AS conditions, a ﬁnding that
we analyze in detail later. Other consistent activation wasobserved in the presupplementary motor area (pre-SMA,
BA 6), one or both of the heads of the caudate (the coronal
sections in Fig. 2), and the inferior parietal/occipital gyrus(BAs 7/19/39) that did not include the main visual cortex(BAs 17/18). The left intraparietal sulcus (IPS, BAs 7/39/
40) was activated under the SC, PS, and SS conditions. The
right insula activation was observed only under the SS
condition.

Potential Effects of Task Difﬁculty and
Syntax on Cortical Activations
As mentioned earlier, the processing of syntactically complex sentences such as scrambled sentences is inevitably
confounded by task difﬁculty. Therefore, we ﬁrst identiﬁed
how task difﬁculty potentially affects cortical activations.
We examined activation in AS–SC and SS–AS (Fig. 3A,B),
since both sentence complexity (Table I) and RTs (Table II)
increased under the SC, AS, and SS conditions in that order.
Because an intransitive verb and a transitive verb wereused in sentences under the SC and AS conditions, respectively, in which their frequency was matched (see MATERIALS AND METHODS), the AS condition required the analysis of dependency relations, but the SC condition did not,as noted earlier. This difference in verb type may be one
reason for the enhanced task difﬁculty under the AS condition when compared with the SC condition.
As shown in Figure 3A and Table IV, prominent activations in AS–SC were observed in the left LPMC (239, 0,54) and bilateral pSTG/MTG [(257, 260, 0) and (54, 266,0)]. Among the brain regions equally activated under theAS, PS, and SS conditions, the left inferior parietal/occipital gyrus (251, 275, 6) also showed activation in this comparison, whereas the pre-SMA and the heads of caudate
were not signiﬁcantly activated in this comparison andthus were not signiﬁcantly affected by task difﬁculty. In

1020 rr Noncanonical Syntactic Processing in the Brain r

Figure 2.
Activation patterns elicited by each condition. A–D: Cortical overall patterns of signiﬁcant activation were similar among theregions identiﬁed by the contrasts of SC, AS, PS, and SS, respec- four conditions. Signiﬁcant activation was also observed in one
tively, which were projected onto the left (L) and right lateral or both heads of the caudate (see the coronal sections). The
surfaces of a surface-rendered standard brain. Coronal sections thresholds were established at P < 0.05, corrected for multiple[y 5 4 at the black lines] are also shown. For each condition comparisons. See Table III for the stereotactic coordinates of(e.g., AS), one covariate was set that corresponded to event- the activation foci.
related responses from the baseline level of the VC task. The
contrast, the most prominent activation in SS–AS wasobserved in the left dF3t (252, 21, 21) and this activatedregion extended to the left F3op/F3t (Fig. 3B), whereas theleft IFG was not signiﬁcantly activated in AS–SC. Signiﬁcant activation was also observed in the left LPMC (239,r0, 45) and left pSTG/MTG (254, 254, 3), which were activated in AS–SC as well. However, the activated region of
the left pSTG/MTG in SS–AS was much wider than that in
AS–SC, indicating that syntactic processing still affects theactivation of this region.

1021 rr Kinno et al. r

TABLE III. Cortical regions identiﬁed by condition

Brain Region

BA

Side

LPMC
F2/F3op/F3t
dF3t
F3op/F3t
Insulapre-SMA
Caudate

6/8/9
8/44/4545
44/45

pSTG/MTG

22/21/37

IPS

7/39/40

Inferior parietal/
occipital g

7/19/39

L
R
L
L
R
M
L
R
L
R
L
R
L

6

x

y

z

Z

x

236
45
254
245

12
15
18
39

51
36
12
9

4.3
4.6
3.9
4.7

245
48
251
251

23

24

48

3.8

254

251

6

4.0

248
42

260
263

51
36

4.0
3.6

y

z

Z

x

y

6
21
18
27

48
33
27
6

4.4
4.6
3.9
4.1

239
45
251
254

23
26
9
254
51

18
3
3
254
254

51
3
0
6
6

4.5
3.8
3.5
4.5
4.1

224

278

33

45

278

6

SC

z

Z

x

y

23
18
21
27

45
36
24
3

4.4
4.7
4.4
4.0

3

18

51

3.3

242
48
251
248
42
23
29

9
254
51
239

3
254
260
257

3
6
9
54

3.3
4.8
3.9
3.8

3.5

230

281

30

4.1

42

278

6

AS

R

z

Z

3
21
21
18
21
18
0

48
33
18
0
26
48
3

4.4
4.4
5.4
3.8
3.6
4.8
4.2

260
54
236

248
236
257

9
3
51

5.2
4.0
3.9

4.0

230

284

30

4.7

3.8

45

275

6

3.5

PS

SS

Stereotactic coordinates (x, y, z) in the MNI space are shown for each activation peak of Z values. The threshold is set at corrected P <0.05 for the voxel level, and clusters smaller than ﬁve voxels were removed from the table for brevity. BA, Brodmann’s area; L, left
hemisphere; R, right hemisphere; M, medial; g, gyrus; F2, middle frontal gyrus; F3op and F3t, opercular and triangular parts of inferior
frontal gyrus; d, dorsal; LPMC, lateral premotor cortex; pre-SMA, presupplementary motor area; pSTG/MTG, posterior superior temporal gyrus and middle temporal gyrus; IPS, intraparietal sulcus.

It is possible that the ceiling effect under the SC condition might have weakened the AS–SC result. Therefore, we
carefully examined the difference in task difﬁculty
between AS–SC and SS–AS. The difference in RTs of AS–
SC (146 6 134 ms) was about 100 ms longer than that of
SS–AS (41 6 50 ms). There was also a signiﬁcant difference
between these two data (paired-t, t(13) 5 2.7, P 5 0.018),
indicating a greater behavioral difference in difﬁculty for
AS–SC than for SS–AS. We performed a more direct andcompelling test of the syntactic processing by task difﬁculty interaction, in which the results of SS–AS and AS–SC
for each participant were submitted to a paired t-test. As
shown in Figure 3C and Table IV, this analysis revealed
greater activation differences in SS–AS than in AS–SC forthe left dF3t (251, 21, 18) and left pSTG/MTG (251, 251,
3). The opposite pattern of results across these two typesof analyses suggest that activation in the left dF3t and left
pSTG/MTG is modulated more by syntactic differences
than by task difﬁculty differences.

Left Frontal Activation Enhanced by
Noncanonical Syntactic Reanalysis
Next we examined activation in PS–AS, thereby directly
contrasting the noncanonical and canonical conditions,where both conditions included subject-initial structures
and where their difference in RTs was not signiﬁcant. To
further control the effect of task difﬁculty, an analysis ofcovariance (ANCOVA) was conducted with the differencein RTs as a covariate, in which the variability of RTs
among participants was removed (Fig. 4, Table IV). This
analysis resulted in a signiﬁcant activation in the left dF3t
alone (248, 24, 21), which matched with the left dF3t activation observed in SS–AS (Fig. 3B,C, Table IV). This resultrdemonstrated that the left dF3t is speciﬁcally recruited forthe noncanonical processing of syntactic reanalysis without
the inﬂuence of domain-general factors, including generalmemory demands and task difﬁculty.

Distinct Activation Patterns in theLeft Frontal and Temporal Regions
Next we examined the relative contributions of the frontal and temporal regions to the cognitive processes
required under the AS, PS, and SS conditions. For this purpose, the amplitudes of ﬁtted hemodynamic responses (6.1
s after each trial event) were calculated under each condition at the local maxima of the left dF3t (248, 24, 21), left
LPMC (239, 0, 45), and left pSTG/MTG (251, 251, 3)(Fig. 5). A repeated-measures ANOVA with two factors(region [dF3t, LPMC, pSTG/MTG] 3 condition [AS, PS,SS]) revealed a signiﬁcant main effect of region (F(2, 26) 5
4.9, P 5 0.016) and that of condition (F(2, 26) 5 15, P <0.001), together with a signiﬁcant interaction of region bycondition (F(4, 52) 5 2.6, P 5 0.045). These results indicated that each of these three regions is differentiallymodulated by task-related factors under the AS, PS, andSS conditions.
Finally, we examined the effects of condition on theamplitudes of ﬁtted hemodynamic responses for eachregion. As shown in Figure 5A, the left dF3t activation
was enhanced more under the PS and SS conditions thanunder the AS condition (PS vs. AS: t(13) 5 2.4, P 5 0.033;
SS vs. AS: t(13) 5 2.5, P 5 0.029), whereas there was no
signiﬁcant difference in response between the PS and SS
conditions (t(13) 5 0.88, P 5 0.15). Moreover, the left
pSTG/MTG showed a distinct activation pattern separablefrom the left dF3t, such that the SS condition elicited sig-

1022 rr Noncanonical Syntactic Processing in the Brain r

niﬁcantly greater responses than either the AS or PS condition (SS vs. AS: t(13) 5 10, P < 0.001; SS vs. PS: t(13) 5 11,
P < 0.001) (Fig. 5B), whereas there was no signiﬁcant difference in amplitude between the AS and PS conditions(t(13) 5 1.1, P 5 0.31). Furthermore, activation in the left
LPMC increased under the AS, PS, and SS conditions inthat order (Fig. 5C). The SS condition elicited signiﬁcantly
greater responses than the AS condition (t(13) 5 2.3, P 5
0.040), whereas there was no signiﬁcant difference in amplitude between the other conditions (PS vs. AS: t(13) 5
1.1, P 5 0.27; SS vs. PS: t(13) 5 0.93, P 5 0.37). These
results conﬁrm the unique contribution of the left dF3t to
noncanonical syntactic processing (Fig. 4), as well as the
supportive roles of the left pSTG/MTG and left LPMC
(Fig. 3B), the former of which was not signiﬁcantly
affected by task difﬁculty (Fig. 3C).

DISCUSSION
The present study with the picture-sentence matchingtask successfully established for the ﬁrst time that the left
dF3t activation was enhanced more by the noncanonicalprocessing under the PS and SS conditions than by the canonical processing under the AS condition, and that thisenhancement was independent of domain-general factors
such as general memory demands and task difﬁculty.
Moreover, the left pSTG/MTG showed more enhanced
responses to object-initial sentences under the SS condition
than to subject-initial sentences under the AS and PS conditions, which were not signiﬁcantly affected by task difﬁculty. Furthermore, activation in the left LPMC increased

TABLE IV. Cortical regions identiﬁed byeach comparison
Figure 3.
Potential effects of task difﬁculty and syntax on cortical activations. The sentence stimuli became more complex under theSC, AS, and SS conditions in that order (Table I). According to
the behavioral data (Table II), RTs also increased signiﬁcantly inthe same order. A: Cortical regions identiﬁed by AS–SC. The
contrast of AS (Fig. 2; uncorrected P < 0.001) was used as aninclusive mask to eliminate any deactivation due to SC. The
threshold was established at a Z-score >3.1. Note that the left
inferior frontal gyrus (IFG) was not signiﬁcantly activated in thiscomparison. B: Cortical regions identiﬁed by SS–AS. The contrast of SS (Fig. 2; uncorrected P < 0.001) was used as an inclusive mask. The threshold was established at a Z-score >3.1 (corrected P < 0.05 after SVC) with a volume of more than ﬁvevoxels. Note the signiﬁcant activation in the left LPMC as well as
in the left dF3t and left pSTG/MTG. C: Cortical regions identiﬁed by (SS–AS) vs. (AS–SC). The threshold was established at a
Z-score >3.1 (corrected P < 0.05 after SVC). Note the signiﬁcant activation in the left dF3t and left pSTG/MTG. See Table IV
for the stereotactic coordinates of the activation foci.

rBrain region

BA

Side

x

AS – SC
LPMC
pSTG/MTG

6/8/9
22/21/37

L
L
R
L

239
0 54 4.0
257 260 0 3.8
54 260 0 5.8
251 275 6 3.7

20
11
19
6

L
L
L

239
0 45 4.8
252
21 21 4.7
254 254 3 4.8

7
11
29

L
L

251
21 18 4.1
251 251 3 4.0

26
29

L

248

10

Inferior parietal/ 7/19/39
occipital g
SS – AS
LPMC
6/8/9
dF3t
45
pSTG/MTG
22/21/37(SS – AS) vs. (AS – SC)
dF3t
45
pSTG/MTG
22/21/37
PS – AS
dF3t
45

y

z

Z

24 21 3.8

VoxelsStereotactic coordinates (x, y, z) in the MNI space and cluster size
are shown for each activation peak of Z values. The threshold is
set at uncorrected P < 0.001 with a volume of more than ﬁve voxels. To exclude false-positive activations, we used an SVC (9 mmradius) at the level of corrected P 5 0.05 for SS – AS, (SS – AS) vs.
(AS – SC), and PS – AS.

1023 rr Kinno et al. r

A number of previous imaging studies on verbal shortterm memory have reported greater activation of the left
frontal regions including the left IFG; this might reﬂect
general task difﬁculty stemming from memory load
[Braver et al., 1997; Clark et al., 2000; Cohen et al., 1997;
Rypma and D’Esposito, 1999]. A recent fMRI study examined the dependency of left IFG activity on the nature of abehavioral task during syntactic processing and suggested
that left IFG activation is related to task parameters suchas mnemonic and other integrative functions [Love et al.,Figure 4.
Left frontal activation enhanced by noncanonical syntactic reanalysis. A single region was identiﬁed by PS–AS, which is projectedin three orthogonal planes (sagittal, coronal, and horizontal fromthe top left panel) and onto a left surface-rendered standard
brain. The threshold was established at a Z-score >3.1 (corrected P < 0.05 after SVC). Note the signiﬁcant activation in theleft dF3t (yellow circles). See Table IV for the stereotactic coordinates of the activation focus.

under the AS, PS, and SS conditions, in that order. It is
possible that task difﬁculty affects the left LPMC, but thethree distinct activation patterns suggest that these frontal
and temporal regions work in concert to process syntactic
structures, with their respective contributions dynamicallyregulated by linguistic requirements.
It has been reported that noncanonical sentence structures are inherently more difﬁcult to process than canonical ones, as shown by the signiﬁcant differences in accuracy and RT in the processing of scrambled and active sentences in Japanese [Tamaoka et al., 2005] as well as inGerman [Fiebach et al., 2005]. On the other hand, the present study showed no signiﬁcant difference in accuracy
among the sentences under the AS, PS, or SS conditions,and the RTs for the sentences under the AS and PS conditions did not differ signiﬁcantly. One possibility for the absence of any signiﬁcant difference in accuracy is that thepresent task did not require memorization, since the wholesentence of a minimal length was visually presented for alonger time than was needed to respond. As a result, we
successfully showed the distinct contribution of eachregion to syntactic processing.

r

Figure 5.
Distinct activation patterns in the left frontal and temporal
regions. The amplitudes of ﬁtted hemodynamic responses for
the AS, PS, and SS conditions are shown with reference to the
SC condition. A: Histograms for the amplitudes of ﬁtted hemodynamic responses at the local maxima of the left dF3t. Error
bars indicate the SEM of participants, and asterisks denote thesigniﬁcance level of P < 0.05. Signal changes under the SS and PS
conditions were signiﬁcantly larger than those under the AS
condition. B: Histograms for the left pSTG/MTG. Signal changes
under the SS condition were signiﬁcantly larger than those underthe AS and PS conditions. C: Histograms for the left LPMC. The
SS condition elicited signiﬁcantly greater responses than the AS
condition.

1024 rr Noncanonical Syntactic Processing in the Brain r

2006]. Other studies have also suggested that the left IFG
activation reﬂects short-term memory demands [Cookeet al., 2002; Fiebach et al., 2005]. In our previous study,
however, we directly compared the cortical activations insyntactic decision tasks with those in verbal short-term
memory tasks and observed that the left dF3t showed
selective activation for syntactic decisions in sentences,and that this activation was much greater than would be
expected merely due to task difﬁculty and verbal shortterm memory demands [Hashimoto and Sakai, 2002]. In
the present study, we ﬁrst examined activation in AS–SC(dependency relations due to verb types) and SS–AS (noncanonical/object-initial sentences) to clarify the effect oftask difﬁculty coupled with sentence complexity. Despite
evidence for a signiﬁcantly larger behavioral effect for thedifference between AS and SC than for SS and AS, wedemonstrated the opposite pattern in the activation data,such that the activation in SS–AS is signiﬁcantly greater inthe left dF3t than that in AS–SC (Fig. 3C). The following
cognitive factors were further strictly equated among theAS, PS, and SS conditions: visual perception, word recognition, verbal memory load (the number of verbal items
held in the phonological store), semantic information, andresponse selection. Therefore, the remaining factor that can
explain the selective activation of the left dF3t in PS–AS
should be syntactic reanalysis per se. Indeed, we have previously reported that a selective priming effect on syntactic
decisions, but not on semantic decisions, was induced
when event-related transcranial magnetic stimulation was
administered to the left IFG with a speciﬁc timing [Sakai
et al., 2002]. Previous neuroimaging studies have also
reported syntactic complexity effects on left IFG activation
in English sentences [Dapretto and Bookheimer, 1999;
Stromswold et al., 1996], as well as an effect of grammatical rules contrasted with linguistically illegal rules [Mussoet al., 2003] or an effect of the language-speciﬁc linearization rules for arguments [Grewe et al., 2005, 2006] as noted
earlier. The present study further clariﬁes a speciﬁc and independent role of the left dF3t during the noncanonicalprocessing of syntactic reanalysis.
We also found a localized activation in the left pSTG/
MTG (251, 251, 3), which showed signiﬁcant activation in(SS–AS) vs. (AS–SC). A previous fMRI study reported activation in the left posterior superior temporal sulcus aswell as other regions, such as the premotor cortex or occipitotemporal sulcus, which were activated by object-initialvs. subject-initial sentences [Bornkessel et al., 2005]. We
previously reported that a focal region in the left pSTG/
MTG (254, 242, 3), proximal to the present activation,
was differentially activated by sentences containing either
syntactic or semantic anomalies when compared with normal sentences [Suzuki and Sakai, 2003]. Although there
were no anomalies in the sentences used in the present
study, it is interesting to note that the left pSTG/MTG activation was modulated by the syntactic processing ofscrambled sentences. It is thus likely that this activation
reﬂects the syntactic reanalysis required by anomalous sen-r

tences or scrambled sentences that were more confusing
than the subject-initial sentences used under the AS and
PS conditions. A recent intraoperative electrocorticography
study in humans showed bidirectional connectivity
between the left IFG and the left pSTG/MTG [Matsumoto
et al., 2004], and additional evidence for this connectivity
has been reported in studies using MRI to investigate
structural connectivity [Catani et al., 2005; Friederici et al.,2006]. Therefore, it is possible that this network subserves
syntactic integration, thereby combining multiple linguistic
information.
The identiﬁcation of linguistic information processed in
the left pSTG/MTG has been one of the main issues
addressed by recent neuroimaging studies. A recent study
with German transitive sentences (nominative-accusative
structures), in which an animate subject acts on either an
inanimate object (a natural, i.e., unmarked, construction)or an animate object (a more complex, i.e., marked, construction), showed that such a deviation leads to increased
activation in the left STG/MTG [Grewe et al., 2007]. This
result is consistent with our present ﬁnding of theenhanced activation of this region due to noncanonical/
object-initial scrambled sentences, where a more detailed
analysis of marked structural relationships between two
animate arguments is required. On the other hand, theright pSTG/MTG has been implicated in the processing of
nonlinguistic information about visual cues such as the
movement of eyes, hands, and mouth [Frith and Frith,
1999; Pelphrey et al., 2005; Wright et al., 2003]. In the present study, the activation of the right pSTG/MTG was signiﬁcant only in AS–SC (Fig. 3A) and not in the other comparisons (Figs. 3B,C, and 4). Although equally complex
pictures were used, the pictures under the AS, PS, and SS
conditions involved more visual cues than those under the
SC conditions regarding two interacting stick ﬁgures (Fig.
1A–D). These results suggest that the left and right pSTG/
MTG play functionally separable roles while receiving andinterpreting relevant information.
The present study also indicated that the activation of
the pre-SMA and bilateral caudate was enhanced in theAS, PS, and SS conditions when compared with the VC
task (Fig. 2), but not in the direct comparisons among theAS, PS, and SS conditions nor in AS–SC (Figs. 3 and 4).
This ﬁnding suggests that these regions play a general rolein linguistic processing. Matsumoto et al. (2004) suggested
a possible indirect pathway between the left IFG and left
pSTG/MTG via subcortical regions. An anatomical study
in primates showed a pre-SMA projection to the head of
the caudate [Inase et al., 1999]; this projection may form
the pre-SMA-basal ganglia loop used in word generation[Crosson et al., 2003]. Previous studies based on an inherited speech disorder also suggested that an inferior frontal-basal ganglia loop is a critical neural circuit for speech
production [Vargha-Khadem et al., 2005]. On the other
hand, it has been proposed that the basal ganglia plays arole in the application of grammatical rules by which morphemes are combined into words (e.g., talk-ed, talk-ing)

1025 rr Kinno et al. r[Ullman, 2001], and a recent neuroimaging study has indicated that in bilinguals the head of the left caudate may
control the language in use at a given moment [Crinion
et al., 2006]. Although many studies have outlined the importance of the basal ganglia in cognitive operations suchas planning and monitoring [Middleton and Strick, 2000],
these previous studies and the present study suggest thatthe pre-SMA and bilateral caudate have a more speciﬁcrole in the language faculties, because such general cognitive factors are completely controlled in our paradigm.
Previous lesion studies have reported aphasics with deﬁcits in sentence comprehension despite adequate lexicosemantic knowledge, i.e., ‘‘agrammatic comprehension’’[Maher et al., 1995; Schwartz et al., 1980]. These studies
used a two-choice picture-pointing task, in which thedemand of lexico-semantic factors was well controlled,
incorporating stick-ﬁgure characterizations of circles andsquares as protagonists in the stimulus pictures. The aphasics judged which of the two pictures correctly depicted an
action scene described by a spoken sentence, such as ‘‘The
square is shooting the circle’’ or ‘‘The circle is shot by thesquare,’’ but they were not always able to interpret thosesentences. The aphasics may have more difﬁculty inunderstanding or producing syntactically complex sentences, such as passive sentences, than canonical active sentences. Our present results provide further supporting evidence for agrammatism, such that grammatical comprehension is separable from domain-general factors.

CONCLUSIONSThe present paradigm utilizing a novel picture-sentence
matching task (Fig. 1) successfully demonstrated the syntactic-selective activation in the left dF3t and left pSTG/
MTG, which also excluded the possible involvement ofgeneral cognitive factors, since these factors cannot explain
the results of direct comparisons between noncanonicaland canonical syntactic processing in both SS–AS and PS–
AS (Figs. 3B,C, and 4). It is a question for future researchwith a design parametrically manipulating task difﬁculty,
whether general short-term memory demands or task difﬁculty have an effect in dF3t and pSTG/MTG if the task
were made more difﬁcult. In this regard, the present
design could be applied to aphasics, since individuals withagrammatism would presumably perform at a much lower
level relative to the normal individuals studied here. The
multiple sentence conditions would also be useful for successfully dissociating any deﬁcits in syntactic processing
for aphasics. Although the agrammatism reported by
Schwartz et al. (1980) was due to extensive lesions, the differential contributions of multiple regions found in thepresent study may allow for more precise identiﬁcationand interpretation of linguistic disorders. Conversely, if apatient’s responses to the various sentence conditions are
similar to one of the three patterns shown in the bar
graphs in Figure 5, it would be possible to narrow downr

the critical regions that could be responsible for such adeﬁcit. The use of multiple sentence conditions will thus
provide, in the near future, a powerful tool for assessing
and screening aphasics, as well as for designing rehabilitation programs for them.

ACKNOWLEDGMENTS
We thank M. Koizumi for his suggestion regarding linguistic issues, N. Saeki for her technical assistance, and S.
Matsukura for her administrative assistance.

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