Neuron, Vol. 35, 1177–1182, September 12, 2002, Copyright 2002 by Cell Press

Selective Priming of Syntactic Processing
by Event-Related Transcranial
Magnetic Stimulation of Broca’s Area
Kuniyoshi L. Sakai,1,2,4 Yasuki Noguchi,1Tatsuya Takeuchi,1 and Eiju Watanabe2,3
1
Department of Cognitive and Behavioral Science
Graduate School of Arts and Sciences
The University of Tokyo, Komaba
3-8-1 Komaba, Meguro-ku
Tokyo 153-8902
2
CREST
Japan Science and Technology Corporation
Kawaguchi-shi 332-0012
3
Department of Neurosurgery
Tokyo Metropolitan Police HospitalTokyo 102-8161
Japan

Summary
It remains controversial whether Broca’s aphasia is anarticulatory deficit, a lexical-access problem, or agrammatism. In spite of recent neuroimaging studies, thecausal link between cortical activity and linguistic subcomponents has not been elucidated. Here we reportan experiment with event-related transcranial magnetic
stimulation (TMS) to clarify the role of Broca’s area, more
specifically, the left inferior frontal gyrus (F3op/F3t),
in syntactic processing. An experimental paradigm
contrasted sentences requiring syntactic decisions
with those requiring semantic decisions. We foundselective priming effects on syntactic decisions when
TMS was administered to the left F3op/F3t at a specifictiming, but not to the left middle frontal gyrus (F2). Our
results provide direct evidence of the involvement of
the left F3op/F3t in syntactic processing.
Introduction
The specialization of syntactic processing in humancognitive systems is one of the central issues in neuroscience, and it has been highly debated from a numberof perspectives based on lesion studies of Broca’s aphasia and functional imaging studies of the prefrontal cortex (Caplan and Waters, 1999; Sakai et al., 2001). The
narrowest definition of Broca’s area is the left pars opercularis (F3op, Brodmann’s area [BA] 44) and the leftpars triangularis (F3t, BA 45), a part of the third frontal
convolution (F3) or the left inferior frontal gyrus (IFG).
However, the syndrome referred to as permanent Broca’s aphasia arises from a considerably larger brain lesion that includes the insula and subjacent white matteras well as the F3op/F3t (Mohr, 1976). The left precentral
gyrus of the insula has been implicated in the motor
planning of speech (Dronkers, 1996). Nevertheless, thefunctional role of the left F3op/F3t still remains unknown.
Transcranial magnetic stimulation (TMS), which is used
to produce physiological effects on neuronal activity,
has been recently applied to the study of various brain
4

Correspondence: sakai@mind.c.u-tokyo.ac.jp

functions (Pascual-Leone et al., 2000; Hallett, 2000). To
clarify the essential role of Broca’s area in syntactic
processing, here we used event-related TMS, administering magnetic pulses time-locked to every stimulus(an “event”). We targeted the left F3op/F3t (Figure 1),
whose activation has been recently reported both in an
implicit syntactic task (Dapretto and Bookheimer, 1999)
and in an explicit syntactic task (Embick et al., 2000).
We tested two language tasks that require specificlinguistic decisions: a syntactic decision (Syn) task anda semantic decision (Sem) task (Figure 2), which weredeveloped in our recent optical topography (OT) study(Noguchi et al., 2002). In the Syn task, subjects judged
whether sentences were either syntactically normal (N)or anomalous (A), while word combinations in each sentence were semantically related. We focused on a universal aspect of syntactic operations that are common
to both English and Japanese: a distinction between
transitive verbs (vt) and intransitive verbs (vi). This distinction is critical in sentence comprehension, because
the choice of a transitive or intransitive verb determines
the syntactic structure of a sentence (Smith and Wilson,
1979). Subjects were explicitly instructed to detect a
syntactic anomaly, but they were not instructed to pay
attention to the distinction between vt and vi. In the Semtask, subjects judged whether sentences were either
semantically normal or anomalous while presented sentences were syntactically correct as to the usage of vt
and vi. Here we focused on the lexico-semantic relationship (selectional restrictions) between a noun and a verb.
In both tasks, the same set of nouns and verbs wereused. Because normal sentences were identical among
these tasks, we tested each task in separate sessions
so that the TMS effect on judging whether a normal
sentence is syntactically correct can be dissociatedfrom that on judging whether the same sentence is semantically correct. In contrast, anomalous sentences
had only one type of linguistic error in each task. Therefore, these stimuli formed minimal pairs for both intratask pairs (N and A sentences) and intertask pairs (anomalous sentences for Syn and Sem). We named thisexperimental design a minimal-pair paradigm.
Results
Event-related TMS was delivered over the left F3op/
F3t at a specific timing (“Real” condition). As a control
condition to the Real condition, the recorded discharge
click without concomitant TMS was presented at thesame volume and timing as each Real condition (“Sham”
condition, the “click” control). Therefore, whether themagnetic stimulus was present or not was the only difference between these two conditions. TMS was delivered at one of three time points in separate sessions(Figure 2): at the onset of a verb stimulus (T ⫽ 0), at 150
ms after the onset (T ⫽ 150), and at 350 ms after the
onset (T ⫽ 350).
The subjects performed the tasks at the accuracy of
92 ⫾ 4.8% (mean ⫾ SD), ranging from 75% to 100%

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Figure 1. The Targeted Regions in the Left
Prefrontal Cortex
Horizontal (A) and coronal (B) MR images indicating the position of the TMS coil for a representative subject. In each panel, the nearest
MR marker to the center of the coil, which
locates over the center of the left F3op/F3t,
is shown (arrow for the stimulated site). The
stimulation sites in the left F3op/F3t and in
the left F2 are labeled as sites I and II, respectively, on the lateral surface image of the MNI
standard brain (C). a, the precentral sulcus;b, the inferior frontal sulcus; c, the superior
frontal sulcus.

across all individuals and conditions. We analyzed thecorrect and incorrect trials separately according to subjects’ responses. Reaction times (RTs, measured fromthe presentation of a verb stimulus) in the correct trials of
all conditions for TMS over the left F3op/F3t are shown in
Table 1. According to an analysis of variance (ANOVA)
with two variables (sentence type ⫻ task; subject as arandom factor) on the Sham data for each time point, there
was no main effect or interaction in any of three time
points (p ⬎ 0.1 for all). Therefore, the two tasks without
TMS were equated in terms of difficulty. To examine the
TMS effects on each task, we pooled individual correct
trials for each TMS condition and calculated ⌬RTs (RTchanges: Real ⫺ Sham) for each subject.
When TMS was delivered at T ⫽ 0, ⌬RTs were notsignificantly different from ⌬RT ⫽ 0 for either N or A
sentences in the Syn task (p ⬎ 0.1, one group t test)
and in the Sem task (p ⬎ 0.5) (Figure 3A). Therefore,
TMS at T ⫽ 0 had no effect on either task. When TMS wasdelivered at T ⫽ 150, ⌬RTs were significantly negative forboth sentence types in the Syn task (N: t(5) ⫽ ⫺3.4, p ⬍0.05; A: t(5) ⫽ ⫺4.5, p ⬍ 0.01), whereas ⌬RTs in the Semtask were not different from ⌬RT ⫽ 0 (p ⬎ 0.1) (Figure
3B). Moreover, ⌬RTs in Syn N and Syn A were negative(range: ⫺45 to ⫺2 ms) for all subjects, whereas thosein Sem N and Sem A were distributed evenly around⌬RT ⫽ 0 (range: ⫺42 to 32 ms). It should be noted thatTMS induced differential effects on physically identical“normal” sentences between the two tasks, which parallel those on anomalous sentences. These results clearly
demonstrated that TMS at T ⫽ 150 over the left F3op/F3t
selectively enhanced syntactic processing. In contrast,
when TMS was delivered at T ⫽ 350, ⌬RTs were notsignificantly different from ⌬RT ⫽ 0 for either N or A
sentences in the Syn task (p ⬎ 0.1) and in the Sem task(p ⬎ 0.5) (Figure 3C). We also confirmed that TMS at
T ⫽ 450 did not result in significant changes of ⌬RTs
under any conditions (p ⬎ 0.1).
To establish the specificity of the effect in the left
F3op/F3t, we obtained data on responses to TMS atanother location in the left prefrontal cortex. We targeteda part of the left middle frontal gyrus (F2, MFG) as acontrol site, whose mean position was 39 mm away (seeExperimental Procedures) from the region of the left
F3op/F3t on the cortical surface (Figure 1C). When TMS
was delivered at T ⫽ 150 over the left F2, which was a
critical timing for syntactic processing in the left F3op/
F3t, ⌬RTs were not significantly different from ⌬RT ⫽ 0
for either N or A sentences in the Syn task (p ⬎ 0.1) andin the Sem task (p ⬎ 0.1) (Figure 4). RTs in the correct
trials of all tested conditions for TMS over the left F2
are shown in Table 2. These results clarified that the left
F3op/F3t, but not the left F2, is specialized in syntactic
processing, demonstrating functional parcellation within
the left prefrontal cortex. We further applied the same
analyses to RTs for incorrect trials (excluding time-out

Selective Syntactic Priming by Event-Related TMS
1179

Figure 2. Language Tasks with a Minimal Pair Paradigm
Normal (N) sentences used in the two tasks were physically identical.
In a syntactic decision (Syn) task, syntactically anomalous (Syn A)
sentences were intermixed with normal sentences. In a semantic
decision (Sem) task, semantically anomalous (Sem A) sentenceswere intermixed with normal sentences. Arrows on the time scale
indicate three time points of TMS: T ⫽ 0, 150, and 350 ms from thepresentation of a verb. Acc, accusative case particle; vt, transitive
verb; vi, intransitive verb.

trials) and accuracy data, and we observed no significant ⌬RT or ⌬accuracy (accuracy changes: Real ⫺Sham) under any conditions (p ⬎ 0.05).
Discussion
The results are striking in three ways: (1) event-related
TMS pulses selectively reduced RTs in explicit syntactic
decisions but not in explicit semantic decisions, which
is an unexpected phenomenon for known TMS effects
on cognitive processes, (2) this effect was observed
during syntactic decisions regarding both normal andanomalous sentences, and (3) it was observed whenmagnetic stimulation was administered to the left F3op/
F3t at a specific timing (150 ms from a verb stimulus),
but not to the left F2. The present TMS study thus demonstrates the causal link between syntactic processing
and activation of the left F3op/F3t, indicating how syntactic processing is specialized and instantiated in thebrain.
Our results are consistent with previous functional
imaging studies, which have implicated selective activation of the left F3op/F3t during syntactic processing
in comparison with semantic processing (Dapretto andBookheimer, 1999; Ni et al., 2000). Recent neuroimaging

Figure 3. Selective Priming Effects of TMS on Syntactic Processing
at the Left F3op/F3t⌬RT (mean and standard error across subjects) indicates the changeof RTs (Real ⫺ Sham) elicited by the TMS. Each bar denotes ⌬RTfor either normal (N) or anomalous (A) sentences. TMS was deliveredat one of three time points: 0 ms (A), 150 ms (B), and 350 ms (C) fromthe presentation of a verb. *p ⬍ 0.05, **p ⬍ 0.01 (t test, n ⫽ 6).

studies have accumulated consistent evidence of theinvolvement of the left F3op/F3t in various cognitive
tasks including syntactic processing (Stromswold et al.,
1996; Just et al., 1996; Embick et al., 2000; Moro etal., 2001; Indefrey et al., 2001). In these studies, theknowledge of English, German, or Italian languages wastested in native speakers. The consistency among thesestudies and the present study using Japanese, a nonIndo-European language, suggests that syntactic specialization of the left F3op/F3t is universal among natural

Table 1. TMS Effects on RTs for Two Language Tasks at the Left F3op/F3t
T⫽0

T ⫽ 150T ⫽ 350

Stimulus Type

Task

Real

Sham

Real

Sham

Real

Sham

Normal (N)

Syn
Sem
Syn
Sem

600 ⫾ 41618 ⫾ 38639 ⫾ 40645 ⫾ 45612 ⫾ 32619 ⫾ 27643 ⫾ 32647 ⫾ 33601 ⫾ 30645 ⫾ 33640 ⫾ 31669 ⫾ 37615 ⫾ 29651 ⫾ 27665 ⫾ 31676 ⫾ 33626 ⫾ 32646 ⫾ 27664 ⫾ 32670 ⫾ 30616 ⫾ 25647 ⫾ 33675 ⫾ 39674 ⫾ 35

Anomalous (A)Values are in ms, mean ⫾ standard error across subjects (n ⫽ 6).

Neuron1180

Figure 4. The Absence of TMS Effects on the Language Tasks at
the Left F2
Each bar denotes ⌬RT for either N or A sentences. TMS was delivered at 150 ms from the presentation of a verb.

languages. The present TMS results clearly establishedthat activation of the left F3op/F3t underlies syntactic
processing.
We found that the TMS effects on normal and anomalous sentences were similar in each task (Figure 3),
which was in agreement with the left F3op/F3t activation
observed in our event-related OT study (Noguchi et al.,2002). These results consistently indicate that common
processes were involved both in judging a sentence tobe normal and in judging it to be anomalous for eachtask. Therefore, explicit syntactic processing subsists
not only in detecting syntactic anomalies per se, which
has been tested in previous functional MRI studies, but
in analyzing syntactic consistency in a sentence. Thisfinding was achieved by utilizing event-related TMS,
thereby differentiating trials with normal and anomalous
sentences. Even if “normal” sentences are physically
identical between the contrasting tasks, we demonstrated that TMS on normal sentences resulted in differential effects that paralleled the effects for anomalous
sentences, depending on the types of explicit linguistic
decisions.
The temporally restricted and syntax-selective reduction of RTs reported here suggests physiological effectsof facilitation or priming, such that the stimulation of theleft F3op/F3t at a specific timing enhances its normal
function. Indeed, the mean reduction of RTs at T ⫽ 150(N: 14 ms, A: 25 ms) was comparable to that of a previous
behavioral study in which RTs for lexical decision werereduced when primed by a syntactically appropriate
word (Goodman et al., 1981). In contrast, it has beenreported that TMS applied to V5 enhanced performanceat a wide time range (ⵑ250 ms), when its normal functionof motion processing was not required in a detection
task (Walsh et al., 1998). Thus the underlying mechanisms of this paradoxical facilitation may not be directly
relevant to the present study. On the other hand, cortico-

cortical inhibition has been reported in the primary motor
cortex when TMS is applied in pairs of a subthresholdconditioning pulse and a suprathreshold pulse with aninterstimulus interval (ISI) of less than 5 ms (Kujirai et al.,1993). However, such an inhibitatory effect disappeared
when the first pulse was set to the motor threshold(Trompetto et al., 1999), and the effect of subthresholdpaired pulses has not been previously reported. It is
possible that a focal TMS temporarily raises the overall
excitability of neurons, which leads to more effective
activation when specific responses of those cells are
required for syntactic decisions.
While it has been reported that repetitive TMS (rTMS)(4–25 Hz, 1–10 s) over Broca’s area induced speecharrest (Pascual-Leone et al., 1991; Epstein et al., 1996;
Stewart et al., 2001), rTMS (20 Hz, 2 s) over Wernicke’s
area resulted in reduction of RTs in a picture-namingtask (Mottaghy et al., 1999). A recent study reported
that rTMS (1 Hz, 300 s) over the left F2, just anteriorand superior to Broca’s area, increased RTs for verb
production in contrast to noun production (Shapiro etal., 2001). Because rTMS causes the spread of corticalexcitation (Pascual-Leone et al., 1993), spatial resolution
becomes lower than the maximum resolution of singlepulse or paired-pulse TMS (a few millimeters) (Walshand Cowey, 2000). Moreover, because rTMS requires alonger time for stimulation than neural events, temporal
resolution also becomes lower than the maximum resolution of single-pulse or paired-pulse TMS (ⵑ20 ms)(Pascual-Leone et al., 2000). The present study with
event-related TMS, in which paired pulses were timelocked to every stimulus, took the full advantage of its
spatio-temporal resolution, thereby narrowing the time
window for the priming effects within ⫾150 ms. Because
we observed no inhibitatory effects on any conditions,
possible interferences of TMS with reading processes
are excluded in the present study, in spite of the factthat rTMS causes speech arrest. Furthermore, it opens
a new possibility for the use of TMS in neuroscience,
not only for a blockade of sensory processes, but for aselective enhancement of higher cognitive processes
with a restricted spatio-temporal window.
Experimental Procedures
Subjects
Six male native Japanese speakers (age: 22–49) participated in all
the TMS experiments. All subjects showed right-handedness (laterality quotient: 81–100) by the Edinburgh inventory (Oldfield, 1971).
During the experiments, their heads were held in place with a TMS
coil and a chin rest. Informed consent was obtained from eachsubject after the nature and possible consequences of the studies
were explained. All experiments strictly followed the safety guidelines of TMS experiments (Wassermann, 1998) and those adaptedby Japan Neuroscience Society. Approval for these experiments
was obtained from the institutional review boards of the Universityof Tokyo, Komaba.

Table 2. TMS Effects on RTs at the Left F2 (T ⫽ 150)
Stimulus Type

Task

Real

Sham

Normal (N)

Syn
Sem
Syn
Sem

639 ⫾ 32667 ⫾ 37668 ⫾ 26713 ⫾ 44634 ⫾ 21673 ⫾ 34672 ⫾ 23704 ⫾ 37

Anomalous (A)Values are in ms, mean ⫾ standard error across subjects (n ⫽ 6).

Visual Stimuli
Sentence stimuli were visually presented to native Japanese speakers. For each trial, a noun phrase stimulus (a noun and a caseparticle) was presented against a dark background, which was followed by a verb stimulus (Figure 2). Each stimulus (visual angle:3⬚ ⫻ 9⬚) was presented for 200 ms and was always three letters(three syllables or moras) in hiragana to ensure constant reading
time. All presented words were frequently used and commonly writ-

Selective Syntactic Priming by Event-Related TMS
1181

ten in hiragana alone. The intertrial interval was 6 s, and subjects
were asked to fixate on a central cross and to respond by pressing
one of two buttons as quickly as possible while ensuring correct
responses.
Tasks
Before the experiments, we explicitly explained the nature of thetwo tasks to the subjects, providing examples of Syn A, Sem A, and
Syn N/Sem N with the following instruction (Figure 2): “The sentence‘yuki-wo tsumoru’ (snow-Acc lie; Acc, the accusative case particle)
is anomalous because of the syntactic violation between a verb
and a noun phrase. Because ‘yuki’ (snow) and ‘tsumoru’ (lie) aresemantically associated, as ‘yuki-ga tsumoru’ (Snow lies [on the
ground]) is acceptable, it is not a semantic but a syntactic error. In
contrast, the sentence ‘yuki-wo shikaru’ (snow-Acc scold) is anomalous because of the semantic mismatch between ‘yuki’ (snow) and‘shikaru’ (scold). Because this sentence is syntactically correct as
to the relationship between a verb and a noun phrase, this is not a
syntactic but a semantic error. Finally, the sentence ‘yuki-wo sawaru’ (snow-Acc touch) is normal because it is both syntacticallyand semantically correct.”
The Syn and Sem tasks were performed in separate sessions,each of which contained 60 consecutive trials with randomized N
or A sentences. Before each session, the subjects were explicitly
informed about which task they should have performed. In the Syntask, we instructed: “Press the green button if the presented sentence is syntactically correct; press the red button if it is syntacticallyincorrect.” In the Sem task, we instructed: “Press the green button
if the presented sentence is semantically correct; press the red
button if it is semantically incorrect.” Other details of the tasks were
described in our previous paper (Noguchi et al., 2002). For eachsession, TMS was delivered at one of three time points: T ⫽ 0, 150,
and 350 ms from the presentation of a verb (Figure 2). Six sessions
were tested in a 1 day experiment, and they were repeated tentimes for each subject. The order of the session sequences wascompletely counterbalanced within and across subjects.
Magnetic Stimulation
Before the experiments, a 3D magnetic resonance (MR) image ofthe brain was taken of each subject, who wore a cap with multiple
MR markers (alfacalcidol beads; diameter: 3 mm) on its surface.
Using the MR image, the vertically projected position of the centerof the left F3op/F3t (close to the vertical ramus of the sylvian fissure)on the scalp surface (site I) was estimated relative to these markers(Figures 1A and 1B). This position was then transferred to the distances from the lateral canthus and from the acoustic meatus, andit was marked on a headband around the subject’s head. TMS wasdelivered through a focal 8-shaped coil (dual 70 mm coil), which
was placed tangentially on the scalp with the coil’s center fixatedon the marked position. The control site (site II) of the left F2 was
40 mm anterior (parallel to the canthus-meatus line) and 40 mm
dorsal (perpendicular to the canthus-meatus line) to site I on thescalp surface. The distance (mean ⫾ SD across subjects) between
the two sites (I and II) was 39 ⫾ 4.9 mm on the cortical surface. With
SPM99 software (Wellcome Department of Cognitive Neurology,
London, UK), each individual brain was spatially normalized to thestandard brain space as defined by the Montreal Neurological Institute (MNI) (Figure 1C). Stereotactic coordinates (x, y, z; mean ⫾ SD
across subjects) of the sites I and II were (⫺63 ⫾ 1.1, 11 ⫾ 5.7, 15 ⫾4.4) and (⫺42 ⫾ 4.0, 25 ⫾ 4.5, 48 ⫾ 3.5), which corresponded to
BA 44 and BA 8/9, respectively. These SDs reflected the overall
spatial errors of the current method.
In order to increase the power of TMS, we used paired pulses(equal intensity; ISI, 2 ms) by combining two Magstim 200 stimulators with a bistimulation module (Magstim, Carmarthenshire, UK).
TMS intensity of paired pulses was set at 33%–50% (mean: 42%
across subjects) of the maximum output of each stimulator. Thisintensity corresponded to 55%–98% (mean: 75%) of the tonically
active motor threshold (10% maximal voluntary contraction) for
paired pulses, which was measured from electromyographic responses in the contralateral first dorsal interosseous muscle (Teraoet al., 1998). The same TMS intensity was used at both sites I and II
for each subject. Under the Sham condition, the recorded discharge

click without concomitant TMS was presented at the same volume
and timing as each Real condition, while maintaining tangential coilplacement. Sixty consecutive trials in each session were divided
into four epochs, each of which contained either Real or Sham trials,
and their order was either R-S-S-R or S-R-R-S (R: Real, S: Sham).
Both RTs and accuracy were recorded online, while the visual stimulus presentation and TMS application (or discharge click) with aparticular delay were controlled using LabVIEW software and interface (National Instruments, Austin, TX).
Acknowledgments
This study was supported by a Core Research for Evolutional Science and Technology (CREST) grant from Japan Science and Technology Corporation and by a Young Investigators’ Grant from Human
Frontier Science Program (HFSP) to K.L.S. We would like to thank
Alec Marantz for encouragement; Yoshikazu Ugawa for his technicaladvice on TMS; Noriaki Yahata, Ryuichiro Hashimoto, Fumitaka Homae, Kei Suzuki, and Yasuki Hashimoto for their technical assistance; and Hiromi Matsuda for her administrative assistance.
Received: January 22, 2001
Revised: June 7, 2002
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