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NeuroImage 37 (2007) 1417 – 1426

Comprehension of implicit meanings in social situations involving

irony: A functional MRI study
Keisuke Wakusawa, a,b,⁎ Motoaki Sugiura, a,c Yuko Sassa, a,d Hyeonjeong Jeong, a
Kaoru Horie, e Shigeru Sato, e Hiroyuki Yokoyama, b Shigeru Tsuchiya, b
Kazuie Inuma, f and Ryuta Kawashima a,d
a
Department of Functional Brain Imaging, Institute of Development, Aging and Cancer, Tohoku University, Sendai, Japan
b
Department of Pediatrics, Tohoku University Graduate School of Medicine, Sendai, Japan
c
Department of Cerebral Research, National Institute for Physiological Sciences, Okazaki, Japan
d
Research Institute of Science and Technology for Society, Japan Science and Technology Corporation, Kawaguchi, Japan
e
LBC Research Center, Tohoku University 21st Century Center of Excellence Program in Humanities, Tohoku University, Sendai, Japan
f
Ishinomaki Red Cross Hospital, Ishinomaki, Japan
Received 5 February 2007; revised 5 June 2007; accepted 6 June 2007
Available online 27 June 2007

To understand implicit social meanings, the interaction of literal Introduction

meanings and relevant information in a situational context is important.
However, previous studies have not investigated such contextual
interactions. Using functional magnetic resonance imaging (fMRI), we
investigated cortical mechanisms underlying the processing of implicit
meanings, particularly irony, in realistic social situations, focusing on
contextual interactions. Healthy subjects were shown pictures depicting
daily communicative situations during judgment tasks involving
situational appropriateness and literal correctness. The left medial
prefrontal cortex showed significantly greater activation during tasks
involving situational judgments than during literal judgments. The right
temporal pole was activated task-independently during irony-specific
processing. The medial orbitofrontal cortex was activated task-
dependently during irony processing in situational judgment tasks.
These regions have been reported to be involved in theory of mind, and
have not been implicated in previous studies on the linguistic processing
of implicit meanings. This suggests that the intentional assessment of
situational appropriateness for task execution is carried out in the left
medial prefrontal cortex, whereas irony is processed in the right
temporal pole by assessing situational context automatically, and is
judged based on the situational context in the medial orbitofrontal
cortex. Our results show that the processing of implicit meanings and
irony in contextually rich situations depends on brain mechanisms in-
volved in the “theory of mind,” based on processing relevant
information in a situational context, and suggest different functions in
each region.
© 2007 Elsevier Inc. All rights reserved.
⁎ Corresponding author. Department of Functional Brain Imaging,
Institute of Development, Aging and Cancer, Tohoku University, Seiryo-
machi 4-1, Aoba-ku, Sendai 980-8575, Japan. Fax: +81 22 717 8499.
E-mail address: kwakusawa@idac.tohoku.ac.jp (K. Wakusawa).
Available online on ScienceDirect (www.sciencedirect.com).
1053-8119/$ - see front matter © 2007 Elsevier Inc. All rights reserved.
doi:10.1016/j.neuroimage.2007.06.013
In daily communication, verbal expressions may imply mean-
ings opposite to, or different from, their literal meaning. Com-
prehension of such implicit meanings may require integration of
the literal meaning into the social context of the communicative
situation. Sperber and Wilson (1995) suggested that interaction of
literal meanings and contextually available “relevant” information
was an important aspect in understanding the speaker's intended
implicit meaning.
This is particularly true for irony; indeed, the negative eval-
uation of the situation that the speaker is commenting on in this
respect is an essential context for the comprehension of the negative
connotation mediated by irony. However, despite the potential
importance of the social situation in the comprehension of implicit
meanings, previous cognitive neuroscience research has focused
only on linguistic aspects of such expressions (Tompkins and
Flowers, 1987; Kaplan et al., 1990; Winner et al., 1998; Giora et al.,
2000; Eviatar and Just, 2006; Wang et al., 2006a).
Previous psychological studies have shown a correlation
between comprehension of implicit meanings and theory of mind
(ToM) or mentalizing (Happé, 1993; Ozonzoff and Miller, 1996;
Baron-Cohen et al., 1999; Channon et al., 2004). ToM is the ability
to attribute mental states to one's self and to others, in com-
prehending the mental states of others (Baron-Cohen et al., 1985).
Comprehension of irony, in particular, has been suggested to be
closely related to ToM. Happé (1993) showed that a higher level of
ToM was necessary to understand irony than to comprehend other
implicit meanings, such as metaphors and similes, whereas idio-
matic expressions, such as conventional metaphors, are processed
similarly to other common words (Swinney and Cutler, 1979). This
may be explained by the higher level of processing in relation to
1418 K. Wakusawa et al. / NeuroImage 37 (2007) 1417–1426
social context necessary to comprehend irony, as opposed to the
metaphors, similes, and idioms.
Our study was designed to examine the cortical mechanisms
underlying the processing of implicit meanings, which are mediated
by communications in realistic social situations rich in social con-
textual information, by means of functional magnetic resonance
imaging (fMRI) in healthy adult subjects.
Using photographs of daily situations as stimuli, we investigated
neural responses to implicit social meanings mediated by social
situations. Stimulus pictures depicted communicative situations in
which one person made an ironic or metaphoric statement to
another. To reveal specific neural correlates for irony processing, we
compared the neural response to an ironic expression with that to a
metaphoric expression. Here, irony is an expression that conveys a
meaning opposite to its literal meaning, with a negative connota-
tion, and metaphor is limited to expressions consisting of con-
ventional phrases, such as idiomatic expressions or proverbs. Direct
comparison between the cortical mechanisms for irony processing
and those for conventional metaphor processing has previously
been made in linguistic studies using fMRI (Eviatar and Just, 2006;
Uchiyama et al., 2006). However, the stimulus in those studies
involved a relatively limited situational context. In contrast, using
photographs, the situational contexts of stimuli in our study were
enriched, as in real-life situations. Thus, the interaction of literal
meanings and situational contexts were better reflected in our
examination than in previous studies, and while both irony and
conventional metaphor have meanings different from their literal
denotations, situational integration is more critical in understanding
irony than conventional metaphors.
We investigated two aspects of the processing of implicit social
meaning using a block design and event-related analyses. First, we
believed that intentional processing of implicit social meanings
should be reflected in task-dependent activation. Using a block
design analysis, we contrasted the situational appropriateness judg-
ment task with the literal correctness judgment task to examine the
intentional processing, because processing of implicit social mean-
ings is essential for the judgment of situational appropriateness, but
irrelevant for ascertaining literal correctness. Second, we differ-
entiated stimulus-specific responses to irony and metaphor by
event-related analysis for each stimulus type. Such stimulus-
specific responses may be task-dependent (observed during the
situational judgment task only) or task-independent (observed
regardless of the task).
Considering the close relationship between the task requirement
in this study and ToM, we predicted involvement of the medial
frontal region, the temporal pole, and the superior temporal sulcus,
in which activation has been shown by functional imaging studies
of ToM (Frith and Frith, 2003).
Materials and methods
Subjects
Thirty-eight healthy, right-handed, Japanese volunteers (21 males
and 17 females, aged 18–38 years, mean = 22.3 years) participated in
this experiment. All subjects had normal vision and none had a
history of neurological or psychiatric illness. Handedness was eval-
uated using the Edinburgh Handedness Inventory (Oldfield, 1997).
Written informed consent was obtained from all subjects accord-
ing to the guidelines of the Ethics Committee of Tohoku Univ-
ersity and the Declaration of Helsinki (1991).
Stimuli
A series of stimulus pictures describe daily communicative
situations with two actors; an utterance by one actor to the other is
shown in a balloon (Fig. 1). The utterances include the expression
of irony [i.e., stating the opposite in relation to a given situation to
imply a negative message (Irony); Fig. 1a], or conventional meta-
phor [i.e., an idiomatic expression or proverb that is literal nonsense
but is routinely used in daily life (Metaphor); Fig. 1b].
To control for the effect of a situation presented in a picture per
se, a stimulus using the same picture but with a different utterance
was prepared for each of the Irony and Metaphor stimuli, in which
the utterance was literally correct but situationally inappropriate
(IronyCon and MetaphorCon, respectively) (Figs. 1c, d). The num-
bers of characters in the balloons were adjusted between Irony and
IronyCon, and between Metaphor and MetaphorCon. As foils,
stimuli in which the utterance was both situationally and literally
appropriate (Appropriate) (Fig. 1e) or inappropriate (Inappropriate;
Fig. 1f) were also prepared. Fourteen stimuli for each of Irony,
Metaphor, IronyCon, and MetaphorCon, and 28 for each of Appro-
priate and Inappropriate, were selected from the original candidate
stimuli (48 for each of Irony and Metaphor, 48 for each of IronyCon
and MetaphorCon, and 90 for each of Appropriate and Inappropri-
ate) on the basis of the preliminary screening test. In this test, seven
or more out of eight subjects correctly evaluated that Irony stated
the opposite meanings in relation to a given situation, to imply a
negative message, and Metaphor was an idiomatic expression or
proverb that is literal nonsense but is routinely used in daily life.
Literal correctness and situational inappropriateness of IronyCon,
MetaphorCon, and situational and literal appropriateness of Appro-
priate, inappropriateness of Inappropriate were also checked.
Mosaic pictures with a balloon showing “press the right button”
or “press the left button” served as the control for low-level visual
processing and motor output (Control; Fig. 1g). Each stimulus was
back-projected onto a semi-translucent screen attached to the head
coil of a magnetic resonance imaging scanner; the subject viewed
the stimuli via a mirror.
Tasks
Each subject performed the SITUATIONAL and LITERAL
tasks alternately. In the SITUATIONAL task, each subject was
instructed to press the left button with the right index finger when
he/she had determined that the presented utterance was situationally
appropriate, and to press the right button with the middle finger
when he/she had determined otherwise. In the LITERAL task, each
subject was instructed to press the left button with the right index
finger when he/she had determined that the presented utterance was
a literally correct description of the given situation, and to press the
right button with the middle finger when he/she had determined
otherwise. During a blocked presentation of the Control stimuli,
each subject pressed a button according to the instruction in the
balloon (CONTROL task). In each block for the SITUATIONAL
and LITERAL tasks, either an Irony or a Metaphor stimulus alone
was intermingled among IronyCon, MetaphorCon, and foils. This
enabled us to separately analyze an Irony stimulus and a Metaphor
stimulus in the blocked design. The task design is schematically
presented in Fig. 2.
Each stimulus was presented for 3.5 s with an interstimulus
interval of 1.5 s. Each block consisted of seven trials starting with a
visual instructional presentation for 4 s, followed by an eye-fixation
 K. Wakusawa et al. / NeuroImage 37 (2007) 1417–1426 1419

Fig. 1. Examples of stimuli. The utterances in balloons were written in Japanese with English translations shown beneath the pictures. (a) Irony: The utterance
was literally opposite to the given situation in order to imply a message. (b) Metaphor: The utterance was an idiomatic expression that is literally nonsense. (c)
IronyCon: The given situation (picture) was the same as that for Irony, but the utterance was literally correct and situationally inappropriate. (d) MetaphorCon:
The given situation (picture) was the same as for Metaphor, but the utterance was literally correct and situationally inappropriate. (e) Appropriate: The utterance
was both situationally and literally appropriate. (f) Inappropriate: The utterance was both situationally and literally inappropriate. (g) Control: the mosaic pictures
with a balloon showed either “push the right button” or “push the left button.”

rest of 17 s. Five types of blocks, SITUATIONAL tasks during
presentation of stimuli including Irony (SITUATIONAL_I) and
those including Metaphor (SITUATIONAL_M), LITERAL tasks
during presentation of stimuli including Irony (LITERAL_I) and
those including Metaphor (LITERAL_M), and CONTROL tasks,
were repeated four times during the task period of 1127s (Fig. 2).
The order of the blocks was counterbalanced across the subjects.
fMRI measurement
Forty-four transaxial gradient-echo images (echo time = 50 ms,
flip angle = 90°, slice thickness = 2.2 mm, slice gap = 0.77 mm,
FOV = 192 mm, matrix = 64 × 64) covering the entire brain were
acquired at a repetition time of 4 s, using an echo planar sequence
and a Siemens Symphony (1.5 T) (Siemens, Erlangen, Germany)
MR scanner. Excluding four dummy scans for stabilization of the
T1-saturation effect, 281 volumes were acquired in each fMRI
session. An anatomical T1-weighted data set (thickness, 1 mm;
FOV, 256 mm; data matrix, 192 × 224; TR = 1900 ms; TE = 3.93 ms)
was acquired from each subject.
Preprocessing
The following preprocessing procedures were performed using
Statistical Parametric Mapping (SPM2) software (Wellcome
Department of Cognitive Neurology, London, UK) and MATLAB
(Mathworks, Natick, MA, USA): adjustment of acquisition timing
across slices, correction for head motion, spatial normalization
using the anatomical image and the MNI template, and smoothing
using a Gaussian kernel with a full-width half-maximum of 9 mm.
Data from seven subjects (three males and four females) with ex-
cessive head motion (more than 3 mm) or dubious task performance
1420 K. Wakusawa et al. / NeuroImage 37 (2007) 1417–1426

Fig. 2. Task design and models for analyses. The task schematically presented at the top. The task and stimulus types are illustrated in the thickness of the frame
line and in color. The order of the tasks is SITUATIONAL_I, LITERAL_I, SITUATIONAL_M, LITERAL_M, and CONTROL. The presented set of tasks was
repeated four times. The model of expected BOLD signal change is presented for five block types and for 4 of 13 event types.

(less than 80% correct responses) were excluded. Thus, data from
31 subjects (18 males and 13 females) were analyzed.
Analysis
Two conventional two-level approaches to fMRI data analysis
were performed using different models (Fig. 2). We used a block
design to identify cortical areas involved in task-dependent
processing, that is, intentional comprehension of implicit social
meanings. We employed an event-related design to detect a neural
response to an Irony or Metaphor stimulus, which reflects a
stimulus-specific process. In both approaches, a voxel-by-voxel,
multiple regression analysis of the expected signal change was
applied to preprocessed images for each subject. Each analysis
employed a standard convolution model using the hemodynamic
response function provided by SPM2. Statistical inference on con-
trasts of parameter estimates was then performed with a second-
level, between-subject (random effects) model using a one-sample
t-test. In the first analysis for examining sustained top-down activ-
ation associated with the tasks, we adopted five block conditions:
SITUATIONAL_I, SITUATIONAL_M, LITERAL_I, LITERAL_M,
and CONTROL, employing a boxcar function at the first in-
trasubject-level analysis. To identify cortical areas exhibiting
greater activation during the SITUATIONAL task than during the
LITERAL task, a contrast (SITUATIONAL_I + SITUATIONAL_M)–
(LITERAL_I + LITERAL_M) was tested. This contrast was masked
by contrasts SITUATIONAL_I–LITERAL_I and SITUATIONAL_M–
LITERAL_M to ensure that activation was not specific to an Irony
or a Metaphor stimulus, and by contrasts SITUATIONAL_I–
CONTROL and SITUATIONAL_M–CONTROL to avoid pseu-
doactivation due to deactivation during the LITERAL task. To
separately identify greater activation during the SITUATIONAL
task than during the LITERAL task for the Irony and Metaphor
stimuli, contrasts SITUATIONAL_I–LITERAL_I and SITUATIO-
NAL_M–LITERAL_M, respectively, were masked by contrasts
SITUATIONAL_I–CONTROL and SITUATIONAL_M–CON-
TROL. These masks enabled us to avoid pseudoactivation due
to deactivation during the LITERAL_M task or the LITERAL_I
task.
In the second analysis, we modeled six stimulus types (Irony,
IronyCon, Metaphor, MetaphorCon, Appropriate, Inappropriate), in
each of the SITUATIONAL and LITERAL tasks (denoted by
suffixes “_S” and “_L,” respectively, on each stimulus abbreviation).
Including the Control trial (Control stimulus/CONTROL task), the
models were of 13 trial types. A standard event-related hemody-
namic function was employed. Thus, to identify cortical areas that
respond to Irony stimuli, the contrast Irony_S–IronyCon_S
(pictures were controlled between these trials) was masked by the
contrasts Irony_S–Appropriate_S, and Irony_S–Control. By mask-
ing with the contrast Irony_S–Appropriate_S, we excluded the
effect of different response types (that is, appropriate/inappropriate).
Masking with the contrast Irony_S–Control enabled us to avoid
pseudoactivation due to deactivation in IronyCon_S. Similarly, to
identify cortical areas that respond to a Metaphor stimulus, the
contrast Metaphor_S–MetaphorCon_S was masked by the contrasts
Metaphor_S–Appropriate_S and Metaphor_S–Control.
For each voxel-by-voxel test, the statistical threshold was set to
p b 0.001 for height, corrected to p b 0.05 for multiple comparisons
using the cluster size. For the masks, p b 0.05 for height was
applied. A small volume correction was adopted for activation in
the following regions in which we had a priori hypotheses (Frith
and Frith, 2003), using box-shaped search areas (shown in []): the
medial prefrontal cortex [−20 ≤ x ≤ 20, 40 ≤ y ≤ 70, and 10 ≤ z ≤
50], the temporal pole [−60 ≤ x ≤ −30, −5 ≤ y ≤ 25, and − 40 ≤ z ≤
− 10], and superior temporal sulcus [25 ≤ x ≤ 65, − 70 ≤ y ≤ −40,
and 0 ≤ z ≤ 30].
 K. Wakusawa et al. / NeuroImage 37 (2007) 1417–1426 1421

The region of interest (ROI) analysis dealt with the activation
profile for each activated area, that is, the estimated activation
(partial regression coefficient) generated at the peak voxel in the
activated areas revealed by voxel-by-voxel analysis.
For the activation peaks in the block design analysis, the differ-
ential estimated activation in the contrast SITUATIONAL–
LITERAL for six stimuli (Irony_S–_L, IronyCon_S–_L, Meta-
phor_S–_L, MetaphorCon_S–_L, Appropriate_S–_L, and Inap-
propriate_S–_L) was analyzed using two-way analysis of variance
(ANOVA), including the effects of stimulus type (6) and subjects
(31) to determine whether the observed activation is caused by the
response to a specific stimulus type, rather than by a task-related
process.
For the activation peaks in the event-related design analysis, the
estimated activation for 12 stimuli (Irony_S, IronyCon_S, Irony_L,
IronyCon_L, Metaphor_S, MetaphorCon_S, Metaphor_L, Meta-
phorCon_L, Appropriate_S, Inappropriate_S, Appropriate_L, and
Inappropriate_L) against the Control stimuli was compared. The
contrasts of interest were Irony_S–IronyCon_S, Irony_L–Irony-
Con_L, Metaphor_S–MetaphorCon_S, and Metaphor_L–Meta-
phorCon_L for the purpose of examining the question of whether
each regional activation for Irony or Metaphor processing depended
on the task-type. For comparison of estimated activation between
conditions in the peak voxel, we adopted a lenient threshold of
p b 0.05 (without correction for multiple comparisons).
Results
Behavioral data
The mean reaction times for the SITUATIONAL_I, SITUATIO-
NAL_M, LITERAL_I, LITERAL_M, and CONTROL conditions
were 2222 ± 371, 2122 ± 320, 2239 ± 334, 2199 ± 263, and 933 ±
163 ms, respectively. Two-way ANOVA (task type × subject)
revealed a significant main effect of task type (F4,124 = 405.73, p b
0.05). The reaction time was significantly shorter under CONTROL
than the other four conditions and under the SITUATIONAL_M
condition than under the LITERAL_I condition (p b 0.05, Tukey–
Kramer test).
The mean reaction time and the mean percentage of correct
responses for each trial type (as used in the event-related analysis)
are shown in Table 1. Two-way ANOVAs (stimulus type × subject)
for the reaction time and the percentage of correct responses both
revealed significant main effects of trial type (reaction time:
F 12,372 = 84.69, p b 0.05, percentage of correct responses:
F12,372 = 5.35, p b 0.05). The contrasts of interest were (1) those
related to the analyses of the activation for irony processing (com-
parisons of Irony_S with IronyCon_S, Irony_S with Appropriate_S,
Table 2
Activated region, determined by block design analysis: implicit social
meaning
Anatomical region Talairach coordinates t-value Cluster
(x, y, z) size (mm3)
Left medial − 10, 58, 24 4.57 424
prefrontal cortex
Coordinate and t-value for the peak voxel of significantly (t N 3.39,
p b 0.001, corrected to p b 0.05 by cluster size) activated regions are given
for the contrast (SITUATIONAL_I + SITUATIONAL_M)–(LITERAL_I +
LITERAL_M).
and Irony_S with Control), and (2) those related to the analyses of
the activation in metaphor processing (comparisons of Metaphor_S
with MetaphorCon_S, Metaphor_S with Appropriate_S, and
Metaphor_S with Control). The reaction time was significantly
shorter in Irony_S than in IronyCon_S (p b 0.05, Tukey–Kramer
test), and longer in Irony_S than in Appropriate_S and Control
(p b 0.05, Tukey–Kramer test). The reaction time in Metaphor_S
did not differ significantly from those in MetaphorCon_S and
Appropriate_S, but was significantly longer than that in Control
(p b 0.05, Tukey–Kramer test). The percentage of correct responses
was significantly lower in Irony_S than in Control (p b 0.05,
Tukey–Kramer test).
Block design analysis
Statistically significant activation determined by the block
design analysis is presented in Table 2 and Fig. 3. The left medial
prefrontal cortex was activated during the SITUATIONAL task in
contrast to the LITERAL task. No statistically significant activation
was observed in the contrast SITUATIONAL_I–LITERAL_I or
SITUATIONAL_M–LITERAL_M tasks.
The results of ROI analysis for this region are also shown in Fig.
3c. Two-way ANOVA (stimulus type × subject) for differential
SITUATIONAL–LITERAL activation revealed no statistically
significant effect of stimulus type (F5,150 = 0.12, p = 0.99).
Event-related design analysis
Statistically significant activation determined by event-related
analysis is shown in Table 3 and Fig. 4. Statistically significant
activation in the contrast Irony_S–IronyCon_S was seen in the
medial orbitofrontal cortex and the right temporal pole, but was not
observed in the contrast Metaphor_S–MetaphorCon_S.
The results of ROI analysis of these two regions are also shown
in Figs. 4d and e. In the medial orbitofrontal cortex, activation was
greater under the Irony_S condition than under the IronyCon_S

Table 1
Mean reaction times and percentage of correct responses for each trial type
Task/trial Irony IronyCon Metaphor MetaphorCon Appropriate Inappropriate
SITUATIONAL (_S) 2190 ± 393 2403 ± 497 2123 ± 353 2193 ± 466 1950 ± 313 2181 ± 380
90.63 ± 0.09 89.73 ± 0.07 92.41 ± 0.11 86.61 ± 0.08 95.98 ± 0.07 91.74 ± 0.09
LITERAL (_L) 2376 ± 421 2061 ± 430 2219 ± 371 2378 ± 358 2341 ± 277 2108 ± 308
87.5 ± 0.12 97.32 ± 0.07 88.39 ± 0.14 90.18 ± 0.10 92.63 ± 0.08 93.65 ± 0.06
CONTROL (Control) 933 ± 163
933 ± 163
In each cell, the top number is mean reaction time (ms) and the bottom number is percentage of correct responses (%) for each trial type. The reaction time was
measured from the onset of the presentation of each stimulus. Values are the mean ± standard deviation (S.D.) of all subjects.
1422 K. Wakusawa et al. / NeuroImage 37 (2007) 1417–1426

Fig. 3. Activated region determined by block design analysis and the activation profile. (a) Significant activation on the glass brain, and (b) mean normalized T1-
weighted MRIs of 31 subjects. In the activation profile (c), the parameter estimate for each stimulus relative to the Control at the peak activation is shown. No
significant effect of stimulus type was observed in differential _S–_L activation. The error bar shows the standard deviation.

condition, and greater under the Metaphor_S condition than under
the MetaphorCon_S condition at the lenient threshold (p b 0.05
without correction for multiple comparisons). No statistically
significant difference in activation was observed between the
Irony_L and IronyCon_L conditions, and between the Metaphor_L
and MetaphorCon_L conditions. The activation for the contrast
Irony_S–IronyCon_S was greater than that for the contrast
Metaphor_S–MetaphorCon_S. In the right temporal pole, activa-
tion was greater under the Irony_S condition than under the
IronyCon_S condition, and greater under the Irony_L condition
than under the IronyCon_L condition, and these differences were
statistically significant. No statistically significant difference in
activation was seen between the Metaphor_S and MetaphorCon_S
conditions, or between the Metaphor_L and MetaphorCon_L
conditions. No statistically significant difference was seen between
the activation for the contrast Irony_S–IronyCon_S and that for the
contrast Irony_L–IronyCon_L.
Table 3
Activated regions, determined by event-related analysis: irony
Anatomical regions Talairach coordinates t-value Cluster size
(x, y, z) (mm3)
Medial orbitofrontal 2, 46, −14 5.61 840
cortex
Right temporal pole 52, 12, −32 4.78 600
Coordinates and t-values for the peak voxels of significantly activated
regions are given for the contrast (Irony_S–IronyCon_S). Other details are
the same as in Table 2.
Discussion
Task-dependent activation was observed in the left medial
prefrontal cortex during the situational judgment task, as compared
to the literal judgment task, suggesting that this region is involved in
intentional processing of implicit social meaning. The right
temporal pole showed stimulus-specific activation during the
processing of ironic stimuli, as compared to processing the same
pictures with literal expressions in both tasks, suggesting that this
region may be linked to irony-specific processing, regardless of the
task. The medial orbitofrontal cortex was activated during the
processing of ironic stimuli, as compared to processing of the same
pictures with literal expressions, only in the situational judgment
task. The ROI analysis showed activation in this region during
metaphor processing; however, it was less active than during irony
processing (the difference was statistically significant). Thus, the
medial orbitofrontal cortex appears to be preferentially related to
task-dependent processing of irony. Consistent with our prediction,
all the identified areas overlapped with the cortical regions
implicated in ToM (Frith and Frith, 2003).
Left medial prefrontal cortex
The results of block design analyses show that the left medial
prefrontal cortex is linked to the task-dependent process of asses-
sing socially implicit meanings. This region has been implicated in
various tasks of social cognition (Frith and Frith, 2003; Ochsner et
al., 2004; Amodio and Frith, 2006). These tasks may be uniformly
conceptualized as an assessment of the relationship between an
 K. Wakusawa et al. / NeuroImage 37 (2007) 1417–1426 1423

Fig. 4. Activated areas determined by event-related analysis and activation profiles. Mean normalized T1-weighted MRIs of 31 subjects: (a) medial orbitofrontal
cortex, (b) right temporal pole, and (c) significant activations on the glass brain. Regarding the activation profiles, activations in response to stimuli were
compared with each other by the paired t-test without correction for multiple comparison (*p b 0.05, n.s. = not significant) at the peak activation determined by
event-related analysis. Other details are the same as those shown in Fig. 3.

individual's information and the specific situation involved
(Fletcher et al., 1995; Greene et al., 2004; Berthoz et al., 2002;
Mitchell et al., 2004; Ochsner et al., 2004; Sugiura et al., 2004). For
example, the formation of an individual's impression in a given
situation (Mitchell et al., 2004) and his/her dispositional inference
(Sugiura et al., 2004) can be seen as a judgment arising from a
person's social position, that is, the assessment of the relationship
between an individual and the social norm. Comprehension of the
mental states of characters (Fletcher et al., 1995; Castelli et al.,
2000) and judgment of emotional facial expressions (Lane et al.,
1997; Phan et al., 2003) require assessment of the relationship
between a person's mental state and the social situation. Emotional
moral judgment (Greene et al., 2004) and processing of social
transgression (Berthoz et al., 2002) constitute processing of social
human relationships. This unified functional concept appears to
agree with our SITUATIONAL task; utterances mediating socially
implicit meanings may be processed in close association with the
person concerned, and be judged by how they relate to the social
situation.
However, the left medial prefrontal cortex has often been
implicated in default mode activation, which is the baseline activity
at rest, and this activity is decreased by various goal-directed
behaviors (Raichle et al., 2001) or attention load (McKiernan et al.,
2003). In our study, the activation in the contrasting SITUA-
TIONAL–LITERAL task was not likely to be a default mode
activation because we used the mask SITUATIONAL_M–CON-
TROL; the reaction times in the SITUATIONAL tasks were shorter
than those in the LITERAL tasks, but were longer than in the
CONTROL task. Thus, the differential activation cannot be
explained by the difference in task difficulty or attention load.
Right temporal pole
The right temporal pole showed stimulus-specific activation in
both SITUATIONAL and LITERAL tasks. These results show that
irony is processed regardless of the task type; that is, irony is
recognized automatically in the right temporal pole. Irony is
distinguishable from metaphor, in that social context (such as the
relationship between a speaker's intention and others) has an
important role in irony comprehension (Sperber and Wilson, 1995).
A role for the right temporal pole in accessing emotional context has
been suggested by activation of this region in studies that examined
subjects while watching sad movies (Lévesque et al., 2003) and that
retrieved an emotional episodic memory (Dolan et al., 2000). The
results of Mobbs et al. (2006) showed that the temporal pole was
related to emotional context framing, consistent with the role of this
region suggested in our study. Activation of this region during
recognition of autobiographical materials (Damasio et al., 1996;
1424 K. Wakusawa et al. / NeuroImage 37 (2007) 1417–1426
Nakamura et al., 2000, 2001; Sugiura et al., 2001) may be related to
access to social context. In addition, the automatic nature of such a
process has also been suggested in previous imaging studies (Dolan
et al., 2000; Lévesque et al., 2003; Sugiura et al., 2006) in which the
right temporal pole was activated independently of the task
requirement.
Medial orbitofrontal cortex
Activation in the medial orbitofrontal cortex was task-dependent
and stimulus-specific, thus constituting irony-selective activation.
These results indicate that this region is associated with the cons-
cious assessment of irony, leading to situational judgment. Irony is
judged to be appropriate in a given situation on the basis of its social
context.
Involvement of the medial orbitofrontal cortex in judgment,
based on the emotional context of a social situation, has been sug-
gested by several functional imaging studies (Farrow et al., 2001;
Berthoz et al., 2002; Moll et al., 2002). While activation of this
region was statistically significant for the metaphor in the ROI
analysis, it was greater for irony than for the metaphor (this was also
statistically significant). A greater involvement of the medial
orbitofrontal cortex in irony than in metaphor processing may be
explained by the fact that comprehension of emotional context is
essential in irony processing, but is arbitrary in metaphor processing
(Sperber and Wilson, 1995).
This activation is not likely to be a default mode activation, in
that we used the mask Irony_S–Control; the reaction time under the
Irony_S condition was shorter than that under the IronyCon_S
condition, but it was longer than in the Control. Thus, differential
activation cannot be explained by the difference in the task dif-
ficulty or attention load.
Comparison to previous studies on the processing of implicit
meaning
This study showed that the left medial prefrontal cortex was
associated with judgment of relational appropriateness between an
individual's information and social situation, and was thus
relevant to the appropriateness judgment of both irony and meta-
phor. Irony was automatically processed by assessing the emo-
tional context of a social situation in the right temporal pole, and
was judged on the basis of this context in the medial orbitofrontal
cortex. Judgment of metaphor was also dependent on the medial
orbitofrontal cortex, but to a lesser extent than irony, presumably
because reference to emotional context is irrelevant for judgment
of metaphors.
Previous studies have shown that these three regions, the left
medial prefrontal cortex, right temporal pole, and medial orbito-
frontal cortex, are related to ToM (Frith and Frith, 2003). However,
few studies have shown that these three regions are involved in the
processing of irony or metaphor (see, e.g., Brownell et al., 1984,
1990; Bottini et al., 1994; Kempler et al., 1999; Rapp et al., 2004;
Eviatar and Just, 2006; Lee and Dapretto, 2006; Mashal et al.,
2007). In these studies, the stimuli involved relatively limited social
situations and these limited situations were presented explicitly. In
contrast, the picture stimuli used in our study were rich in social
context and were presented implicitly, as they would occur in daily
life in which such expressions would be used. The lack of activation
in regions involved in ToM in previous studies (Eviatar and Just,
2006; Lee and Dapretto, 2006; Mashal et al., 2007) further suggests
a role for these regions in the processing of situational context, as
found in the present study.
We also showed that each of these areas had a different activ-
ation pattern across stimulus and task conditions. Functional differ-
entiation between ToM-related regions is a topic of recent interest
and has been discussed in several publications (Saxe and Wexler,
2005; Amodio and Frith, 2006; Frith and Frith, 2006), and the
present results may contribute to the understanding of such matters.
Regions previously found to be related to linguistic processing,
such as the left inferior frontal gyrus, implicated in accessing the
mental lexicon (Giora et al., 2000; Lee and Dapretto, 2006), and the
right superior and middle temporal gyri, implicated in the
construction of narrative coherence (Eviatar and Just, 2006), were
not found to be active in this study. The lack of activation in these
areas for the linguistic processing was replicated even at a liberal
threshold (p b 0.05, without correction for multiple comparisons).
The reason for this inconsistency may be that the implicit meanings
in our study were judged primarily on the basis of situational
information, derived from the pictures. Thus, the need for linguistic
processing was much less than in previous studies. Accordingly, our
results suggest that if rich situational contexts are available,
processing of implicit meanings depends more on brain mechanisms
involved in ToM, especially the mechanisms underlying interaction
of literal meanings and relevant information in situational contexts,
than on the linguistic processing of these expressions. Wang et al.
(2006b) showed that children engaged the medial prefrontal cortex
and left inferior frontal gyrus more strongly than adult subjects,
while adults recruited anterior temporal regions more strongly than
children during irony processing. This observed shift in the regions
involved from the network for linguistic processing (inferior frontal
gyrus) to the anterior temporal regions may be explained by the
increased amount of available situational context for the adults.
A possible counterargument to our results is that the irony-
related activation in the right temporal pole and the medial
orbitofrontal cortex may be explained by the negative connotation
of irony, rather than an integrative process with the situational
context. However, we do not think this is likely. The temporal pole
is not activated in processing of simple negative connotations, but is
activated in processing negative emotions perceived in a certain
social context, in the present and previous studies (Dolan et al.,
2000; Mobbs et al., 2006). Furthermore, the medial orbitofrontal
cortex is involved in reflecting negative emotions to judgment in
this and previous studies (Farrow et al., 2001; Moll et al., 2002),
rather than mere perception of negative emotions.
Conclusions
In social situations, comprehension of irony involves the right
temporal pole and the medial orbitofrontal cortex, presumably
because it requires automatic access to the social context and
judgment, based on this context, carried out in these regions,
respectively. The left medial prefrontal cortex is involved in the
judgment of appropriateness of both irony and metaphor, probably
by means of the processing of the relationship between a person's
information and the situation. These regions have been suggested to
be involved in ToM, and our results reveal that each region has a
different function in processing implicit meaning and irony in
realistic situations. Our results suggest that processing of implicit
meanings in context-rich situations depends more on brain
mechanisms involved in ToM, especially the mechanisms related
to the interaction of literal meanings and relevant information in
 K. Wakusawa et al. / NeuroImage 37 (2007) 1417–1426
situational contexts, than on the linguistic processing of the
expressions.
Acknowledgments
We thank Atsushi Sekiguchi (IDAC, Sendai, Japan) and Ai
Fukushima (IDAC, Sendai, Japan) for support in stimulus
preparation. We also thank Wataru Suzuki (Ontario Institute for
Studies in Education of the University of Toronto) for comments
on an earlier version of this paper. This study was supported by
RISTEX/JST, CREST/JST, and the 21st Century Center of
Excellence (COE) Program (Ministry of Education, Culture,
Sports, Science and Technology) entitled “A Strategic Research
and Education Center for an Integrated Approach to Language,
Brain and Cognition” (Tohoku University). Motoaki Sugiura is
supported by a Grant-in-Aid for Young Scientists (A) (KAKENHI
18680026) (MEXT).
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