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					                   Neurology and Clinical Neurophysiology 2004:28 (November 30, 2004)



       MEG Analysis of “Theory Of Mind” in Emotional Vignettes Comprehension
     Ishii, R1,2, Gojmerac, C2,6, Stuss, DT 2,6, Gallup, GG Jr3, Alexander, MP 4, Chau, W 2, Pantev, C 5
   1
    Department of Psychiatry and Behavioral Science, Osaka University Graduate School of Medicine,
   Japan. 2The Rotman Research Institute, Baycrest Centre for Geriatric Care, Canada. 3Department of
     Psychology, State University of New York at Albany, USA. 4Department of Neurology, Harvard
         University, Beth Israel Deaconess Medical Center, USA. 5Institute of Biomagnetism and
                 Biosignalanalysis, University of Munster, Germany. 6University of Toronto

 Corresponding Author: Ryouhei Ishii, M.D., Ph.D., Department of Psychiatry and Behavioral Science,
 Osaka University Graduate School of Medicine, D-3, 2-2, Yamada-oka, Suita, Osaka, 565-0871 Japan,
                   Phone: +81-6-6879-3059; Email: ishii@psy.med.osaka-u.ac.jp
ABSTRACT

   [Objective] Several studies suggested that an impaired “theory of mind” might play a key role in
psychiatric disorders, such as autism and schizophrenia. Medial frontal lobe lesions of the right frontal
lobe were reported to impair this ability. The aim of our study was to locate areas of the brain associated
with the process of “theory of mind” in normal subjects. [Methods] In order to index the activity of brain
areas related to "theory of mind" reasoning in sixteen normal adults, we administered an emotional
(“happy”, “sad”, “angry” and “neutral”) vignettes comprehension task during magnetoencephalography
(MEG) recordings and analyzed these data by using SAM (synthetic aperture magnetometry), SPM99 and
the permutation method. Subjects were presented with eight different videotaped social situations (each
emotion has two vignettes) and were asked to indicate which emotion they represented. [Results]
Statistically significant activation in the comparison of “happy”-“sad” and “angry”-“sad” was observed in
the bilateral medial prefrontal cortices in the alpha frequency band. There were no significant differences
in comparisons of each type of emotional vignette to the neutral vignettes, “happy”-“angry” comparison,
and male-female comparisons. There was no significant difference in other frequency bands. [Conclusion]
This result suggests that bilateral medial prefrontal cortex are involved in the comprehension of emotional
states of others.

KEY WORDS

   MEG, Theory of mind, Spatial filter, Autism, Schizophrenia, Emotion, SPM, Permutation, Synthetic
aperture magnetometry (SAM)

INTRODUCTION

   “Theory of mind” is the ability to explain and predict the behavior of others in terms of their mental
states [Perner, 1988]. Several studies have suggested that an impaired theory of mind may lie at the heart
of psychological disorders that are characterized by deficits in social understanding. It has been reported
that patients with autism have deficits in performance on theory of mind tasks, i.e., requiring the
interpretation of mental states of others [Happe, 1995]. Schizophrenia is also a biologically based disorder
that appears to be characterized by a specific impairment in this theory of mind process [Corcoran, 1995].

   Medial frontal lobe lesions, with a particular preeminence for the right front lobe, impaired
performance on theory of mind tasks [Stuss, 2001]. A recent PET study showed that a language-based
“theory of mind” task activated an extensive neural network that included the medial frontal cortex, the
superior frontal cortex, the anterior and retrosplenial cingulate, and the anterior temporal pole [Calarge,
2003]. Although several other brain regions have been implicated in theory of mind, the frontal lobes
have been considered to play a special role in human behaviour, with damage in this region affecting




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                   Neurology and Clinical Neurophysiology 2004:28 (November 30, 2004)


high-level cognitive functions but also social behavior, personality, personal memories and self-
awareness.

   Our study used MEG to locate areas of brain associated with the process of theory of mind in normal
subjects. To index the activity of neural systems that are engaged during theory of mind reasoning in
normal adults, we measured MEG recordings during the emotional vignettes comprehension task (Stuss,
Gallup, & Alexander, in preparation) and analyzed the data by using SAM, SPM99 and permutation.

METHODS

   Sixteen normal subjects (eight males and eight females, all right-handed, age 25 to 37) participated in
this study. After explaining the nature of the study, informed consent was obtained. Experimental
procedures were in accordance with the Ethics Commission of the Baycrest Centre for Geriatric Care and
the Declaration of Helsinki. The subjects had no history of neurological and psychiatric disorders. During
recording the subjects sat relaxed under the MEG helmet-shaped device and kept their eyes open and their
arms relaxed.

   To index the activity of neural systems that are engaged during theory of mind reasoning in normal
adults, we employed the emotional videotaped vignettes comprehension task (Stuss, Gallup, & Alexander,
in preparation). These emotional vignettes depicted four types of emotions (happy, sad, angry and
neutral), two vignettes for each emotional type, played once for each. The time length of those vignettes
varied from 25sec to 50sec. These vignettes showed the scenes of the emotional reactions which were
acted out by people unfamiliar to all the subjects. Subjects were instructed to rate their emotional intensity
and empathic level for these vignettes after the experiments. After viewing each scene, subjects were
asked to indicate which emotion was represented in the vignette by pointing to one of four face pictures,
each representing one of the four emotions.

    MEG data were obtained using a whole head helmet-shaped 151-channel SQUID sensor array (Omega
151, CTF Systems Inc.) within a magnetically shielded room. MEG signals were digitized at 625 Hz and
filtered using a 60 Hz notch filter and 200 Hz low pass filter.

   The tomographic distributions of the current source density in alpha, beta and gamma frequency bands
were determined from the MEG data, using synthetic aperture magnetometry (SAM) [Robinson, 1992]
[Ishii, 1999]. SAM is a spatial filtering technique based on the nonlinear constrained minimum-variance
beamformer. This technique overcomes the nonuniqueness of generalized inverse solutions, such as the
minimum norm, and thereby permits unambiguous three-dimensional source mapping during task
performance.

    SAM images were generated by subtracting each emotional vignette (25 seconds during happy, sad,
angry and neutral vignettes x 2 trials) from the other: e.g., “happy”-“neutral”, “angry”- “neutral”, “sad”-
“neutral”, “happy”- “sad”, “angry”- “sad” and “happy”- “angry”. We also compared these activation
images between male and female subjects. This was done for each voxel divided by their ensemble
standard error of instrumental (SQUID sensor) and environmental noise. The distributions of the SAM
images were transformed to the SPM T1 template space. A nonparametric permutation technique was
applied to the normalized SAM results to determine the statistical significance of the results. The omnibus
null hypothesis of no activation anywhere in the brain was rejected if at least one t-value was above the
critical threshold for P<0.05 determined by 1024 permutation. Voxels with t-values above this critical
0.05 threshold were considered as a region of activation.

RESULTS

   After viewing the emotional vignettes, all subjects were able to identify correctly the emotional state
represented in the vignette. All subject rated some emotional intensity and empathy for emotional


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                   Neurology and Clinical Neurophysiology 2004:28 (November 30, 2004)


vignettes (particularly high for sad vignettes), but not for neutral vignettes. SAM-SPM99-permutation
revealed statistically significant increase in alpha frequency band in subtraction of “sad” from “happy”
and from “angry” (“happy”- “sad”, “angry”- “sad”) in the bilateral medial prefrontal cortices (Fig.1 and
2). We could not find any difference in comparisons of each emotional vignette to neutral vignettes, the
“happy”-“angry” comparison, or in the male-female comparison. There were no significant differences in
other frequency bands.

DISCUSSION

   The major finding of this study was that statistically significant activation in the comparison of
“happy”-“sad” and “angry”-“sad” was observed in the bilateral medial prefrontal cortices in the alpha
frequency band. Like the previous studies using rCBF methods to investigate “theory of mind” [Calarge,
2003], our MEG study also showed that the medial prefrontal region is activated when subjects tried to
imagine and estimate the mental states of others. Frith and colleagues had suggested that there might be a
“theory of mind system” in the human brain like the language system and the facial recognition system,
and this system might be composed of medial prefrontal, superior temporal and inferior frontal regions




       Figure 1. SAM-SPM99-Permutation images of the comparison “happy”-“sad”. (n=16,
       p<0.05)




       Figure 2. SAM-SPM99-Permutation images of the comparison “angry”-“sad”. (n=16,
       p<0.05)




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                   Neurology and Clinical Neurophysiology 2004:28 (November 30, 2004)


[Frith, 1999]. We suggest that the bilateral medial prefrontal cortices have an important role for
comprehension of emotional states of others.

   The significant bilateral medial prefrontal activation was found only in the comparison of “happy”-
“sad” and “angry”-“sad” scenes. The sad vignettes represented quite depressing scenes (e.g., people
crying at a gravesite). The sad scenes might evoke and prolong the emotional states more easily than other
emotional vignettes. We speculated that the subjects might be more in the empathic mode during the sad
vignettes as shown in the result of the emotional ratings from subjects.

   Keightley et al (2003) studied limbic-cortical activation under transient emotional stress as a function
of personality style using PET. In their study, subjects were divided into a negative affective style (NAS)
group versus a positive affective style (PAS) group, according to their scores on a personality inventory.
PET scan while performing sad and neutral mood induction tasks showed a group-specific pattern in the
NAS group with sad mood, and involved increased activity in anterior cingulate cortex but in association
with decreased medial frontal activity, a pattern not seen in the PAS group, associated with acute sadness.
We can speculate that the alpha deactivation during the sad vignettes might be related to decreased medial
frontal activity in their study. The classification by using the personality inventory would be the future
application for our study.

   We could not find any difference in the comparisons of each emotional vignette to neutral vignettes.
Post hoc questioning suggested that the subjects tried to extract emotional clues from these neutral
vignettes and found that there was no emotional significance in these vignettes only after analyzing of the
entire vignette. We speculated from these insights that the neutral vignettes were not an appropriate
comparison, because the subjects may have still engaged theory of mind processing in trying to find an
emotional significance which was not present. There was no difference between the 8 male and 8 female
subjects. Increasing the subject number and analyzing correlations of MEG in relation to personality
variables of individuals may be a future avenue of research.

   This study provides experimental evidence for an independent cerebral implementation of self-
perspective in the context of theory of mind. Our study design using the relatively non-invasive MEG
imaging procedure might be useful as an experimental tool in the study of patient populations who are
reported to have theory of mind deficits, e.g., autism and schizophrenia.

REFERENCES

Calarge C, Andreasen NC, O'Leary DS. Visualizing how one brain understands another: a PET study of
theory of mind. Am J Psychiatry. 2003;160:1954-64.

Corcoran R, Mercer G, Frith CD. Schizophrenia symptomatology and social inference: investigating
“theory of mind” in people with schizophrenia. Schizophre Res 1995;17:5-13.

Fretcher PC, Happe F, Frith U, Baker SC, Dolan RJ, Frackowiak RS, Frith CD. Other minds in the brain:
a functional imaging study of “Theory of mind” in story comprehension. Cognition 1995;57:109-28.

Frith CD, Frith U. Interacting minds—a biological basis. Science 1999;286:1692–5.

Happe FG. The role of age and verbal ability in the theory of mind task performance of subjects with
autism. Child Dev 1995;66:843-55.

Ishii R, Shinosaki K, Ukai S, Inouye T, Ishihara T, Yoshimine T, et al. Medial prefrontal cortex generates
frontal midline theta rhythm. Neuroreport 1999;17:675-9.




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Keightley ML, Seminowicz DA, Bagby RM, Costa PT, Fossati P, Mayberg HS. Personality influences
limbic-cortical interactions during sad mood induction. Neuroimage. 2003 ;20:2031-9.

Perner J, and Wimmer H. Misinformation and unexpected change: testing the development of epistemic-
state attribution. Psychol Res 1988;50:191-7.

Robinson SE, Rose DF. Current source image estimation by spatially filt1ered MEG. In: Hoke M, Eme
SN and Okada YC, eds. Biomagnetism: Clinical Aspects: Proceedings of the 8th International Conference
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Stuss DT, Gallup GG Jr, Alexander MP. The frontal lobes are necessary for ‘theory of mind’. Brain
2001;124:279-86.




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