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Department of Psychology and Brain and Behavior Center, University of Haifa, Haifa, Israel
b
Cognitive Neurology Unit, Rambam Health Care Campus, Haifa, Israel
c
Shalvata Mental Health Care Center, Hod Hasharon, Israel
Received 27 June 2006; received in revised form 13 September 2006; accepted 15 September 2006
Available online 19 December 2006
Abstract
Patients with schizophrenia show impaired emotional and social behavior, such as misinterpretation of social situations and lack
of Theory of Mind (ToM). However, the neuroanatomical basis of impaired ToM and its nature in schizophrenia is still
largely unknown. Based on previous findings, the present study suggests that impaired social cognition observed in schizophrenic
patients may be similar to that observed in patients with prefrontal (PFC) damage due to impaired affective ToM abilities, rather
than to a general impairment in ToM. We examined the behavioral and neural mechanisms that underlie the social and
communicative impairments observed in patients with schizophrenia and with PFC damage, by looking at differential patterns of
ToM impairment in these individuals. The performance of 24 patients with schizophrenia was compared to the responses of patients
with localized lesions in the ventromedial (VM) or dorsolateral PFC, patients with non-frontal lesions, and healthy control subjects.
Patients with schizophrenia and those with VM lesions were impaired on affective ToM tasks but not in cognitive ToM
conditions. It was concluded that the pattern of mentalizing impairments in schizophrenia resembled those seen in patients with
lesions of the frontal lobe, particularly with VM damage, providing support for the notion of a disturbance of the fronto-limbic
circuits in schizophrenia.
2006 Elsevier B.V. All rights reserved.
Keywords: Social cognition; Theory of mind; Prefrontal cortex
1. Introduction
Impaired social cognition has been observed in
patients with schizophrenia and found to be linked to
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2. Methods
2.1. Subjects
Ethical approval was granted by both hospitals
(Rambam medical center and Shalvata Mental Health
Care Center) Ethics Committees. All subjects signed
informed consent.
Table 1
Demographic details
Gender
Males
Females
Age, mean (SD)
Years of education, mean (SD)
Similarities, mean (SD)
Recognition of emotions, mean %
of correct responses (SD)
Perspective taking scale,
mean (SD)
Schizophrenia
N = 24
VM
N=9
DLC
N=7
MIX
N = 11
NF
N = 16
HC
N = 28
Sig
15
9
32.47 (10.66)
12.90 (3.38)
9.95 (3.00)
85.43 (8.02)
8
1
40.11 (15.55)
13.25 (3.41)
9.55 (1.13)
77.89 (11.69)
6
1
33.57 (7.28)
13.42 (1.81)
11.80 (1.30)
78.17 (8.54)
9
5
34.63 (15.74)
13.00 (2.36)
8.92 (1.49)
81.92 (2.08)
11
4
37.87 (16.28)
13.66 (2.22)
10.75 (1.815)
85.31 (8.79)
15
13
28.35 (7.44)
13.39 (1.13)
11.08 (2.29)
88.18 (11.37)
NS
NS
NS
NS
p = 0.034
1.75 (4.60)
4.00 (6.58)
2.40(3.36)
1.57 (4.43)
5.00 (5.85)
5.9 (3.48)
p = 0.0001
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and men, aged 2158 years, with 1216 years of education. Subjects with a history of alcohol or drug abuse
or previous head trauma were excluded. Two schizophrenic patients and one HC refused to complete all the
tasks.
2.2. Assessment of cognitive and affective ToM:
cognitive and affective mental inference and mentalistic
significance of eye direction
This computerized task (programmed using E-prime)
is based on a task described previously by Baron-Cohen
(1995) and involves the ability to judge mental states
based on verbal and eye gaze cues. The original stimuli
were developed and further divided into three main
conditions: affective cognitive and physical (for description and sample of items see Appendix A).
2.3. Clinical assessment
The patient group was assessed, by a clinical
psychologist, using the Positive and Negative Symptoms
of Schizophrenia (PANSS, Kay et al., 1987).
To obtain an estimate of verbal intellectual functioning, we measured performance on the Similarities
subscale (WAIS-R).
2.3.1. Assessment of perspective taking abilities
Perspective taking abilities were assessed using the
perspective taking subscale taken from the Interpersonal
Reactive Index (IRI) (Davis, 1983). This scale was
chosen based on previous study suggesting that affective
aspects of ToM are related to cognitive empathy and
may be mediated by the orbitofrontal and medial
prefrontal cortex (Shamay-Tsoory et al., 2004).
2.3.2. Recognition of basic emotional facial expression
This computerized task was designed to assess the
individual's ability to recognize basic emotions. The test
consists of 24 photographs of facial expressions taken
from Ekman and Friesen (1976). At the bottom of each
picture stimulus, two words were printed; the correct
emotion expressed and a distracter.
3. Results
As Table 1 shows, one-way ANOVA between
groups of subjects indicated that the groups did not
differ in age (F[5,88] = 2.039, NS), education (F[5,88] =
0.225, NS), or estimated overall level of verbal
functioning (F[5,57] =0.906, NS). Significant differences between groups were evident in recognition of
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278
Fig. 2. The mean scores of the affective (Aff2) and cognitive (Cog2):
the schizophrenia, the VM and MIX groups had significantly lower
accuracy scores as compared to the HC group in the affective ToM
condition but not in the cognitive ToM condition. The schizophrenia
group was also significantly impaired as compared to the NF
groups. * Significantly impaired (lower accuracy) as compared to
the HC.
279
280
Acknowledgements
This study was supported by a research grant from the
Israeli National Institute of Psychobiology. We are thankful
for the NARSAD's Young Investigator Award Program.
Appendix A. ToM task: cognitive and affective
mental inference and mentalistic significance of eye
direction: description of the task and sample of items
The task consists of 64 trials, each showing a cartoon
outline of a face (named Yoni) and four colored pictures of
objects belonging to a single category (e.g., fruits, chairs)
or faces, one in each corner of the computer screen. The
subject's task is to point to the correct answer (the image to
which Yoni is referring), based on a sentence that appears
at the top of the screen and available cues, such as Yoni's
eye gaze, Yoni's facial expression, or the face's (the one to
which Yoni is referring) eye gaze and facial expression (see
sample of items below). Subjects are instructed to point at
the correct picture using the computer mouse as fast as they
can. There are three main conditions: cognitive (24
trials), affective (24 trials) and physical (16 trials),
each requiring either a 1st (32 trials) or a 2nd (32 trials)
order inference. The cognitive and affective conditions
involve mental inferences, while the physical condition
requires a choice based on a physical attribute of the
character (thus serving as a control condition, to ensure that
the subject understands the task). In the 1st order physical
condition the subject is asked to refer to Yoni's location
(Yoni is near____), while in the 2nd order condition the
subject is asked to point to the same object Yoni and the
character have (Yoni has the same fruit as ____has). In
the cognitive conditions, both Yoni's facial expression and
the verbal cue are neutral, while in the affective conditions,
both cues provide affective conditions (For example: Yoni
is thinking of ___ [Cog1 condition] vs. Yoni loves___
[Aff1 condition]). In the 2nd order condition (Cog2, Aff2,
Phy2), the four stimuli consist of face images and the
choice of the correct response requires understanding of
the interaction between each of these figures and Yoni's
mental state. Thus, while the Cog2 requires understanding
beliefs about others' beliefs and desires (Yoni is thinking of
the toy that _______wants), the Aff2 involves understanding of one's emotions in regard to the others'
emotions (Yoni loves the toy that _______loves).
In 70% of the 2nd trials, Yoni's eye gaze is directed at
one of the four face stimuli (the correct answer) and, in
30% of the trials, Yoni's gaze is directed straight ahead.
When Yoni's gaze is directed straight ahead, the
decision must be based on the verbal cue and the face's
gaze. Subject's performance was rated for accuracy.
281
282
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