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Article 4. Gender differences in brain activity generated by unpleasant word stimuli concerning body image: an fMRI study, The British Journal of Psychiatry

(C) 2005 The Royal College of Psychiatrists

Volume 186, January 2005, pp 48-53

Abstract

Background: We have previously reported that the temporomesial area, including
the amygdala, is activated in women when processing unpleasant words concerning
body image.

Aims: To detect gender differences in brain activation during processing of
these words.

: Functional magnetic resonance imaging was used to investigate 13 men and 13
women during an emotional decision task consisting of unpleasant words
concerning body image and neutral words.

: The left medial prefrontal cortex and hippocampus were activated only among
men, and the left amygdala was activated only among women during the task:
activation in the apical prefrontal region was significantly greater in men than
in women.

Conclusions: Our data suggest that the prefrontal region is responsible for the
gender differences in the processing of words concerning body image, and may
also be responsible for gender differences in susceptibility to eating
disorders.

Declaration of interest: None. Funding detailed in Acknowledgement.
----------------------------------------------

Eating disorders, which have been associated with concerns about body shape and
size (American Psychiatric Association, 1994), are about 10 times more common in
women than in men (Weissman & Olfson, 1995). A possible reason for this
difference in susceptibility might be a gender difference in the neural
processing of unpleasant information about body image. We previously reported
that women showed amygdalar activation while processing unpleasant words
concerning body image and perceived these words to be emotionally negative
(Shirao et al, 2003a). The medial prefrontal cortex has connections to the
amygdala, constituting an interaction zone between emotional and cognitive
processing (Drevets & Raichle, 1998). In this study we compared the brain
activation between men and women while processing these words. We predicted that
the amygdala would be less activated and the medial prefrontal cortex more
activated in men than in women during the emotional decision task.

METHOD

Study sample

An age-matched sample of 13 men (mean age 25.3 years, s.d.=2.8, range 21-30) and
13 women (mean age 25.2 years, s.d.=3.2, range 21-30) participated in this study
(P=0.949 by two-tailed, two-sample Student's t test). Participants were
recruited by community announcement and paid incentives equivalent to their
transportation expenses. All of them were right-handed and were native Japanese
speakers. Handedness was determined using the Edinburgh Handedness Inventory
(Oldfield, 1971). According to self-report, participants had no history of
psychiatric, neurological or other major medical illness, and had never been
treated with a psychotropic medication. There was no significant difference in
the average years of education between men and women: men 15.2 (s.d.=1.6) v.
women 14.9 (s.d.=2.5); P=0.645 by two-tailed, two-sample Student's t-test. The
average body mass index of the men was 22.4 kg/m2 (s.d.=3.2, range 18.0-31.3)
and that of the women was 21.5 kg/m2 (s.d.=3.7, range 18.8-28.4); P=0.543 by
two-tailed two-sample Student's t-test. The average of the total Eating Disorder
Inventory - 2 (EDI-2; Garner, 1991) scores of men was 45.5 (s.d.=28.4, range
9-103) and that of women was 37.9 (s.d.=23.5, range 7-85); P=0.330 by two-tailed
Wilcoxon single-rank test. The average score for the item 'body dissatisfaction'
for the men was 7.43 (s.d.=5.45, range 2-19) and for the women was 11.31
(s.d.=7.00, range 0-22); P=0.330 by two-tailed Wilcoxon single-rank test. The
study was conducted using a protocol approved by the ethics committee of
Hiroshima University School of Medicine. All individuals provided written
informed consent for participation in the study.

Emotional decision task

We used the emotional decision task developed by Tabert et al (2001), with some
modifications. The words used in the task were selected from the database of
Toglia & Battig (1978), which includes 2854 words that have been rated on
several items such as familiarity and pleasantness, on a scale of 1 (very
unfamiliar; very unpleasant) to 7 (very familiar; very pleasant), with 4 as the
mid-point. For our study, 30 neutral words were selected from the database and
translated into Japanese. We also selected 30 highly unpleasant words concerning
body image, chosen from Japanese-language dictionaries and thesauri. The two
groups of words did not significantly differ with regard to word length (mean
length in Japanese letters: body image words 3.2, neutral words 3.1; P=0.575 by
two-tailed, two-sample Student's t-test). Our previous validation study
comparing women who had eating disorders with a control group of healthy women
showed that there was no significant difference in familiarity between the two
categories of words (eating disorder group mean familiarity score: body image
words 4.2; neutral words 4.1, P=0.727; control group mean familiarity score:
body image words 3.9, neutral words 4.1, P=0.218, by two-tailed Wilcoxon
single-rank test) and there was no significant difference in the familiarity
ratings of words concerning body image between women with eating disorders and
the control group (P=0.365 by two-tailed Wilcoxon single-rank test), whereas
there were significant differences in pleasantness between the two categories of
words (mean pleasantness score in the eating disorder group: body image words
2.4, neutral words 3.9, P=0.0002; mean pleasantness score in the control group:
body image words 3.0, neutral words 4.0, P=0.0001, by two-tailed Wilcoxon
single-rank test) and there were significant differences in the ratings of
pleasantness between the eating disorders group and the control group (P=0.030
by two-tailed Wilcoxon single-rank test) (Shirao et al, 2003b). Both lists of
words contained nouns, verbs, adjectives and adverbs.

The selected words were used to generate sets of unpleasant words concerning
body image and sets of neutral words. Each word set comprised a unique
combination of three words. The word sets were presented in six alternating
blocks of two conditions (the task condition and the control condition) in three
cycles (Fig. 1). During the task condition unpleasant word sets were presented,
and during the control condition neutral word sets were presented. Each block
began with a 3 s cue identifying the condition by displaying the word 'task' or
'control'. Five word sets were presented in each block. Each word set was shown
for 4 s with a 1.4 s interstimulus interval (Fig. 1). The blood oxygen
level-dependent (BOLD) response was recorded during three blocks of unpleasant
words and three blocks of neutral words. During each interstimulus interval, a
fixation cross placed centrally on the screen replaced the word set. Baseline
functional magnetic resonance images were obtained during a 9 s period prior to
the first block of trials, during which the individual viewed a centrally placed
fixation cross. During each trial, the word set was projected to the centre of
the person's field of view by a Super Video Graphics adapter computer-controlled
projection system. The timing of presentation of word sets was controlled by
Presentation Software Version 0.51 (Neurobehavioral Systems, Inc., San
Francisco, CA, USA) and the word sets were presented in a randomised order.
Immediately before functional magnetic resonance imaging (fMRI) scanning was
begun, each participant was given ten practice trials (five unpleasant word sets
and five neutral word sets). The words presented in the practice trials did not
overlap with the experimental words.

----------------------------------------------
Fig. 1 Design of the study task. (a) Six alternating blocks of task
condition (T) trials and control condition (C) trials were presented successively;
the total scan time was 189 s (3 min and 9 s), yielding 63 images of 28 axial
slices (1764 images). (b) Blocks of task condition and control condition trials
were preceded by a baseline imaging period. Each block began with a cue ('task'
or 'control'). The participant selected the word judged to be the most
unpleasant or most neutral in each word set, by pressing one of three buttons.
(C) Translations of typical word sets presented in this study (left-hand block,
task condition; right-hand block, control condition).
----------------------------------------------

Participants were instructed to select the most unpleasant word from each set of
unpleasant words based on their personal knowledge and experience, and for each
set of neutral words, participants were instructed to select the word that they
thought was the most neutral; they indicated their choice by pressing one of
three buttons on a response pad in the MRI scanner.

Image acquisition and processing

The MRI scanner used was a Magnex Eclipse 1.5T Power Drive 250 (Shimadzu Medical
Systems, Kyoto, Japan). A time-course series of 63 volumes was acquired with
T2*-weighted, gradient echo, echo planar imaging (EPI) sequences. Each volume
consisted of 28 slices, each 4.0 mm thick with no gap, encompassing the entire
brain. The interval between two successive acquisitions of the same image (time
to repetition, TR) was 3000 ms, the time to echo (TE) was 55 ms and the flip
angle was 90[degrees]. The field of view was 256 mm and the matrix size 64x64,
giving voxel dimensions of 4.0 mmx4.0 mm x4.0 mm. After fMRI scanning,
structural scans were acquired using a T1-weighted gradient echo pulse sequence
(TR 12 ms, TE 4.5 ms, flip angle 20[degrees], field of view 256 mm, voxel
dimensions 1.0 mm x 1.0 mm x 1.0 mm), to facilitate localisation and co-registration
of the functional data.

Image processing and statistical analysis were performed using Statistical
Parametric Mapping (SPM) 99 software (Wellcome Department of Cognitive
Neurology, London, UK) implemented in Matlab (Mathworks, Inc., Natick, MA, USA).
The first two volumes of the fMRI run (pre-task period) were discarded because
the magnetisation was unsteady, and the remaining 61 volumes were used for the
statistical analysis. Images were corrected for motion and realigned with the
first scan of the session, which served as the reference. The T1 anatomical
images were co-registered to the first functional images in each individual and
aligned to a standard stereotaxic space, using the Montreal Neurological
Institute (MNI) T1 template in SPM99. The calculated non-linear transformation
was applied to all functional images for spatial normalisation. Finally, the
fMRI images were smoothed with a 12 mm full-width, half-maximum Gaussian filter.

Using group analysis according to a random effect model that allowed inference
to the general population (Friston et al, 1999), we first identified brain
regions that showed a significantly greater response to unpleasant word sets in
comparison with the response to neutral word sets among male and among female
participants, as brain areas related to the cognition of unpleasant word stimuli
concerning body image in men and women, respectively. We then took the data of
13 of the 15 women who had participated in our previous study (Shirao et al,
2003a) and directly compared the activation of the entire brain in the male and
female sub-samples using the two-sample Student's t-test. The resulting set of
voxel values for each contrast constituted an SPM{t} map. The SPM{t} maps were
then interpreted by referring to the probabilistic behaviour of Gaussian random
fields. The data were given an initial threshold at an uncorrected Pa priori
hypothesis were reported at this threshold (Elliott et al, 2000). For regions
about which there was no clear hypothesis, a more stringent threshold of P x, y
and z coordinates provided by SPM, which were in MNI brain space, were converted
to the x, y and z coordinates in Talairach & Tournoux's (TT) brain space
(Talairach & Tournoux, 1988) using the following formulae:

(a) xTT=xMNIx0.88-0.8;

(b) yTT=yMNIx0.97-3.32;

(c) zTT=yMNIx0.05+zMNIx0.88-0.44.

Labels for brain activation foci were obtained in Talairach coordinates using
the Talairach Daemon software (Research Imaging Center, University of Texas, TX,
USA), which provides accuracy similar to that of neuroanatomical experts
(Lancaster et al, 2000). The labelling of areas given by this software was then
confirmed by comparison with activation maps overlaid on MNI-normalised
structural images.

Evaluation of pleasantness and familiarity of the word stimuli

Each participant was asked to rate the pleasantness and familiarity of all the
words presented in the tasks on a scale from 1 (very unfamiliar; very unpleasant)
to 7 (very familiar; very pleasant), immediately after scanning. For this rating
procedure the list of words was presented in randomised order in a table format.

RESULTS

Rating of words

The ratings of familiarity with the two categories of words did not significantly
differ among men (mean familiarity score: unpleasant words 3.8, neutral words
4.4, P=0.054 by two-tailed Wilcoxon single-rank test) or women (mean familiarity
score: unpleasant words 4.3, neutral words 4.3, P=0.456). However, all
participants rated the unpleasant words concerning body image as significantly
more unpleasant than the neutral words (mean pleasantness score: unpleasant
words 3.1, neutral words 4.1, P=0.007 in men; unpleasant words 2.7, neutral
words 4.1, P=0.002 in women). Neither the ratings of pleasantness nor the
ratings of familiarity in each word category significantly differed between the
male and female groups.

Brain activation

In men there was significantly greater activation of the left hippocampus, left
superior temporal gyrus, left fusiform gyrus and left medial frontal gyrus when
the emotional decision task involved unpleasant words compared with neutral
words, whereas the women showed significantly greater activity of the left
parahippocampal gyrus including amygdala, left thalamus and right caudate body
in the same comparison (Table 1, Fig. 2).

----------------------------------------------
Table 1 Relative increases in brain activity associated with unpleasant
words concerning body image (task) and neutral words (control)
----------------------------------------------

----------------------------------------------
Fig. 2 Brain areas showing significantly greater activation during the
task condition compared with the control condition. Three-dimensional 'look-through'
projections of statistical parametric maps of the brain regions are shown
(one-sample Student's t-test; corrected P n=13; d.f.=12).
----------------------------------------------

The two-sample Student's t-test revealed that there was a significantly higher
BOLD response in the left apical prefrontal region in men than in women during
the unpleasant word task compared with neutral word task (Table 1, Fig. 3). No
brain area showed significantly higher activation in women than in men during
any of the tasks.

----------------------------------------------
Fig. 3 Brain regions showing significantly greater activation in men than
in women during the task condition of the emotional decision task compared with
the control condition. Clusters of activation are overlaid onto a T1-weighted
anatomical magnetic resonance image. The white spots show areas of high
activation. Two-sample Student's t-test; uncorrected P n=26 (13 men, 13 women);
d.f.=24.
----------------------------------------------

Correlation between psychological data and brain activation

Among the 13 women participants, activation in the left apical prefrontal area,
which was significantly lower than that in men during the unpleasant words task,
was negatively correlated with the total EDI-2 score (Spearman's rank-order
correlation analysis: correlational coefficient -0.699, P=0.008). There was no
correlation between any brain area showing significant BOLD response and the
EDI-2 scores or the pleasantness rating of the unpleasant words.

DISCUSSION

We used the emotional decision task to examine the brain areas engaged in the
perception of unpleasant words concerning body image and to compare the patterns
of brain activation in men and women. Our results showed that the left medial
part of the frontal gyrus, the left limbic area excluding the amygdala, the left
superior temporal gyrus and the left fusiform gyrus play an important part in
processing unpleasant words concerning body image in men.

Lack of amygdalar activation in men

Consistent with our hypothesis, the amygdala did not show significant activation
among men; however, the gender difference of the BOLD response in the amygdala
was not significant by two-sample Student's t-test.

The amygdala has been suggested by many studies to be strongly associated with
stimuli signalling threat. Human lesion and imaging studies consistently
indicate that the amygdala is concerned in fear conditioning (Morris et al,
1998), in the recognition of fearful facial expressions (Adolphs, 1999) and in
the evocation of fearful emotional responses from direct stimulation (Halgren et
al, 1978). The amygdala is also considered to be important in the detection of
environmental threat (Scott et al, 1997), including verbal stimuli (Isenberg et
al, 1999). Therefore, the lack of significant activation in the amygdala among
men suggests that men may not process unpleasant words concerning body image as
fearful information, whereas women seem to do so.

Medial prefrontal cortex and emotional processing

The significant activation in the medial part of the frontal gyrus - Brodmann
areas (BAs) 9 and 10; medial prefrontal cortex - was only detected in men, and
there was a significantly higher BOLD response in men than in women in the left
apical prefrontal region (BA 9) when performing the unpleasant word task
compared with the neutral word task by two-sample Student's t-test. These
results were consistent with our hypothesis. Many previous studies have
suggested that the medial prefrontal cortex might have a role generally in
emotional processing. It is reported that visual stimuli that evoke emotions,
such as films or pictures, activated the medial prefrontal cortex, and that
recall of various emotions such as happiness, sadness and disgust, and a mixture
of these emotions, all separately engaged this brain region (Lane et al, 1997;
Reiman et al, 1997). Several more recent studies suggest that when people turn
their attention inwards to assess self-relevant attributes or emotional
awareness, activity increases in the medial prefrontal cortex (Johnson et al,
2002; Zysset et al, 2002). The medial prefrontal cortex has connections to
limbic structures, including the amygdala, constituting an interaction zone
between emotional processing and cognitive processing (Drevets & Raichle, 1998),
and this region may have a role in modulating the emotional response in the
amygdala and other limbic structures. Limbic structures, including the amygdala,
are likely to respond to emotional stimuli at a sensory or perceptual level
(Reiman et al, 1997), whereas the medial prefrontal cortex may be involved in
the cognitive aspects of emotional processing, such as attention to emotion,
appraisal or identification of emotion (Drevets & Raichle, 1998). From this
viewpoint, the gender differences detected in our study may demonstrate
differences of cognitive pattern in men and women. Our results suggest the
possibility that men processed the emotional decision task including words
concerning body image more cognitively rather than emotionally, and activation
in the medial prefrontal cortex was prominent; on the other hand, women
processed this task more emotionally rather than cognitively, and the medial
prefrontal cortex did not exhibit any significant activation. Both men and women
perceived the unpleasantness of the words concerning body image to the same
degree, according to their subjective ratings, but the fMRI data suggest that
their processes are different: women are likely to use more intuitive processing
whereas men use more rational processing. This discrepancy between the genders
in cognitive style related to body image may contribute to the large gender
difference in susceptibility to eating disorders.

Another possible explanation of the different patterns of activation in the
medial prefrontal cortex between men and women may be the difference in men's
familiarity with the unpleasant word set compared with the neutral words.
Although the ratings of familiarity were not different between men and women
(P=0.133 by Mann-Whitney U test), there was a trend for male participants to be
less familiar with the unpleasant words concerning body image than with the
neutral words (P=0.054 by two-tailed Wilcoxon single-rank test). When processing
unfamiliar words concerning body image, men might turn more attention inwards,
and subsequently the BOLD response in the medial prefrontal cortex was higher
than while processing neutral words.

Among women, correlational analysis revealed that the BOLD response in the left
apical prefrontal region (BA 9), which was significantly lower in women than in
men, was negatively correlated with total EDI-2 scores; in other words women
with higher EDI-2 scores exhibited lower activity in this brain area. These
results suggest the possibility that the apical prefrontal region might be
involved in the pathophysiology of eating disorders.

Comparison with other neuroimaging studies

To our knowledge, two fMRI studies concerning body image distortion have
investigated the effects of pictorial body image stimuli in women with anorexia
nervosa and healthy controls (Seeger et al, 2002; Wagner et al, 2003). One study
reported that patients with anorexia nervosa showed activation in the right
amygdala, right fusiform gyrus and brain-stem associated with stimulation with
their own body image whereas healthy controls showed activation only in the
fusiform gyrus (Seeger et al, 2002), and the other reported that patients with
anorexia nervosa showed greater activation in the prefrontal cortex and the
inferior parietal lobule than did controls (Wagner et al, 2003). The latter
authors explain the discrepancy between these results as a consequence of the
design of the task. Many differences in the experimental conditions between
these studies and ours make it difficult to compare the brain activation data,
but a possible explanation of the discrepancy between the study by Wagner et al
(2003) and our study is the age of the participants: those in the former study
were adolescents (approximately 15 years old), whereas we recruited young adults
(approximately 25 years old). An fMRI study which investigated the brain
activation of adult and adolescent men and women while processing emotional
facial expressions reported that the adult men and adolescents (both boys and
girls) showed significant activation in the bilateral orbitofrontal cortex and
anterior cingulate cortex in response to an angry face, whereas the adult women
showed significant activation in the left amygdala in addition to these brain
areas (McClure et al, 2004). These results suggest that the patterns of neural
responses to emotional stimuli may be different in adults and adolescents.

A positron emission tomography study of gender differences in brain activation
patterns during recognition of emotional facial expressions revealed that
greater amygdalar activation was observed in women and greater medial frontal
activation was observed in men (Hall et al, 2004); these authors suggest that
men might take a more analytic approach and might regulate their emotional
reaction to the stimuli more than women. Although the categories of stimuli are
different, these results support our findings.

Study limitations

Our study has some limitations. First, we did not administer a structured
interview when selecting the participants; however, they had no psychiatric or
neurological illness at the time of their participation, although we cannot rule
out its occurrence in the future. Second, participants were asked to rate only
the unpleasantness and familiarity of the words used. If we had also asked about
the fearfulness induced by the stimuli, we might have found gender differences
in subjective rating and the results with brain image data would have been more
clear-cut. Last, although our data suggest that there is differential activation
of the brains of men and women when processing unpleasant words concerning body
image, we cannot conclude whether these results are specific to unpleasant
stimuli concerning body image or would apply to a wide range of unpleasant
stimuli. Among women, a lower BOLD response in the prefrontal region compared
with men while processing unpleasant words concerning body image exhibited a
negative correlation with the total EDI-2 score, but it is unclear whether this
brain region is the focal area responsible for susceptibility to eating
disorders.

In conclusion, our study revealed that the paralimbic area including the
amygdala was activated only in women and that the left medial prefrontal cortex
was activated only in men while performing the emotional decision task with
unpleasant words concerning body image. These results suggest that gender
differences in brain activation might explain the differences in the style of
cognition towards unpleasant stimuli concerning body image. Further studies
comparing people who have eating disorders with healthy controls and which
include general unpleasant word stimuli to contrast with words specific to body
image are needed to elucidate the neural substrate responsible for the onset of
eating disorders.

CLINICAL IMPLICATIONS

* Gender differences in brain activation suggest differences between men and
women in the style of cognition toward unpleasant stimuli concerning body image.

* This discrepancy in cognitive style may have relevance to the large gender
difference in susceptibility to eating disorders.

* The medial prefrontal cortex may be the brain area linked to the pathophysiology
of eating disorder.

LIMITATIONS

* We did not use a structured interview when selecting participants.

* We asked the participants to rate only pleasantness and familiarity of the
word stimuli and we could find no clear relationship between brain activation
and the subjective rating of the words concerning body image.

* It is unclear whether the patterns of activation in the prefrontal area were
specific to the stimuli concerning body image.

ACKNOWLEDGEMENT

The study was supported by the Research on Psychiatric and Neurological Diseases
and Mental Health, Ministry of Health, Labour and Welfare, Japan.
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