Body image distortions in bulimia nervosa: Investigating body size overestimation and body size satisfaction by fMRI

NeuroImage 56 (2011) 1822–1831

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Body image distortions in bulimia nervosa: Investigating body size overestimation and body size satisfaction by fMRI Harald Matthias Mohr a,b,c,⁎, Christian Röder d, Jan Zimmermann a,c, Dennis Hummel a,c, Alexa Negele e, Ralph Grabhorn b a

Department of Neuro-Cognitive Psychology, Institute for Psychology, Goethe University, Mertonstrasse 17, 60054 Frankfurt, Germany Department of Psychiatry, Psychosomatic und Psychotherapy, Heinrich-Hoffmann-Str. 10, Goethe University Hospital, 60528 Frankfurt, Germany Brain Imaging Center Frankfurt, Schleusenweg 2–16, 60590 Frankfurt, Germany d Department of Psychiatry, Erasmus University, Medical School, Rotterdam, The Netherlands e Sigmund-Freud-Institute, Myliusstrasse 20, 60323 Frankfurt, Germany b c

a r t i c l e

i n f o

Article history: Received 17 October 2010 Revised 21 February 2011 Accepted 23 February 2011 Available online 26 February 2011 Keywords: Bulimia nervosa Eating disorders fMRI Body image

a b s t r a c t Background: Body image distortion is a key symptom of eating disorders. In behavioral research two components of body image have been defined: attitudes towards the body and body size estimation. Only few fMRI-studies investigated the neural correlates of body image in bulimia; those are constrained by the lack of a direct distinction between these different body image components. Methods: The present study investigates the neural correlates of two aspects of the body image using fMRI: satisfaction rating and size estimation of distorted own body photographs in bulimia nervosa patients (15) and controls (16). Results: Patients were less satisfied with their current body shape than controls and preferred to be thinner. The amount of insula activity reflects the pattern of the satisfaction rating for patients and controls. Patients also overestimated their own body size. For control subjects, an activated cluster in lateral occipital cortex was sensitive for body size distortions, whereas bulimic patients did not demonstrate such a modulation. Furthermore, bulimic subjects did not recruit the middle frontal gyrus (MFG) in contrast to controls during the body size estimation task, maybe indicating a reduced spatial manipulation capacity. Therefore, this activation pattern of lateral occipital cortex and MFG might be responsible for body size overestimation in bulimia. Conclusions: The present results show that bulimic patients exhibit two distinct deficits in body image representations similar to anorectic patients and that specifically associated neuronal correlates can be identified. Concludingly, our study support psychotherapeutic strategies specifically targeting these two aspects of body image distortions. © 2011 Elsevier Inc. All rights reserved.

Introduction Body image distortion is a key symptom of eating disorders. In DSM-IV bulimia nervosa is characterized as “a self-evaluation that is unduly influenced by body shape and weight” (APA, 2000), while ICD10 criteria specify “a morbid dread of fatness and the patient sets herself or himself a sharply defined weight threshold” (World Health Organization, 1992). In behavioral research on eating disorders two different components of body image can be distinguished: (a) the estimation of one's

⁎ Corresponding author at: Department of Biological Psychology, Institute for Psychology, Goethe University, Mertonstrasse 17, 60054 Frankfurt, Germany. Fax: +49 69/798 25209. E-mail address: [email protected] (H.M. Mohr). 1053-8119/$ – see front matter © 2011 Elsevier Inc. All rights reserved. doi:10.1016/j.neuroimage.2011.02.069

own body size and (b) the attitude towards one's own body in terms of an emotional evaluation (Slade, 1994; Skrzypek et al., 2001). A set of various techniques for the assessment of body size perception has been developed, including video distortions (Probst et al., 1998), questionnaire methods (Stunkard et al., 1983) as well as computerbased image distortions (Johnstone et al., 2008). Methods usually applied to assess an emotional evaluation of the own body size are self-report questionnaires or perceptual tasks examining the perceived discrepancy between current body size and ideal body size (Stunkard et al., 1983; Williamson et al., 1989). The overestimation of one's body size by bulimic patients was confirmed in several studies (Vocks et al., 2007a, 2007b; Cash and Deagle, 1996), yet no significant differences occurred between bulimic and anorectic patients (Schneider et al., 2009). With regard to the emotional body evaluation, bulimic patients often demonstrate high body dissatisfaction, mostly higher than

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anorectic patients do (Cash and Deagle, 1996; Mizes et al., 2004; Ruuska et al., 2005). Only a few neuroimaging studies concerning body image in bulimia nervosa have been realized so far, and they revealed an inconsistent pattern of results. Miyake et al. (2010) reported for bulimic patients in contrast to healthy controls and patients with anorexia nervosa less activation of the right amygdala and the left medial prefrontal cortex during the processing of the participants' own fat images. Different results were reported by Uher et al. (2005), who found that activations to drawn body images in the posterior parietal and lateral occipitotemporal cortex were less strong in eating disorder patients (anorexia nervosa and bulimia nervosa) compared to control subjects, whereas activities in these areas were significantly higher for bulimic patients compared to patients with anorexia nervosa. The authors concluded that the lower activation of the posterior parietal cortex might be related to deficits in body perception and might facilitate the development of body image disturbances. Altogether, results indicate disparities for the activation of bodyrelated neuronal circuits between healthy subjects and bulimic patients as well as differences in the processing of the body image between bulimic and anorectic patients. The two studies mentioned above are constrained by the fact that body image was investigated as a unitary concept. No distinction was made between the commonly accepted aspects of body image, the estimation of one's own body size and the attitudes towards one's own body (Skrzypek et al., 2001; Smeets and Kosslyn, 2001). Therefore, the present study is set out to investigate the neural correlates of two components of the body image: (1) satisfaction rating of one's own body and (2) body size estimation. We used the same design as in a previous study with anorectic participants and healthy controls (Mohr et al., 2009), in which we were able to find specific behavioral responses and neural activation patterns including the insula and the posterior parietal cortex for the two examined components of body image. In the present study we hypothesized that patients suffering from bulimia nervosa would be less satisfied with their current body shape in comparison to healthy controls. Furthermore, we expected bulimic patients to show a bias in overestimating their body size when performing a body size estimation task. We considered that modulations in task and levels of body picture distortion should clarify neuronal activity patterns that are differentially modulated for bulimic and control subjects. Specifically, the involvement of areas related to emotional evaluation and estimation of one's own body size should lead to distinguishable activations in bulimic and control subjects. To investigate this aspect, a whole brain three-way interaction analysis with the factors task (body size estimation versus satisfaction rating), group (bulimic versus control group) and distortion level of selfimages (thinner, about actual size, fatter) was calculated. Material and methods Subjects Fifteen female bulimic patients according to DSM-IV criteria and 16 female healthy controls (as reported in Mohr et al., 2009) participated in the experiment. All participants were right-handed and had normal or corrected-to-normal visual acuity. Subjects were excluded if they reported any history of substance abuse, schizophrenia and psychotic symptoms, bipolar disorders, neurological disease or closed head injury. The control group of the present study is largely identical to the control group of the previously published study (Mohr et al., 2009). None of the bulimic subjects met criteria for a major depressive or severe anxiety disorder within the past two weeks. Nine patients fulfilled the criteria for a major depressive episode during their lifetime. Subjects participating in the control group reported no

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history of psychiatric or neurological illness and no psychotherapeutic interventions. All patients underwent a full physical examination. Four of the patients were on antidepressants medication (selective serotonin reuptake inhibitors). All healthy subjects were free from medication. For the bulimic and control group, the mean age was 24.8 (SD = 3.2) and 25.5 (S.D= 4.5) years, respectively (t(29) = .55, p = .56). Current body mass index (BMI) was not different between bulimic (mean= 22, SD = 2.1) than in control subjects [mean= 21.8, SD = 2.6; t(29)=.24, p = .8]. Written informed consent was obtained from each subject after the procedure had been explained in detail. The ethics committee of the Goethe University Medical School approved the experiment. Stimuli Digital photographs of each subject's whole body in a standardized pose (standing upright, feet approximately as wide as the shoulders, arms spread horizontally) were created on a monotonous, orangecolored background. Each participant was photographed from the front-perspective. Photographs showed the whole body of the participants except their head and feet. Participants wore standardized clothes, i.e., a black shirt and black leggings. The clothes were available in several sizes to make sure they would fit tightly to the body shape (see Fig. 1). The computer program Body Form Imaging (Sands et al., 2004) was used to manipulate each digital image of the subjects. Shoulders, chest, hips, thighs and calves were jointly distorted in steps of 1% to obtain 31 images with different degrees of body size distortion relative to the original. We used the following images for each subject respectively: 15 fatter than the actual body image (distortion at +1% to +15% of the original image) and 15 thinner than the actual body image (distortion at −1% to −15% of the original image) in addition to the original photograph. Paradigm Images were projected onto a removable screen inside the MR bore (Sony data beamer, VPL-XP20, 1400 ANSI). To investigate the two components of the body image, we used an fMRI-design previously published by Mohr et al. (2009). Subjects were asked to perform two tasks, one in which they were asked to rate the presented images compared to their real body image (body size estimation task), and another task in which they were asked to rate the presented images with regard to their ideal body image (body satisfaction task). Each subject underwent each task modulation twice for the whole set of morphed images respectively. Tasks were presented in balanced order. Body size estimation Most body size estimation tasks require subjects to choose the silhouette (from thin to big) that most closely resembles the subject's real figure (Stunkard et al., 1983; computer-based estimation with individualized images, Johnstone et al., 2008). However, assessment with fMRI makes several repetitions of each trial necessary, so we adapted this type of task in the following way: subjects were presented with images of themselves (randomized in terms of distortion from thin to big) for 4000 ms, and were then given 4000 ms to decide how closely the presented image matched their real body shape. Ratings were made by button press: −2 = image is extremely distorted, −1 = image is moderately distorted, +1 = image is nearly realistic, +2 = image is realistic and undistorted. During the inter-trial interval (ITI, baseline) of 8 or 12s, a white fixation cross on a black background was presented. Body satisfaction In most perceptual body satisfaction tasks, subjects are asked to select an image matching their ideal body size and one matching their

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Fig. 1. Examples of the stimuli and their variations (distortion at ±10% of the original image).

actual body size (Stunkard et al., 1983; computer-based estimation, Johnstone et al., 2008). The extent of discrepancy between selfperception and ideal perception was interpreted as a measure of body satisfaction (Fallon and Rozin, 1985). We adapted this task with regard to the demands during fMRI scanning on the one hand, and the comparability to the previously described body size estimation task on the other hand. The stimuli and presentation durations of the second task were identical to the first. The subjects had to evaluate how closely the shown images represented their ideal body image: −2 = image is not identical at all, −1 = image is not identical, + 1 = image is nearly identical, + 2 = image is identical to ideal body shape. The two tasks were presented in two blocks for each task; blocks were presented in pseudorandomized order. One block consisted of 30 trials lasting 7 min 20 s. Control variables To obtain a more detailed picture of body image and body awareness, subjects additionally completed the body image questionnaire FKB-20 (Clement and Lowe, 1996). This instrument assesses two dimensions of body image: (a) negative attitudes towards one's own body, such as disgust and dissatisfaction, and (b) restricted body dynamics, such as how healthy, fit and powerful a subject experiences her body. MRI procedure Images were acquired on a 3-T Siemens Magneton Allegra Scanner (Siemens, Medical Systems, Germany) using a standard four-channel head coil. During the experiment, 33 oblique axial slices (in-plane resolution = 3.5 × 3.5 mm2, slice thickness = 3 mm, interslice distance = 0.6 mm) covering the entire cortical volume were acquired using a T2*-weighted echo planar imaging (EPI) sequence [repetition time (TR) = 2000 ms, echo time (TE) = 30 ms, flip angle (FA) = 90°, matrix size = 64 × 64]. The subjects underwent four functional runs (220 volumes per run, two runs per task condition) resulting in a total number of 880 volumes per subject. The first two volumes of every run were discarded to account for T1 saturation effects. Highresolution anatomical volumes using a T1-weighted three-dimensional (3D) magnetization prepared rapid acquisition gradient echo (MP-RAGE) sequence (TR = 2300 ms, TE = 3.93 ms, resolution = 1 mm3, 144 slices) were acquired after the functional runs for co-registration with the functional data. Data analysis The functional and anatomical images were analyzed using the Brainvoyager QX software package (Brain Innovation, Maastricht,

Netherlands). Data pre-processing included a slice scan time correction using sync-interpolation, 3D motion correction using rigid body transformations, spatial smoothing with a 4 mm Gaussian kernel (full-width at half-maximum), temporal high-pass filtering to remove low-frequency non-linear drifts of three or fewer cycles per time course and linear trend removal. The functional data were subsequently co-registered with the anatomical scans and transformed into Talairach space (Talairach and Thournoux, 1988) for each subject. General linear models (GLMs) were computed from the 128 znormalized volume time courses (32 subjects x four runs). The blood oxygen level-dependent (BOLD) response was modeled using a two gamma hemodynamic response function. For fMRI analysis we pooled the images of the four scans into three categories of predictors: 10 thinner (−15% to − 6%), 11 about actual size (−5% to + 5%) and 10 fatter pictures (+6% to +15%) per scan, for both of the tasks performed. Analysis was based on a second-level random-effects GLM with factors task (baseline, body size estimation, satisfaction rating) × group (bulimia vs. control group) × distortion level of self-images (thinner, about actual size, fatter). For clarification and interpretation of the complex three-way interaction effects we extracted the beta values of significant clusters by averaging over all voxels within a cluster. Repeated-measures ANOVAs and post-hoc t-tests (two-tailed) were performed on the extracted beta values. Statistical results were visualized by projecting the data on the inflated surface reconstruction of a template brain (courtesy of Montreal Neurological Institute; MNI). Results Behavioral data Body satisfaction task Testing the direct behavioral responses with a 2 × 3 ANOVA [group (bulimia vs. control) × distortion level (thinner, about actual size, fatter)] revealed a highly significant main effect for distortion level [F(2, 58) = 87, p b 0.001], no significant main effect for group [F(1, 29) =.21, p = 0.64] but a highly significant interaction between distortion level and group [F(2, 58) = 22.5, p b 0.001]. A post-hoc t-test (two-tailed) demonstrated that patients with bulimia nervosa showed a more positive rating of their thinner sized (−6% to −15%) images in contrast to controls [t(29)= 3.95, p b 0.001]. Conversely, healthy controls rated their about actual sized images (−5% to +5% distortion) more positive than patients [t(29)= 4.3, p b 0.001]. Both groups judged their fatter images (+6% to +15%) as negative; ratings of bulimic participants were more negative than those of controls [t(29) = 3.6, p b 0.001]. Furthermore, for the bulimia nervosa group a linear trend occurred showing a decline in satisfaction rating from thinner sized images to actual and fatter images (F(1, 14) = 126, p b 0.001). In contrast, a

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quadratic trend occurred for the healthy subjects in satisfaction rating with highest ratings for actual sized self images (F (1, 15) = 230, p b .001). Results are presented in Fig. 2. Body size estimation task Tests on the basis of the original rating data with a 2 × 3 ANOVA (group × distortion levels) revealed a highly significant main effect for distortion level [F(2, 58) = 47, p b 0.001], no significant main effect for group [F(1, 29) = .79, p b .39], but a highly significant interaction between distortion level and group [F(2, 58) = 6.8, p b 0.002]. Bulimic patients estimated their presented fatter self-images to be more realistic than controls [t(29) = 2.8, p b 0.01]; however, this was not the case for the thinner than actual images [t(29) = 1.6, p = .12.] and the about actual sized images [t(29) = .38, p = .7]. Results are presented in Fig. 2. FKB-20 questionnaire Significant differences between the groups were also found for the two dimensions of the FKB-20 questionnaire. On average patients showed more negative attitudes and feelings towards their own bodies [t(29) = ,6.6 p b. 01] and experienced their bodies as being less healthy and strong (body dynamics) than controls [t(29)= ,5.3 p b .01]. Neuroimaging data The aim of the current study was to investigate the impact of body size modulation from two perspectives in bulimia nervosa and control participants. We calculated a whole-brain three-way ANOVA for the factors task × group × distortion level of self-images. The statistical threshold was set at p b .001, uncorrected for multiple comparisons, the cluster size threshold was set at N15 voxels. The results are presented in Tables 1 and 2 and Figs. 3–6. Further investigations of clusters located in primary or secondary somatosensory or motor cortices were omitted. Main effect of group Middle frontal gyrus (MFG), posterior parietal cortex demonstrated stronger activation in healthy controls. To obtain areas possibly involved in general

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differences of body image processing independent from distinguishing satisfaction versus perception, we firstly calculated a main effect for group over the task and level factor. Clusters in the left MFG (BA 9) and in the right posterior parietal cortex (BA 31) demonstrated a significantly stronger activation in the healthy control group (Fig. 3). Group × task interaction MFG demonstrates a stronger recruitment for body size estimation only in the healthy group. Interestingly, the MFG clusters exhibiting a group-main effect also demonstrated a strong group × task interaction (Fig. 3). To clarify the direction of the interactions, we carried out post-hoc t- tests. The healthy group activated the cluster in the MFG significantly stronger for the perception task in contrast to the satisfaction task (MFG, t(15) = .2.42, p b .05), whereas the bulimic patients demonstrated the opposite effect — MFG was more strongly activated during satisfaction ratings (MFG, t(14) = 2.6, p b .05). Group × distortion level interaction Posterior temporal-occipital cortex is sensitive for body size distortions in the healthy group only. A cluster in the left lateral occipital cortex demonstrated a significant group × distortion level interaction (Fig. 4). For healthy subjects, this cluster, located near the extra-striate body area (EBA, Downing et al., 2001), was sensitive for body size distortions (about actual bthin, t(15) = 3.8, p b .001; about actual b thick t(15) =4.1, p b .001), whereas bulimic patients did not demonstrate such a modulation (about actual = thin t(14) =1.6, p =.13; about actual = thick t(14) = 1.1, p = .27). For this cluster, no difference occurred between satisfaction rating and body size estimation, main effect task F(1,29) = .86, p = .36. Group × task × distortion-size interaction The three-way-interaction group × task × distortion level revealed a range of significant activated clusters in the bilateral anterior insula (BA 13), around the medial frontal gyrus/anterior cingulate cortex (ACC), in the posterior insula (LH, BA 13) and the superior frontal cortex (Table 2 and Fig. 5).

Fig. 2. a, Behavioral responses for bulimic patients (dashed line) and controls (solid line) in satisfaction rating (sat) for thin, about actual and thick self-images, (+2 = image is identical to ideal body shape). Bulimic patients were less satisfied with their current body shape than controls and preferred to be thinner. b, Behavioral responses for bulimic patients (dashed line) and controls (solid line) in perception rating (perc) for thin, about actual and thick self-images (+ 2 = image is realistic and undistorted). Bulimic patients estimated their presented thicker self-images to be more realistic than controls.

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Table 1 Brain regions exhibiting significant activity of main effect group and two-way interaction from ANOVA. Area

Hem

x

y

z

Cluster size

Main effect group, control N bulemia Middle frontal gyrus, BA 9 Posterior Cingulate Cortex, BA 31 Precuneus, BA 31

LH RH RH

− 24 17 23

27 − 29 − 50

30 34 35

152 201 79

Group × task Middle Frontal Gyrus, BA 9

LH

− 25

26

27

498

xyz = −25, 1, 7; see Fig. 6). The result of the correlation analysis further supports an involvement of the insula (LH) in satisfaction with one's body image. B. Complex interaction in posterior insula (LH, BA 13) and superior frontal cortex (RH, BA 6) Activity in the posterior insula and superior frontal cortex demonstrated a complex, three-way interaction pattern without a clear relationship to behavioral task demands or to group differences (Table 2). Discussion

Group × level Posterior temporal-occipital cortex, BA39

LH

− 52

− 72

11

21

Centers of mass and cluster sizes. BA = Brodmann area. Hem. = hemisphere, (LH = left, RH = right), Group = group with the stronger BOLD response; x, y, z = Talairach coordinates; Cluster size is provided in mm3, random effect, p b .001, uncorrected, cluster size threshold was set at N 15, N = 31.

A. Activity in anterior insula and in medial frontal gyrus/ACC is higher for the satisfaction rating and the amount of activity in insula reflects the pattern of the satisfaction rating. A post-hoc t-test demonstrated that activity in the anterior insula (RH) and in the medial frontal gyrus was generally higher for the satisfaction rating in contrast to the body size estimation task [RH insula: t(30) = 1.81 p b .05; medial frontal gyrus: t(30) = 1.8 p b .05]; this effect occurred also as a trend in the left anterior insula/striatum [t(30) = 1.6 p = .07]. Interestingly, the amount of bilateral insula activity reflected the pattern of the satisfaction rating task for bulimia nervosa and control participants: for the bulimic group a linear trend occurred with a decline in insula and medial frontal gyrus activity from thinner sized images to actual and fatter images [RH insula: F (1,14) = 7, p b.05; LH insula: F (1,14) = 6.2, p b.05, medial frontal gyrus: F (1,14) = 11, p b.001]. In contrast, in healthy controls insula activity was best fitted with a quadratic trend [RH insula: F(1,15) = 22, p b .001, LH insula: F(1,15) = 4.6, p b .05], meaning that activity was highest for actual sized self-images in contrast to thinner and fatter sized selfimages. This quadratic interaction for healthy controls could not be observed in the medial frontal gyrus [F(1,15) = .9, p = .35] limiting the evidence that activity in this area also reflects the pattern of the satisfaction rating. Correlation-analysis The amount of insula activity reflects the pattern of the satisfaction rating for patients and controls. Furthermore, patients with bulimia were significantly more satisfied with thin self images than controls. To get a clearer insight into the possible relationship between insula-activity and satisfaction rating of thin body images we calculated a whole-brain-correlation analysis between BOLDactivity and satisfaction rating for the thin self images. We found a moderate positive relationship between insula-activity (LH) and satisfaction rating; r = .486, p = .008 (cluster size = 32 voxels; Table 2 Brain regions exhibiting significant activity of main effect for three-way interaction group × level × task from ANOVA. Area

Hem

x

y

z

Cluster size

Anterior insula, BA13 Anterior insula BA13/striatum Medial frontal cortex/ACC BA32 Posterior insula Postcentral gyrus BA 3 Postcentral gyrus BA 3 Cerebellum, Culmen

RH LH RH LH RH LH RH

31 − 28 11 − 36 42 − 37 18

20 11 10 − 11 − 27 − 29 − 44

2 3 43 20 58 53 − 20

134 133 342 413 1660 11317 1701

Centers of mass and cluster sizes. BA = Brodmann area. Hem. = hemisphere, (LH = left, RH = right), Group = group with the stronger BOLD response; x, y, z = Talairach coordinates; Cluster size is provided in mm3, random effect, p b .001, uncorrected, and cluster size threshold was set at N15, N = 31.

Body satisfaction and body size experience are two distinguishable aspects of body image both often investigated behaviorally in the field of eating disorders. In this study we examined the neural correlates of these aspects in a sample of bulimic patients. In the satisfaction rating task, participants were asked to compare a presented image of themselves with their own ideal body image. In this way participants had to retrieve their representation of what they subjectively judged to be an ideal body size and compare whether a more or less distorted image fitted to their ideal body image. In the body size estimation task – in which the same stimuli were used – subjects were instructed to compare the presented self-images with their real body image. This task thus required subjects to retrieve the representation of their current body image and compare it with the presented stimuli. We were able to demonstrate that compared to controls bulimic subjects judged their ‘about actual size’ body images as poorly corresponding to their ideal body and thus were less satisfied with their current body shape. Furthermore, bulimic patients also overestimated their own body size during the body size estimation task. A broad range of brain regions demonstrated differences between the groups and complex interactions. In general, bulimic subjects demonstrated a reduced activation of the precuneus and MFG during both tasks in contrast to healthy controls. Anterior insula and medial frontal gyrus activity was generally higher for the satisfaction rating task. More specifically, the bilateral insula and the medial frontal gyrus seemed to be modulated by group differences in the satisfaction rating, indicating an important role of this circuit in emotional components of the body image. In contrast, the MFG was more strongly activated during body size estimation only in healthy controls. Furthermore, lateral temporaloccipital cortex near the EBA was sensitive to distortions of the selfimages for healthy subject, while bulimic subjects did not demonstrate such a modulation. It can be speculated that the MFG and the lateral temporal-occipital cortex/EBA support a realistic perception of one's own body size and shape (indicated by an increased activity) and that the observed activation patterns in these areas are related to the body size estimation bias in bulimia nervosa. Satisfaction rating We hypothesized that patients suffering from bulimia nervosa were less satisfied with their current body shape in comparison to healthy controls (see also Cash and Deagle, 1996; Mizes et al., 2004; Ruuska et al., 2005). Accordingly, patients rated their ‘about actual size’ body images with lower satisfaction scores than controls. More negative attitudes towards their actual body shape were additionally confirmed by the FKB-20 questionnaire. The bilateral anterior insula showed higher activation during the satisfaction rating task in contrast to the size estimation task, indicating an important role of this area in emotional components of the body image (Mohr et al., 2009). Remarkably, the activity in this brain area also reflects the differences in satisfaction rating between bulimic and healthy participants: whereas healthy subjects demonstrated the highest insula activity for “about actual” sized self-images, bulimic patients activated this region strongest for the thinner self-

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Fig. 3. Comparison of bulimia vs. control by a random-effect GLM (main effect for group). Activated clusters are shown at p b .001, the cluster size threshold was set at N15 voxels. Middle frontal gyrus (MFG) and posterior parietal cortex (PPC) demonstrated stronger activation for healthy controls. MFG also demonstrates a two-way interaction group (bulimia vs. control) × task (satisfaction vs. perception rating) with stronger recruitment for body size estimation in the healthy group and the opposite effect for the bulimic subjects, betavalues for bulimic patients = dashed line and controls = solid line.

images. Interestingly, both groups demonstrated less recruitment of this area for the thick images, reflecting their negative satisfaction rating for bigger self-images in the accordant rating (see Table 1). The moderate positive relationship between insula activity and satisfaction rating while viewing thin body images also underlines a possible involvement of this region in body image satisfaction. This result

Fig. 4. Random-effects GLM, two-way interaction group (bulimia vs. control) × level (thin; about actual, thick). Activated clusters are shown at p b .001, the cluster size threshold was set at N15 voxels. The cluster in the posterior temporal-occipital cortex, located near the extra-striate body area, is sensitive for body size distortions only in the healthy group (a). For this cluster no difference occurred between satisfaction rating and body size estimation (b), beta-values for bulimic patients = dashed line and controls = solid line.

supports former findings of higher anterior insula activation for the desired body size in patients suffering from anorexia nervosa (Mohr et al., 2009; Friederich et al., 2010) and confirms theories of altered insula functioning during the integration of interoceptive information and emotion processing in eating disorders (Kaye et al., 2009). For healthy subjects insula activation was often related to emotional and interoceptive awareness (for a review see Craig, 2009), to a wide range of emotions including disgust (Zald and Pardo, 2000; Fitzgerald et al., 2004) and aversion (Nitschke et al., 2006), but also happiness and reward (Johnstone et al., 2006, for a review see Phan et al., 2004; Goldstone et al., 2009). Some studies demonstrated that the amount of anterior insula activity is positively related to the amount of reward provided by a stimulus (e.g. Goldstone et al., 2009). Furthermore, the anterior insula is supposed to be related to selfinstantiation processes by linking cognitive, affective and interoceptive information (e.g. Critchley et al., 2004, for a review see Kaye et al., 2009). It can be speculated that during the satisfaction rating of one's own body size the anterior insula represents a key region for integration processes of interoceptive body awareness, affective evaluation and reward, resulting in a higher activity during the presentation of the desired body shape. Activity in the medial frontal gyrus/ACC (BA 32), an important projection area of the insular cortex (Devinsky et al., 1995), was also more highly activated during the satisfaction rating task and demonstrated complex interactions with group and distortion level. This supports an extended anterior insula-medial frontal gyrus/ACC-circuit for the awareness and evaluation of one's own body. Medial frontal gyrus/ACC activity is related to widespread emotional processing like conflict monitoring in the emotional Stroop task (e.g. Bush et al., 2000) and is likely to be involved in modulating patterns of autonomic physiological responses underlying emotion (Ongür and Price, 2005; Urry et al., 2009). Importantly, in our study, medial frontal gyrus/ACC did not reflect the differences in satisfaction rating between bulimic and healthy participants as the bilateral anterior insula did. Thus, anterior insula activity seems to be exclusively related to emotional evaluation processes of one's own body during satisfaction rating; contrastingly,

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Fig. 5. Random-effects GLM, three-way interaction group (bulimia vs. control) × level (thin; about actual, thick) × task (satisfaction vs. perception rating). Activated clusters are shown at p b .001, the cluster size threshold was set at N15 voxels. Activity in bilateral anterior insula and in medial frontal gyrus/ACC is higher for the satisfaction rating (see results) and the amount of activity in insula reflects the pattern of the satisfaction rating in bulimia and controls, beta-values for bulimic patients = dashed line, controls = solid line.

the role of the medial frontal gyrus/ACC in emotional body image processing seems to be more speculative. In this study we cannot exclude that the reported group differences in brain activation are specific for the processing of self body images. There is also the possibility that these differences in brain activation are induced by the processing of the body images of other persons. To clarify this issue future studies could investigate body processing in eating disorders, e.g., by gradually morphing different levels of body size and identity. Body size comparison As hypothesized patients did overestimate their own body size in contrast to healthy controls which supports results of former studies

(Vocks et al., 2007a, 2007b; Cash and Deagle, 1996). The lateral occipital cortex is a key region for the perception of the human body (EBA, Downing et al., 2001). Neurons in the EBA are demonstrated to be sensitive for changes in size of presented body images (Aleong and Paus, 2010). In accordance to Aleong and Paus (2010) our results show that the activity of the lateral occipital cortex was sensitive to distortions of body size (thinner or thicker) in healthy controls. In the present study the talairach coordinates of the center of mass in the lateral occipital cortex (xyz= −52, − 72, 11) lay within the range of coordinates reported in 15 fMRI studies for the left EBA (x = −38… −63, y = −64…−80, z = −2…22; mean xyz = −49, −72, 8; calculated by Moro et al., 2008). Interestingly, in bulimic patients this region was not modulated by distortions of body size. It can be speculated that the lateral occipital

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Fig. 6. Scatterplott of the satisfaction rating for thin self images and the activity (betaweights) in the insula (LH, cluster size = 32 voxels; xyz = − 25, 1, 7).

cortex/EBA plays an important role in detecting body size and shape distortions, and that the function of body size sensitive neurons in this region is pathologically changed in bulimia nervosa. Supporting evidence for a possible involvement of the EBA in body perception and eating disorders was also given by Vocks et al. (2010). The authors reported a reduced responsiveness of the EBA in patients with eating disorders that changed after cognitive-behavioral therapy (body image exposure). Further support for a possible link between EBA, body image distortions and eating disorders is also given by the finding of a reduced EBA gray matter density in anorectic patients (Suchan et al., 2010). The important role of the EBA in adequate body shape perception is also underlined by brain lesion studies (Moro et al., 2008) and by application of rTMS (Urgesi et al., 2004). Moro et al. (2008) documented a double dissociation of body shape recognition (lesions to the EBA) and body action recognition (lesions to the ventral premotor cortex) by combining different perception tasks with lesion-mapping techniques. Urgesi et al. disrupted the adequate perception of the human body and its parts, except the face, with application of rTMS on the coordinates of the EBA. In conjunction with the present data these results suggest that reduced and inhibited responsiveness of the EBA could be responsible for perceptual body image distortions. Several possible mechanisms could lead to the alteration of lateral occipital cortex/EBA activations in bulimic patients. First, it is possible that self body images are avoided by patients leading to a distraction of attention, lower activation in lateral occipital cortex and less precise body size comparison. However, a general distraction of attention should rather induce a general deficit in the perception of the own body size (under- and overestimation) than the overestimation that was found by the present study. Second, it is known that bulimic patients spend increased attention to pictures of thin models in media and internet (Blechert et al., 2009; for a review of selective attention in eating disorders see Williamson et al., 1999; Dobson and Dozois, 2004; see also pro-mia forums). It could be hypothesized that this selective visual examination of thin body images in daily life leads to prolonged neural adaptation in the EBA, realized by a reduced and flattened activation profile in conjunction with perceptual aftereffects in form of an overestimation of the own body. This interpretation is highly speculative, but some studies give evidence for body related perceptual after-effects following a prolonged examination of thin and thick body shapes in healthy subjects (Hummel et al., 2011) in conjunction with a reduced and flattened activation of the EBA (neural EBA-adaptation; Cziraki et al., 2010). Another region possibly related to the body size overestimation is the MFG. The healthy subjects recruited this region stronger for the body size comparison task exclusively, ruling out a possible task-unspecific involvement of the MFG for e.g. decision making. Importantly, the MFG seems to be an unspecific workspace for body size estimation, because

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no modulation for distortion levels of the images occurred in this region. It can be speculated that healthy subjects use this brain region for executive control (MFG and executive functions e.g. Petrides, 1994; Miller and Cohen, 2001; Mohr et al., 2006) as well as spatial processing (MFG and spatial processing, e.g., Goldman-Rakic, 1987; Mohr et al., 2006) during the body size estimation task which leads to a more accurate body size estimation in healthy controls. The posterior parietal cortex is supposed to be related to the multimodal coding of the body schema (Schwoebel and Coslett, 2005) and to multimodal spatial imagery (e.g. Muckli et al., 2006). Alterations in this area were found to be associated with distortions of spatial body relationships and motor behavior (Sirigu et al., 1991) as well as with body image processing in anorectic (Uher et al. 2005; Mohr et al., 2009) and bulimic (Uher et al. 2005) patients. Alterations in body size perception were assumed to be related to multimodal coding of the body in posterior parietal areas (Uher et al., 2005; Mohr et al., 2009). In this study we were able to find a generally lower recruitment of the posterior parietal cortex for bulimic patients in contrast to healthy participants. This result seems to support the assumption of a general deficit in the recruitment of a multimodally coded body image in posterior parietal areas. However, we were not able to demonstrate a task- or distortion-specific involvement of the posterior parietal lobe in body image processing for bulimic patients, as was the case for anorectic subjects (Mohr et al., 2009). There are several explanations for this discrepancy. First, the body perception bias in the perception task of our study might not be specifically related to alterations in posterior parietal lobe functioning caused by eating disorders. Findings of alterations in this area of anorectic subjects might be triggered by other factors such as cerebral changes in metabolism due to long-lasting malnutrition. Second, spatial body image distortion could be induced by alterations in multiple cortical regions involved in visuo-spatial processing like the parietal cortex, higher visual areas (EBA, FBA) and frontal regions. Thus, unknown factors led anorectic subjects to demonstrate changes in parietal areas while bulimic patients showed alterations in visual and prefrontal regions (but see Suchan et al., 2010). Third and importantly, fMRI-studies are often limited by small sample sizes (b30 participants per group). So, only group differences with large to very large effect sizes can be detected providing a high risk of missing detections of finely modulated activations in task-specific regions. In summary, body size perception bias in bulimic patients seems to be induced by a reduced sensitiveness of body size distortions in the lateral occipital cortex, combined with a lacking recruitment of the MFG, maybe related to a lack of central executive top-down control and spatial processing. Conclusion Our results provide behavioral evidence for a processing bias of bulimic patients in both body satisfaction rating and body size estimation task. Furthermore, anterior insula activity was exclusively related to the satisfaction rating task and also reflected the differences between bulimic patients and controls during satisfaction rating. Thus, the anterior insula seems to play an important role in emotional evaluation of one's own body, and accordingly for the development and maintenance of bulimia nervosa. The present results also highlight the importance of psychotherapeutic interventions targeting the low acceptance of the actual body shape and the idealization of low body weight that is highly relevant within the circuit of restraining food intake, binging and purging. Amongst others the lateral occipital cortex is an area specialized in the perception of the human body (EBA). Interestingly, this region was sensitive to distortions of body size (thinner or thicker) only in healthy controls, whereas bulimic subjects did not demonstrate such a modulation. It can be speculated that this missing sensitivity to

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distortions of one's own body in the lateral occipital cortex raises the vulnerability for the development of a perceptional bias in BN. Furthermore, bulimic subjects did not recruit the MFG in contrast to controls during the body size estimation task, maybe indicating a reduced involvement of central executive resources as well as reduced spatial manipulation capacities during this task. This activation pattern of lateral occipital cortex and MFG might mainly be responsible for the body size overestimation that is found behaviorally. Although disturbances of the different aspects of body image in bulimia nervosa were confirmed in several studies (Vocks et al., 2007a, 2007b; Cash and Deagle, 1996; Mizes et al., 2004; Ruuska et al., 2005) specific therapies concerning the body image remained rather rare. Furthermore, most therapies addressing body image use interventions that mainly target body-size dissatisfaction (by e.g. exposure towards the body combined with cognitive restructuring) and not body size over-estimation. Yet, there is some evidence that body size overestimation is a better predictor for the development of eatingdisorders in longitudinal studies than body-size dissatisfaction (e.g. Liechty, 2010; Isomaa et al., 2011). Our present results underline that bulimic patients, similar to anorectic patients (Mohr et al., 2009), exhibit a deficit in body size estimation adjacent to body size dissatisfaction. Moreover, specifically associated neuronal correlates in e.g. higher visual areas can be identified. In conclusion, the present results support the development of psychotherapeutic treatment strategies that specifically target both aspects of body image distortions through, e.g., exposures to emotional aspects of body image (e.g. Vocks et al., 2007a, 2007b; Jansen et al., 2008) and additionally multimodal trainings of body size perception and awareness. Acknowledgments We thank Karl-Heinz Untch and Caroline Mannweiler for helpful discussions. The authors declare no conflicts of interests including any financial, personal or other relationships with other people or organizations within three years of beginning the work submitted that could inappropriately influence their work. References Aleong, R., Paus, T., 2010. Neural correlates of human body perception. J. Cogn. Neurosci. 22 (3), 482–495. American Psychiatric Association, 2000. Diagnostic and statistical manual of mental disorders DSM-IV-TR, 4th ed. American Psychiatric Publishing, Washington, DC. Blechert, J., Ansorge, U., Tuschen-Caffier, B., 2009. A body-related dot-probe task reveals distinct attentional patterns for bulimia nervosa and anorexia nervosa. J. Abnorm. Psychol. 119 (3), 575–585. Bush, G., Luu, P., Posner, M.I., 2000. Cognitive and emotional influences in anterior cingulate cortex. Trends Cogn. Sci. 4, 215–222. Cash, T.F., Deagle, E.A., 1996. The nature and extent of body-image disturbances in anorexia nervosa and bulimia nervosa. a meta-analysis. Int. J. Eat. Disord. 22 (2), 107–125. Clement, U., Lowe, B., 1996. Validation of the FKB-20 as scale for the detection of body image distortions in psychosomatic patients. Psychother. Psychosom. Med. Psychol. 46, 254–259. Craig, A.D., 2009. How do you feel now? The anterior insula and human awareness. Nat. Rev. Neurosci. 10, 59–70. Critchley, H.D., Wiens, S., Rotshtein, P., Ohman, A., Dolan, R.J., 2004. Neural systems supporting interoceptive awareness. Nat. Neurosci. 7 (2), 189–195. Cziraki, C., Greenlee, M.W., Kovács, G., 2010. Neural correlates of high-level adaptationrelated after effects. J. Neurophysiol. 103 (3), 1410–1417. Devinsky, O., Morrell, M.J., Vogt, B.A., 1995. Contributions of anterior cingulate to behavior. Brain 118, 279–306. Dobson, K.S., Dozois, D.J., 2004. Attentional biases in eating disorders: a meta-analytic review of Stroop performance. Clin. Psychol. Rev. 23, 1001–1022. Downing, P.E., Jiang, Y., Shuman, M., Kanwisher, N., 2001. A cortical area selective for visual processing of the human body. Science 28, 2470–2473. Fallon, A.E., Rozin, P., 1985. Sex differences in perceptions of desirable body shape. J. Abnorm. Psychol. 94, 102–105. Fitzgerald, D.A., Posse, S., Moore, G.J., Tancer, M.E., Nathan, P.J., Phan, K.L., 2004. Neural correlates of internally-generated disgust via autobiographical recall, a functional magnetic resonance imaging investigation. Neurosci. Lett. 11, 91–96. Friederich, H.C., Brooks, S., Uher, R., Campbell, I.C., Giampietro, V., Brammer, M., Williams, S.C., Herzog, W., Treasure, J., 2010. Neural correlates of body dissatisfaction in anorexia nervosa. Neuropsychologia 48 (10), 2878–2885.

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