Resting-state synchrony between anterior cingulate cortex and precuneus relates to body shape concern in anorexia nervosa and bulimia nervosa

Abstract

Cortical areas supporting cognitive control and salience demonstrate different neural responses to visual food cues in patients with eating disorders. This top-down cognitive control, which interacts with bottom-up appetitive responses, is tightly integrated not only in task conditions but also in the resting-state. The dorsal anterior cingulate cortex (dACC) is a key node of a large-scale network that is involved in self-referential processing and cognitive control. We investigated resting-state functional connectivity of the dACC and hypothesized that altered connectivity would be demonstrated in cortical midline structures involved in self-referential processing and cognitive control. Seed-based resting-state functional connectivity was analyzed in women with anorexia nervosa (N=18), women with bulimia nervosa (N=20) and age matched healthy controls (N=20). Between group comparisons revealed that the anorexia nervosa group exhibited stronger synchronous activity between the dACC and retrosplenial cortex, whereas the bulimia nervosa group showed stronger synchronous activity between the dACC and medial orbitofrontal cortex. Both groups demonstrated stronger synchronous activity between the dACC and precuneus, which correlated with higher scores of the Body Shape Questionnaire. The dACC-precuneus resting-state synchrony might be associated with the disorder-specific rumination on eating, weight and body shape in patients with eating disorders.

Introduction

Anorexia Nervosa (AN) is characterized by intense fear of gaining weight and relentless pursuit of thinness (American Psychiatric Association, 2013). The term ‘anorexia (lack of appetite)’ is misleading, as individuals with anorexia nervosa are preoccupied with food and exhibit inappropriate eating rituals (Kaye et al., 2009). In addition, excessive cognitive control traits such as perfectionism, distorted body image, and obsessive–compulsive personality are predisposing factors and persist after clinical recovery (Anderluh et al., 2003, Johnson et al., 2006). By contrast, subjects with Bulimia Nervosa (BN) are known to lack of impulse control and experience intense food craving, which likely results in binge-eating episodes (Moreno et al., 2009). However, it has not yet been determined whether AN and BN share a primary disturbance of cognitive control and what neural correlates underlie their different clinical presentations (Brooks et al., 2012).

Cortical areas supporting cognitive control and salience demonstrate different neural responses to visual food cues in patients with eating disorders compared to healthy individuals (García-García et al., 2013). Functional brain imaging studies have reported abnormal prefrontal neural responses in patients with anorexia nervosa applying symptom-provoking paradigms (Cowdrey et al., 2011, Brooks et al., 2011a, Uher et al., 2004). Previously we reported that women with anorexia nervosa demonstrate greater activations within the dorsal anterior cingulate cortex (dACC) while watching high-calorie food images and proposed that the dACC activations represent excessive cognitive control effort to restrain appetite as well as the ambivalence toward food (Kim et al., 2012). This top-down cognitive control network, which interacts with bottom-up appetitive responses, is tightly integrated not only in task conditions but also in the resting-state (Cole and Schneider, 2007).

Here, we expanded our focus and investigated the resting-state functional connectivity of the dACC in patients with AN and BN. Resting-state functional connectivity is based on the observation that spontaneous blood oxygen level dependent (BOLD) signal fluctuations among brain regions reflects intrinsic interactions between functionally correlated regions (Biswal et al., 1995). Therefore, the resting-state functional connectivity is not a reaction to external stimuli, but represents intrinsic properties of functional brain organization (Raichle et al., 2001). The ACC is a part of the default network, which exhibits high baseline metabolic activity at rest and is proposed to be associated with self-referential mental activity (Gusnard et al., 2001). Converging evidence suggests that self-referential processing is mediated by cortical midline structures, such as the ventromedial prefrontal cortex, dorsomedial prefrontal cortex, and the posterior cingulate cortex/precuneus (Northoff et al., 2006). Recent studies showed that resting-state functional connectivity between these brain regions involved in self-referential processing and cognitive control were disturbed in participants recovered from anorexia nervosa (Cowdrey et al., 2012). Taken together, we hypothesized that the resting-state functional connectivity between the dACC and other cortical midline structures would be altered in women with eating disorders and underlie their ruminative preoccupation of body image and weight. We performed a region of interest (ROI) seed-based functional connectivity analysis in order to investigate the intrinsic dACC neural network in women with anorexia nervosa and bulimia nervosa.