Neural signature of food reward processing in bulimic-type eating disorders

Social Cognitive and Affective Neuroscience, 2016, 1393–1401 doi: 10.1093/scan/nsw049 Advance Access Publication Date: 6 April 2016 Original article Neural signature of food reward processing in bulimic-type eating disorders 1 Department of General Internal Medicine and Psychosomatics, Centre for Psychosocial Medicine, University Hospital Heidelberg, Heidelberg, Germany, 2Department of Psychosomatic Medicine and Psychotherapy Medical Faculty, Heinrich-Heine-University Düsseldorf, Düsseldorf, Germany, 3Department of General Adult Psychiatry, Centre for Psychosocial Medicine, Heidelberg, University Hospital Heidelberg, Heidelberg, Germany, and 4Department of Neuroradiology, University Hospital Heidelberg, Heidelberg, Germany Correspondence should be addressed to Joe J. Simon, Centre for Psychosocial Medicine, General Internal Medicine and Psychosomatics, University Hospital Heidelberg, Im Neuenheimer Feld 410, 69120 Heidelberg, Germany. E-mail: . Abstract Clinical observations and similarities to addiction suggest heightened reward sensitivity to food in patients with bulimictype eating (BTE) disorders. Therefore, we investigated the expectation and receipt of food reward compared with monetary reward in patients with BTE. Fifty-six patients with BTE (27 patients with binge eating disorder and 29 with bulimia nervosa) and 55 matched healthy control participants underwent event-related functional magnetic resonance imaging while performing both food and monetary incentive delay tasks. BTE patients exhibited reduced brain activation in the posterior cingulate cortex during the expectation of food and increased activity in the medial orbitofrontal cortex, anterior medial prefrontal cortex and posterior cingulate cortex during the receipt of food reward. These findings were relevant to food because we found no significant group differences related to monetary reward. In the patients, higher brain activity in the medial orbitofrontal cortex during the receipt of food reward was related to higher levels of trait food craving and external eating. BTE patients exhibited increased hedonic processing during the receipt of food reward. These findings corroborate the notion that an altered responsiveness of the reward network to food stimuli is associated with BTE. Key words: bulimia nervosa; binge eating disorder; reward processing; functional MRI; medial orbitofrontal cortex; posterior cingulate cortex Introduction Binge eating behavior is characterized by recurrent episodes of eating an objectively large amount of food and is associated with feelings of loss of control. Binge eating behavior is clinically considered to be a subtype of overeating, although the neurobiological underpinnings of different subtypes of overeating remain unknown. Binge eating represents the core symptom of bulimictype eating (BTE) disorders such as bulimia nervosa (BN) and binge eating disorder (BED). These are common mental disorders with heightened morbidities and all-cause mortalities (Arcelus et al., 2011). To counteract binge eating and prevent weight gain, BN patients exhibit compensatory behaviors such as self-induced vomiting or laxative misuse. BED patients exhibit no compensatory behaviors, overweight or obesity in the long term occurs in  the majority of cases (Agh et al., 2015). A common theory that has been put forward to explain the phenomenon of overeating is the ‘food addiction model’, which suggests that an unbalanced neuronal reward system overrides the homeostatic regulation of food intake (Friederich et al., 2013; Smith and Robbins, 2013). There is evidence from experimental animal research that intermittent availability of sugar leads to Received: 4 November 2015; Revised: 11 March 2016; Accepted: 31 March 2016 C The Author (2016). Published by Oxford University Press. For Permissions, please email: V 1393 Joe J. Simon,1,2 Mandy Skunde,1 Stephan Walther,1,3 Martin Bendszus,4 Wolfgang Herzog,1 and Hans-Christoph Friederich1,2 1394 | Social Cognitive and Affective Neuroscience, 2016, Vol. 11, No. 9 Table 1. Demographic and clinical characteristics of participants Patients with BED (N 5 27) Mean s.d. Mean s.d. 38.26 32.61 12.07 23.07 2.64 95.08 19.37 28.04 26.04 41.30 81.81 13.75 4.55 1.69 12.54 1.75 6.75 6.93 8.92 6.99 14.64 19.66 38.00 34.02 12.18 8.61 — 83.44 15.39 13.61 20.54 33.21 57.54 10.85 4.50 2.06 7.48 — 23.44 6.97 9.24 6.37 13.49 17.60 deprivation-induced sugar binging that is associated with the sensitization of mesocorticolimbic reward pathways to energydense foods (Corwin et al., 2011). Previous studies using functional magnetic resonance imaging (fMRI) in humans have found that, in response to visual food cues, patients with BTE display hyper-reactivity in reward regions including the orbitofrontal cortex (OFC) and anterior cingulate cortex (ACC) (Uher et al., 2004; Schienle et al., 2009). Patients with BN also exhibit reduced anterior insula activity (Schienle et al., 2009; Bohon and Stice, 2011), which suggests the involvement of the primary gustatory cortex. However, not all studies found differences in neural processing of food cues in BTE (Van den Eynde et al., 2013). Studies examining gustatory processing have found that the reactivity of the reward system is positively related to binge eating episodes in patients with BED (Wang et al., 2011), whereas in BN, both increases (Radeloff et al., 2014) and decreases (Frank et al., 2006; Bohon and Stice, 2011) in brain responses within the reward network have been observed. Furthermore, general reward processing (i.e. monetary reward) is not significantly altered in BTE patients compared with normal-weight controls (Wagner et al., 2010; Balodis et al., 2013). A previous study using repetitive transcranial magnetic stimulation (rTMS) found that stimulation of the dorsolateral prefrontal cortex reduces cue-induced food craving in patients with BTE (Van den Eynde et al., 2010), indicating a shared neural correlate of food craving across BTE disorders. In summary, the available findings support the occurrence of altered responsivity of the reward system to both visual food cues and palatable food in BTE. However, most of the applied paradigms have not allowed for the differentiation between anticipation and receipt of food rewards nor have they directly compared food reward with general reward processing. Therefore, the aims of this study were to investigate whether BTE patients display dysfunctional activations in brain reward network during the anticipation and receipt of food reward and to examine whether these differences are specific to food reward or whether they result from a generalized impairment in reward processing. In line with the Research Domain Criteria framework (RDoC, NIMH, 2008), which proposes the investigation of specific neurobiological dimensions across mental disorders, we adopted a study design focusing on the investigation of the ‘positive valence system’ domain (Sanislow (...truncated)