Altered Brain Activity during Reward Anticipation in Pathological Gambling and Obsessive-Compulsive Disorder

Jung-Seok Choi,Sam-Wook Choi,Jae Yeon Hwang,Young-Chul Shin,Chi-Hoon Choi,Jun Soo Kwon,Wi Hoon Jung,Do-Hyung Kang,Joon Hwan Jang,Jun-Young Lee

doi:10.1371/journal.pone.0045938

Abstract

BackgroundPathological gambling (PG) and obsessive-compulsive disorder (OCD) are conceptualized as a behavioral addiction, with a dependency on repetitive gambling behavior and rewarding effects following compulsive behavior, respectively. However, no neuroimaging studies to date have examined reward circuitry during the anticipation phase of reward in PG compared with in OCD while considering repetitive gambling and compulsion as addictive behaviors.Methods/Principal FindingsTo elucidate the neural activities specific to the anticipation phase of reward, we performed event-related functional magnetic resonance imaging (fMRI) in young adults with PG and compared them with those in patients with OCD and healthy controls. Fifteen male patients with PG, 13 patients with OCD, and 15 healthy controls, group-matched for age, gender, and IQ, participated in a monetary incentive delay task during fMRI scanning. Neural activation in the ventromedial caudate nucleus during anticipation of both gain and loss decreased in patients with PG compared with that in patients with OCD and healthy controls. Additionally, reduced activation in the anterior insula during anticipation of loss was observed in patients with PG compared with that in patients with OCD which was intermediate between that in OCD and healthy controls (healthy controls < PG < OCD), and a significant positive correlation between activity in the anterior insula and South Oaks Gambling Screen score was found in patients with PG.ConclusionsDecreased neural activity in the ventromedial caudate nucleus during anticipation may be a specific neurobiological feature for the pathophysiology of PG, distinguishing it from OCD and healthy controls. Correlation of anterior insular activity during loss anticipation with PG symptoms suggests that patients with PG fit the features of OCD associated with harm avoidance as PG symptoms deteriorate. Our findings have identified functional disparities and similarities between patients with PG and OCD related to the neural responses associated with reward anticipation.

Highlights

Pathological gambling (PG) is a chronic disorder that occurs primarily in men and is characterized by a persistent pattern of continued gambling behavior despite adverse consequences
Correlation of anterior insular activity during loss anticipation with PG symptoms suggests that patients with PG fit the features of obsessive-compulsive disorder (OCD) associated with harm avoidance as PG symptoms deteriorate
Our findings have identified functional disparities and similarities between patients with PG and OCD related to the neural responses associated with reward anticipation

Summary

Introduction

Pathological gambling (PG) is a chronic disorder that occurs primarily in men and is characterized by a persistent pattern of continued gambling behavior despite adverse consequences. With respect to defective reward processing in substance addiction, Beck et al [8] reported that male alcoholics show reduced activation of the ventral striatum during the anticipation of monetary gain relative to that in healthy controls. De Ruiter et al [12] reported that PG is related to response perseveration and diminished reward and punishment sensitivity, as indicated by hypoactivation of the ventrolateral prefrontal cortex when money was gained or lost While these studies looked at outcome of reward, Balodis et al [13] found decreased activity in the ventral striatum during reward anticipation and in the anterior insula during loss anticipation. Pathological gambling (PG) and obsessive-compulsive disorder (OCD) are conceptualized as a behavioral addiction, with a dependency on repetitive gambling behavior and rewarding effects following compulsive behavior, respectively. No neuroimaging studies to date have examined reward circuitry during the anticipation phase of reward in PG compared with in OCD while considering repetitive gambling and compulsion as addictive behaviors

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