Altered brain activity during reward anticipation in pathological gambling and obsessive-compulsive disorder

Abstract

Background: 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. 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 findings: To 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.

Conclusions: Decreased 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.

Figure 1. Group differences in whole brain analysis among healthy controls, PG and OCD in response to anticipation of gain and anticipation of loss (for illustrative purpose, P<0.005 uncorrected, cluster level 15).

PG: Pathological Gambling; OCD, Obsessive-compulsive disorder; L, left; R, right.

Figure 2. Group differences in percent signal changes of the selected brain regions during the phase of anticipation among healthy controls, pathological gambling (PG) and obsessive-compulsive disorder (OCD).

Significant differences in brain activations between groups are marked (asterisk).

Figure 3. The relationship between brain activity in the anterior insula and South Oaks Gambling Screen (SOGS) score in patients with pathological gambling (PG) during the phase of loss anticipation (r = 0.64, p = 0.02).