Diminished frontostriatal activity during processing of monetary rewards and losses in pathological gambling

Abstract

Background: Mesocorticolimbic neurocircuitry and impulsivity have both been implicated in pathological gambling (PG) and in reward processing. However, the neural underpinnings of specific phases of reward and loss processing in PG and their relationships to impulsivity remain only partially understood. The present functional magnetic resonance imaging study examined brain activity associated with different phases of reward and loss processing in PG. Given an inverse relationship between ventral striatal recruitment during anticipation of monetary rewards and impulsivity in alcohol dependence, the current study explored whether a similar association might also be present in PG.

Methods: Fourteen adults with PG and 14 control comparison participants performed the Monetary Incentive Delay Task to identify brain activation changes associated with reward/loss prospect, reward/loss anticipation, and reward/loss notification. Impulsivity was assessed separately using the Barratt Impulsiveness Scale.

Results: Relative to the control comparison group, the PG group exhibited significantly reduced activity in the ventromedial prefrontal cortex, insula, and ventral striatum during several phases, including the prospect and anticipation phases of both gains and losses. Activity in the ventral striatum correlated inversely with levels of impulsivity in PG participants, consistent with prior findings in alcohol dependence.

Conclusions: Relatively decreased activity in corticostriatal neurocircuitry during multiple phases of reward processing suggests consistent alterations in neurocircuitry underlying incentive valuation and loss prediction. Together with findings in alcohol dependence, these results suggest that impulsive tendencies in addictions may be reflected in diminished ventral striatal activations to reward anticipation and may represent targets for treatment development in addictions.

Figure 1

Monetary Incentive Delay Task (MIDT) adapted from Knutson et al., 2001, described in Andrews et al., 2011. Participants first view an incentive cue signaling the potential to win or lose money and then fixate on a ‘+’ (A1 phase). Then, in the A2 phase, a target appears. Participants win (or avoid losing) money by pressing a button before the target disappears. Participants then wait for feedback notifying whether they’ve won or lost the trial (A2). In the outcome phase participants receive feedback on whether they have won or lost the trial and their cumulative earnings. Task difficulty (length of target presentation) is based on reaction times collected during a pre-scan practice session, such that participants win on ~66% of trials.

Figure 2. Group Differences on the MIDT in Ventral Fronto-striatal Areas: PGvsCC

Brain activation maps demonstrate differences in the PG group contrasted with the CC group during the: a) A1 winning phase, associated with the prospect of monetary wins. Maps depict significant differences in the vmPFC, mPFC and precuneus (x = 0), ventral and lateral PFC (z = −15, −11, −6) and ventral striatum (z = −11, −6); b) A1 losing phase, associated with the prospect of monetary losses. Maps depict significant differences in the vmPFC and mPFC (x = 0), ventral and lateral PFC (z = −15, −11, −6), ventral striatum (z = −11, −6) and left insula (z= −6). c) A2 winning phase, associated with the anticipation of winning money. Maps depict significant differences in the vmPFC (x = 0; z = −15, −11, −6) and ventral striatum (z = −11, −6). d) OC winning phase, associated with the receipt of a monetary reward. Maps depict significant differences in the mPFC and vmPFC (x = 0), vmPFC (z = −15, −11, −6), and ventral striatum (z = −11, −6). e) OC losing phase, associated with the receipt of a monetary loss. Maps depict significant differences in the middle PFC and the middle occipital gyrus (x = 0, z=−15,−11), superior temporal gyrus (z = −15, −11, −6), middle temporal gyrus (z = −11, −6) and insula (z = −11, −6). All contrast maps are thresholded at an uncorrected level of p < 0.05 two-tailed and FWE-corrected at p < 0.05 with a cluster threshold of 91. Blue color demonstrates areas where PG subjects show relatively less activation and red color indicates areas where PG subjects show relatively greater activation. For axial slices, the right side of the brain is on the right. Abbreviations: vmPFC = ventromedial prefrontal cortex; mPFC = medial prefrontal cortex.