Functional Dissociation in Frontal and Striatal Areas for Processing of Positive and Negative Reward Information

Reward-seeking behavior depends critically on processing of positive and negative information at various stages such as reward anticipation, outcome monitoring, and choice evaluation. Behavioral and neuropsychological evidence suggests that processing of positive (e.g., gain) and negative (e.g., loss) reward information may be dissociable and individually disrupted. However, it remains uncertain whether different stages of reward processing share certain neural circuitry in frontal and striatal areas, and whether distinct but interactive systems in these areas are recruited for positive and negative reward processing. To explore these issues, we used a monetary decision-making task to investigate the roles of frontal and striatal areas at all three stages of reward processing in the same event-related functional magnetic resonance imaging experiment. Participants were instructed to choose whether to bet or bank a certain number of chips. If they decided to bank or if they lost a bet, they started over betting one chip. If they won a bet, the wager was doubled in the next round. Positive reward anticipation, winning outcome, and evaluation of right choices activated the striatum and medial/middle orbitofrontal cortex, whereas negative reward anticipation, losing outcome, and evaluation of wrong choices activated the lateral orbitofrontal cortex, anterior insula, superior temporal pole, and dorsomedial frontal cortex. These findings suggest that the valence of reward information and counterfactual comparison more strongly predict a functional dissociation in frontal and striatal areas than do various stages of reward processing. These distinct but interactive systems may serve to guide human's reward-seeking behavior.