Frontostriatal pathways gate processing of behaviorally relevant reward dimensions

The value of rewards arises from multiple hedonic and motivational dimensions. Reward-encoding brain regions such as the ventral striatum (VS) are known to process these dimensions. However, the mechanism whereby distinct reward dimensions are selected for neural processing and guiding behavior remains unclear. Here, we used functional imaging to investigate how human individuals make either hedonic (liking) or motivational (wanting) evaluations of everyday items. We found that the two types of evaluations were differently modulated depending on whether participants won or lost these items. Neural activity in the VS encoded both hedonic and motivational dimensions of reward, whereas ventromedial prefrontal activity encoded primarily motivational evaluations and central orbitofrontal activity encoded predominantly hedonic evaluations. These distinct prefrontal representations arose regardless of which judgment was currently relevant for behavior. Critically, the VS preferentially processed the reward dimension currently being evaluated and showed judgment-specific functional connectivity with the dimension-specific prefrontal areas. Thus, our data are in line with a gating mechanism by which prefrontal cortex (PFC)–VS pathways flexibly encode reward dimensions depending on their behavioral relevance. These findings provide a prototype for a generalized information selection mechanism through content-tailored frontostriatal communication.Author summary: People and animals typically both want and like rewards. Here, we show that these two dimensions of value can be dissociated at both the behavioral and the neural level. In keeping with rodent findings, our human neuroimaging data indicate that the ventral striatum—a part of the reward system in the basal ganglia—encodes both dimensions. However, it does so depending on the judgment being made: during wanting judgments, activity in the ventral striatum increases with the degree of wanting significantly more than with the degree of liking, and vice versa during liking judgments. Accordingly, activity in the ventral striatum expresses the value dimension currently needed for behavior. In contrast, distinct regions of the prefrontal cortex encode either the degree of wanting or the degree of liking, irrespective of judgment type. Functional coupling analysis suggests that the ventral striatum preferentially communicates with wanting- or liking-related regions in the prefrontal cortex according to the type of expressed judgment. These findings suggest that flexible frontostriatal coupling can serve a gating mechanism to achieve behaviorally relevant selection of value dimensions.