Independent circuits in basal ganglia and cortex for the processing of reward and precision feedback

In order to understand human decision making it is necessary to understand how the brain uses feedback to guide goal-directed behavior. The ventral striatum (VS) appears to be a key structure in this function, responding strongly to explicit reward feedback. However, recent results have also shown striatal activity following correct task performance even in the absence of feedback. This raises the possibility that, in addition to processing external feedback, the dopamine-centered reward circuit might regulate endogenous reinforcement signals, like those triggered by satisfaction in accurate task performance. Here we use functional magnetic resonance imaging (fMRI) to test this idea. Participants completed a simple task that garnered both reward feedback and feedback about the precision of performance. Importantly, the design was such that we could manipulate information about the precision of performance within different levels of reward magnitude. Using parametric modulation and functional connectivity analysis we identified brain regions sensitive to each of these signals. Our results show a double dissociation: frontal and posterior cingulate regions responded to explicit reward but were insensitive to task precision, whereas the dorsal striatum - and putamen in particular - was insensitive to reward but responded strongly to precision feedback in reward-present trials. Both types of feedback activated the VS, and sensitivity in this structure to precision feedback was predicted by personality traits related to approach behavior and reward responsiveness. Our findings shed new light on the role of specific brain regions in integrating different sources of feedback to guide goal-directed behavior.