Many hats: intratrial and reward level-dependent BOLD activity in the striatum and premotor cortex

Human functional magnetic resonance imaging (fMRI) studies, as well as lesion, drug, and single-cell recording studies in animals, suggest that the striatum plays a key role in associating sensory events with rewarding actions, both by facilitating reward processing and prediction (i.e., reinforcement learning) and by biasing and later updating action selection. Previous human neuroimaging research has failed to dissociate striatal activity associated with reward, stimulus, and response processing, and previous electrophysiological research in nonhuman animals has typically only examined single striatal subregions. Overcoming both these limitations, we isolated blood oxygen level-dependent (BOLD) signal associated with four intratrial processes (stimulus, preparation of response, response, and feedback) in a visuomotor learning task and examined activity associated with each within four striatal subregions (ventral striatum, putamen, head of the caudate nucleus, and body of the caudate) and the lateral premotor cortex. Overall, the striatum and lateral premotor cortex were recruited during all trial components, confirming their importance in all aspects of visuomotor learning. However, the caudate was most active at stimulus and feedback, whereas the putamen peaked in activity at response. Activation in the lateral premotor cortex was, surprisingly, strongest during stimulus and following response as feedback approached. Activity was additionally examined at three reward magnitudes. Reward magnitude affected neural activity only during stimulus in the caudate, putamen, and premotor cortex, whereas the ventral striatum showed reward sensitivity during both stimulus and feedback. Collectively, these results indicate that each striatal region makes a unique contribution to visuomotor learning through functions performed at different points within single trials.