Striatal contributions to reward and decision making: making sense of regional variations in a reiterated processing matrix

Abstract

The striatum is the major input nucleus of the basal ganglia. It is thought to play a key role in learning on the basis of positive reinforcement and in action selection. One view of the striatum conceives it as comprising a reiterated matrix of processing units that perform common operations in different striatal regions, namely synaptic plasticity according to a three-factor rule, and lateral inhibition. These operations are required for reinforcement learning and selection of previously reinforced actions. Analysis of the behavioral effects of circumscribed lesions of the striatum, however, suggests regional specialization of learning and decision-making operations. We consider how a basic processing unit may be modified by regional variations in neurochemical parameters, for example, by the gradient in density of dopamine terminals from dorsal to ventral striatum. These variations suggest subtle differences between dorsolateral and ventromedial striatal regions in the temporal properties of dopamine signaling, which are superimposed on regional differences in connectivity. We propose that these variations make sense in relation to the temporal structure of activity in striatal inputs from different regions, and the requirements of different learning operations. Dorsolateral striatal (DLS) regions may be subject to brief, precisely timed pulses of dopamine, whereas ventromedial striatal regions integrate dopamine signals over a longer time course. These differences may be important for understanding regional variations in the contribution to reinforcement of habits, versus incentive processes that are sensitive to the value of expected rewards.