Ventral striatum’s role in learning from gains and losses

Significance

A broad set of neural circuits, including the amygdala and frontal-striatal systems, has been implicated in mediating learning from gains and losses. The ventral striatum (VS) has been implicated in several aspects of this process. Here, we examined the specific contribution of the VS to learning from gains vs. losses. We found that the VS plays a role in learning to choose between two options that vary in gains but plays no role in learning to choose between two options when one or both is associated with a loss. Computational modeling supported this by showing that animals with VS lesions specifically learned slowly when choosing between gains but not losses.

Abstract

Adaptive behavior requires animals to learn from experience. Ideally, learning should both promote choices that lead to rewards and reduce choices that lead to losses. Because the ventral striatum (VS) contains neurons that respond to aversive stimuli and aversive stimuli can drive dopamine release in the VS, it is possible that the VS contributes to learning about aversive outcomes, including losses. However, other work suggests that the VS may play a specific role in learning to choose among rewards, with other systems mediating learning from aversive outcomes. To examine the role of the VS in learning from gains and losses, we compared the performance of macaque monkeys with VS lesions and unoperated controls on a reinforcement learning task. In the task, the monkeys gained or lost tokens, which were periodically cashed out for juice, as outcomes for choices. They learned over trials to choose cues associated with gains, and not choose cues associated with losses. We found that monkeys with VS lesions had a deficit in learning to choose between cues that differed in reward magnitude. By contrast, monkeys with VS lesions performed as well as controls when choices involved a potential loss. We also fit reinforcement learning models to the behavior and compared learning rates between groups. Relative to controls, the monkeys with VS lesions had reduced learning rates for gain cues. Therefore, in this task, the VS plays a specific role in learning to choose between rewarding options.