The motivational role of the ventral striatum and amygdala in learning from gains and losses.

The ventral striatum (VS) and amygdala are two structures often implicated as essential structures for learning. The literature addressing the contribution of these areas to learning, however, is not entirely consistent. We propose that these inconsistencies are due to learning environments and the effect they have on motivation. To differentiate aspects of learning from environmental factors that affect motivation, we ran a series of experiments with varying task factors. We compared monkeys (Macaca mulatta) with VS lesions, amygdala lesions, and unoperated controls on reinforcement learning (RL) tasks that involve learning from both gains and losses as well as from deterministic and stochastic schedules of reinforcement. We found that for all three groups, performance varied by experiment. All three groups modulated their behavior in the same directions, to varying degrees, across the three experiments. This behavioral modulation is why we find deficits in some experiments, but not others. The amount of effort animals exhibited differed depending on the learning environment. Our results suggest that the VS is important for the amount of effort animals will give in rich deterministic and relatively leaner stochastic learning enivornments. We also showed that monkeys with amygdala lesions can learn stimulus-based RL in stochastic environments and environments with loss and conditioned reinforcers. These results show that learning environments shape motivation and that the VS is essential for distinct aspects of motivated behavior. (PsycInfo Database Record (c) 2023 APA, all rights reserved).

Effects of Amygdala Lesions on Object-Based Versus Action-Based Learning in Macaques.

The neural systems that underlie reinforcement learning (RL) allow animals to adapt to changes in their environment. In the present study, we examined the hypothesis that the amygdala would have a preferential role in learning the values of visual objects. We compared a group of monkeys (Macaca mulatta) with amygdala lesions to a group of unoperated controls on a two-armed bandit reversal learning task. The task had two conditions. In the What condition, the animals had to learn to select a visual object, independent of its location. And in the Where condition, the animals had to learn to saccade to a location, independent of the object at the location. In both conditions choice-outcome mappings reversed in the middle of the block. We found that monkeys with amygdala lesions had learning deficits in both conditions. Monkeys with amygdala lesions did not have deficits in learning to reverse choice-outcome mappings. Rather, amygdala lesions caused the monkeys to become overly sensitive to negative feedback which impaired their ability to consistently select the more highly valued action or object. These results imply that the amygdala is generally necessary for RL.

Ventral striatum's role in learning from gains and losses.

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.