Motor system-dependent effects of amygdala and ventral striatum lesions on explore-exploit behaviors

Deciding whether to forego immediate rewards or explore new opportunities is a key component of flexible behavior and is critical for the survival of the species. Although previous studies have shown that different cortical and subcortical areas, including the amygdala and ventral striatum (VS), are implicated in representing the immediate (exploitative) and future (explorative) value of choices, the effect of the motor system used to make choices has not been examined. Here we tested male rhesus macaques with amygdala or VS lesions on two versions of a three-arm bandit task where choices were registered with either a saccade or an arm movement. In both tasks we presented the monkeys with explore-exploit tradeoffs by periodically replacing familiar options with novel options that had unknown reward probabilities. We found that monkeys explored more with saccades but showed better learning with arm movements. VS lesions caused the monkeys to be more explorative with arm movements and less explorative with saccades, although this may have been due to an overall decrease in performance. VS lesions affected the monkeys’ ability to learn novel stimulus-reward associations in both tasks, while after amygdala lesions this effect was stronger when choices were made with saccades. Further, on average, VS and amygdala lesions reduced the monkeys’ ability to choose better options only when choices were made with a saccade. These results show that learning reward value associations to manage explore-exploit behaviors is motor-system dependent and they further define the contributions of amygdala and VS to reinforcement learning.Significance StatementThe amygdala and VS are known to be important for learning reward associations and for mediating explore-exploit behaviors. These behaviors are typically studied in experimental paradigms where choices are made with a single motor system. Here we show that nonhuman primates mediate explore-exploit behaviors in a motor system-dependent way. Monkeys were more explorative with eye movements but showed better learning performance with arm movements. Moreover, we showed different effects of amygdala and VS lesions on explore-exploit behaviors based on the motor system implementing task choices. Thus, we further define amygdala and VS contributions to explore-exploit behaviors and suggest that a different value representation might be driving learning in the oculomotor and skeletomotor systems.