Neural Representations of Post-Decision Choice Confidence and Reward Expectation in the Caudate Nucleus and Frontal Eye Field

Abstract

Performance monitoring that supports ongoing behavioral adjustments is often examined in the context of either choice confidence for perceptual decisions (i.e., "did I get it right?") or reward expectation for reward-based decisions (i.e., "what reward will I receive?"). However, our understanding of how the brain encodes these distinct evaluative signals remains limited because they are easily conflated, particularly in commonly used two-alternative tasks with symmetric rewards for correct choices. Previously we reported behavioral and neural results related to decision formation by monkeys performing a visual motion discrimination task with asymmetric rewards (Doi et al., 2020; Fan et al., 2020). Here we leveraged this task design to partially decouple trial-by-trial estimates of choice confidence and reward expectation and examine their impacts on behavior and their representations in the caudate nucleus (part of the striatum in the basal ganglia) and the frontal eye field (FEF, in prefrontal cortex). We found that these evaluative signals had infrequent, but consistent, effects on the behavior of well-trained monkeys. We also identified distinguishable representations of the two types of signals in FEF and caudate neurons, including different distribution patterns, time courses, and relationships to behavior in the two brain areas. These results suggest that the cortico-striatal decision network may use diverse evaluative signals for performance monitoring and add to our understanding of the different roles of the FEF and caudate nucleus in decision-related computations.