Population coding of distinct categories of behavior in the frontal eye field

Abstract

Brain regions frequently contribute to the control of diverse behaviors. Within these regions, individual neurons often respond to various motor tasks, suggesting that the ability to control multiple behaviors is rooted in the organization of neuronal populations. To study this organization, we examined how the frontal eye field (FEF) encodes distinct behaviors by recording the activity of 1200 neurons during various eye movement tasks in two female fascicularis monkeys. We focused on three behaviors: smooth pursuit, pursuit suppression, and saccades. We found that single neurons tended to respond in all three tasks, thus challenging the notion that the FEF is organized into task-specific clusters. We then identified the low-dimensional subspaces that contained most of the population activity during each behavior and quantified the extent of overlap between these spaces across behaviors. Population activity during pursuit and pursuit suppression exhibited a substantial overlap, with highly correlated directional tuning at the single-neuron level, as reflected by similar outcomes for the population decoders. These distinct behaviors combined with similar encoding suggest that the suppression of movement occurs mostly downstream from the FEF. By contrast, pursuit and saccades mostly occupied orthogonal subspaces, prompting an independent linear readout of saccades and pursuit. Thus overall, these results indicate that distinct behaviors can exhibit either separate or overlapping population codes within a specific brain region, hence emphasizing the importance of the system-level organization of behavior. Significance statementHow do brain areas control multiple behaviors? We investigated the organization of the FEF in monkeys during three different types of eye movements: smooth pursuit, pursuit suppression, and saccades. We found that individual neurons tended to respond to all three tasks, thus challenging a task-specific FEF cluster organization. Further, the low-dimensional subspaces that contained most of the population activity during pursuit and pursuit suppression overlapped substantially, implying that movement suppression occurs downstream from the FEF. In contrast, pursuit and saccades occupied orthogonal subspaces, prompting independent linear readouts. These results underscore the importance of adopting a system-level perspective to comprehend how diverse behaviors are encoded in the brain.