Behavioral states affect eye position tuning in the parietal cortex of macaques

Posterior parietal neural populations compute flexible yet stable representations of spatial locations using eye position information and plan effector movements across various goal-directed contexts. Little is known about how space is represented during internally driven, non-goal-directed behaviors and whether these spatial representations are affected by the different behavioral contexts and the underlying brain states. We addressed this issue in medial posterior parietal area V6A, a node of the parietofrontal network, which is involved in space perception and motor planning. We compared eye position signals in single V6A neurons in macaque monkeys during constrained fixations towards visual targets (presented in various directions and distances in the peripersonal and extrapersonal space) with gaze activity during self-paced fixations that occurred under free gaze conditions in darkness before target appearance. We looked for changes in firing rates and spike variability, in the selectivity of gaze modulations and the structure of the eye position field in the two contexts. We found that, while the firing rates of V6A neurons were comparable in the two conditions, the spatial tuning of gaze activity was stronger during the spontaneous fixations than during task-constrained fixations on visual targets. Moreover, neural responses were more variable in constrained fixation. Our results confirm the flexibility of spatial representations in parietal cortex and suggest that eye-position signals can provide spatial information in a wider range of behavioral contexts beyond visual and visuomotor processing.