Primate pre-arcuate cortex actively maintains persistent representations of saccades from plans to outcomes

Abstract

Dorso-lateral prefrontal cortex (dlPFC) in primates plays a key role in the acquisition and execution of flexible, goal-directed behaviors. Recordings in monkey dlPFC have revealed possible neural correlates of the underlying cognitive processes like attention, planning, or decision-making, both at the single-neuron and population levels. Integrating these observations into a coherent picture of dlPFC function is challenging, as these studies typically focused on neural activity in relation to a few, specific events within a single, fully learned behavioral task. Here we obtain a more comprehensive description of dlPFC activity from a large dataset of population recordings in monkeys across a variety of behavioral contexts. We characterized neural activity in relation to saccades that monkeys made freely, or at different stages of training in multiple tasks involving instructed saccades, perceptual discriminations, and reward-based decisions. Across all contexts, we observed reliable and strong modulations of neural activity in relation to a retrospective representation of the most recent saccadic movement. Prospective, planning-like activity was instead limited to task-related, delayed saccades that were directly eligible for a reward. The link between prospective and retrospective representations was highly structured, potentially reflecting a hard-wired feature of saccade responses in these areas. Only prospective representations were modulated by the recent behavioral history, but neither representations were modulated by learning occurring over days, despite obvious concurrent behavioral changes. Dorso-lateral PFC thus combines tightly linked flexible and rigid representations, with a dominant contribution from retrospective signals maintaining the memory of past actions.