Abstract deliberation by visuomotor neurons in prefrontal cortex

During visually guided behavior, the prefrontal cortex plays a pivotal role in mapping sensory inputs onto appropriate motor plans. When the sensory input is ambiguous, this involves deliberation. It is not known whether the deliberation is implemented as a competition between possible stimulus interpretations or between possible motor plans. Here we study neural population activity in prefrontal cortex of macaque monkeys trained to flexibly report categorical judgments of ambiguous visual stimuli. The subjects judged whether a visual stimulus presented near the central visual field was oriented clockwise or counterclockwise from vertical. They communicated their judgment with a saccade to one of two peripheral visual targets. The meaning of the response options was signaled by the targets’ orientation (clockwise vs counterclockwise), and was unrelated to their spatial position (one target was placed in the neurons’ estimated motor response field, the other on the opposite side of the fixation mark). Because the spatial configuration of the choice targets varied randomly from trial-to-trial, our task design allowed for the dissociation of neural predictors of the upcoming categorical choice and the upcoming motor response used to report this choice. We find that the population activity initially represents the level of commitment to a categorical choice before transitioning into the stereotypical representation of the motor plan. We show that stimulus strength and prior expectations both bear on the formation of the categorical choice, but not on the formation of the action plan. These results reveal that prefrontal circuits involved in action selection are also used for the deliberation of abstract propositions, divorced from a specific motor plan, thus providing a crucial mechanism for abstract reasoning.