Neural Dynamics of Variable Grasp-Movement Preparation in the Macaque Frontoparietal Network

Our voluntary grasping actions lie on a continuum between immediate action and waiting for the right moment, depending on the context. Therefore, studying grasping requires an investigation into how preparation time affects this process. Two macaque monkeys (Macaca mulatta; one male, one female) performed a grasping task with a short instruction followed by an immediate or delayed go cue (0–1300 ms) while we recorded in parallel from neurons in the grasp preparation relevant area F5 that is part of the ventral premotor cortex, and the anterior intraparietal area (AIP). Initial population dynamics followed a fixed trajectory in the neural state space unique to each grip type, reflecting unavoidable movement selection, then diverged depending on the delay, reaching unique states not achieved for immediately cued movements. Population activity in the AIP was less dynamic, whereas F5 activity continued to evolve throughout the delay. Interestingly, neuronal populations from both areas allowed for a readout tracking subjective anticipation of the go cue that predicted single-trial reaction time. However, the prediction of reaction time was better from F5 activity. Intriguingly, activity during movement initiation clustered into two trajectory groups, corresponding to movements that were either "as fast as possible" or withheld movements, demonstrating a widespread state shift in the frontoparietal grasping network when movements must be withheld. Our results reveal how dissociation between immediate and delay-specific preparatory activity, as well as differentiation between cortical areas, is possible through population-level analysis.

SIGNIFICANCE STATEMENT Sometimes when we move, we consciously plan our movements. At other times, we move instantly, seemingly with no planning at all. Yet, it's unclear how preparation for movements along this spectrum of planned and seemingly unplanned movement differs in the brain. Two macaque monkeys made reach-to-grasp movements after varying amounts of preparation time while we recorded from the premotor and parietal cortex. We found that the initial response to a grasp instruction was specific to the required movement, but not to the preparation time, reflecting required movement selection. However, when more preparation time was given, neural activity achieved unique states that likely related to withholding movements and anticipation of movement, shedding light on the roles of the premotor and parietal cortex in grasp planning.