Neural dynamics of variable grasp movement preparation in the macaque fronto-parietal network

Abstract

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 investigating how preparation time affects this process. Two macaque monkeys (Macaca mulatta) 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 hand area (F5) 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 preparation, then diverged depending on the delay. Although similar types of single unit responses were present in both areas, population activity in AIP stabilized within a unique memory state while F5 activity continued to evolve, tracking subjective anticipation of the go cue. Intriguingly, activity during movement initiation clustered into two trajectory clusters, 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 static and dynamic components of movement preparation as well as differentiation between cortical areas is possible through population level analysis. Significance StatementMany of our movements must occur with no warning, while others we can prepare in advance. Yet, it's unclear how planning for movements along the spectrum between these two situations differs in the brain. Two macaque monkeys made reach to grasp movements after varying amounts of preparation time while we recorded from premotor and parietal cortex. We found that the initial response to a grasp instruction was specific to the required movement, but not the preparation time, reflecting required processing. However, when more preparation time was given, neural activity achieved unique states that likely related to withholding movements and anticipation of movement, which was more prevalent in premotor cortex, suggesting differing roles of premotor and parietal cortex in grasp planning.

Latent factors and dynamics in motor cortex and their application to brain-machine interfaces

“…Similarly, in MC, an altered preparatory state relates to altered movement execution. If neural preparatory activity is not in the right state at the time of the go cue, either due to natural fluctuations (Churchland et al, 2006a;Afshar et al, 2011;Michaels et al, 2015Michaels et al, , 2018, sub-threshold microstimulation during the delay period (Churchland and Shenoy, 2007b), or a change in the location of the target (Ames et al, 2014), the reaction time is delayed compared to well-prepared trials. This suggests that, if motor preparation is incorrect, subjects do not move until their preparation has been corrected.…”

Autoregressive Point Processes as Latent State-Space Models: A Moment-Closure Approach to Fluctuations and Autocorrelations

“…ese models have been used in a variety of tasks, such as describing population spiking activity in the motor system (e.g. Truccolo 2014, 2016;Churchland et al 2012;Michaels et al 2017). However, while such models can certainly lead to biological insights, latent state-space models remain phenomenological: the recurrent spiking activity itself does not implement the latent state-space dynamics (Fig.…”