Uncertainty Shapes Neural Dynamics in Motor Cortex During Reaching

Abstract

Voluntary reaching movements are often made with incomplete information about the movement goal, which may require the brain to flexibly adjust motor plans and ongoing movements. To examine how uncertainty about a reach target influences neural preparation and execution, we recorded activity from dorsal premotor (PMd) and primary motor (M1) cortices of a rhesus macaque trained to reach to one of two potential targets. In the task, a timing cue flashed three times in succession. Potential targets were displayed at the time of the first flash and the monkey needed to initiate the movement almost simultaneously with the third flash. Colorings of potential targets indicated the probability that the target would be at one location or the other, thereby inducing varying levels of uncertainty about the final target location. On half the trials, the final target was displayed so late that the monkey had to guess the target location, based on cues provided by the potential targets. While the monkey performed this task, we recorded 165 neurons from PMd and 37 from M1. Population neural trajectories in the preparatory subspace of PMd (but not M1) were progressively less expansive with higher levels of uncertainty. Despite differences in preparatory states associated with uncertainty, the movements produced were the same. The narrower separation between states suggested a neural-based explanation for more rapid movement re-preparation with higher uncertainty. Furthermore, we found a dimension in neural state-space representing the level of uncertainty during movement preparation and execution. SIGNIFICANCE STATEMENTThe dorsal premotor cortex (PMd) in primates plays a critical role in organizing preparatory states needed for the execution of target-directed movements mediated downstream by the primary motor cortex (M1). But what if the location of the target is uncertain - as often occurs in our daily lives, such as reaching for a pair of glasses in the dark that have fallen to the floor. We found that different levels of uncertainty are clearly represented in population neural activity during preparation for movement in monkey PMd but not M1. Furthermore, these different neural states related to uncertainty were not associated with changes in the movements produced. These findings provide further insight (and questions) about the operations of the motor cortex.