Cortical pattern generation during dexterous movement is input-driven.

Abstract

SummaryMotor cortex controls skilled arm movement by sending temporal patterns of activity to lower motor centers1. Local cortical dynamics are thought to shape these patterns throughout movement execution2–4. External inputs have been implicated in setting the initial state of motor cortex5,6, but they may also have a pattern-generating role. Here, we dissect the contribution of local dynamics and inputs to cortical pattern generation during a prehension task in mice. Perturbing cortex to an aberrant state prevented movement initiation, but after the perturbation was released, cortex either bypassed the normal initial state and immediately generated the pattern that controls reaching, or it failed to generate this pattern. The difference in these two outcomes was likely due to external inputs. We directly investigated the role of inputs by inactivating thalamus; this perturbed cortical activity and disrupted limb kinematics at any stage of the movement. Activation of thalamocortical axon terminals at different frequencies disrupted cortical activity and arm movement in a graded manner. Simultaneous recordings revealed that both thalamic activity and the current state of cortex predicted changes in cortical activity. Thus, the pattern generator for dexterous arm movement is distributed across multiple, strongly-interacting brain regions.