Neuronal population dynamics during motor plan cancellation in nonhuman primates

Significance

A core question in neuroscience is how the brain generates arm movements. Most studies have approached this issue by investigating the neuronal dynamics that accompany movement production, leaving unanswered the question of which aspects of this dynamics are logically necessary to make the movement. Here, we explored this topic by characterizing the neuronal correlates of movement decisions between active inhibition and release of movements. We found that active inhibition and stillness require neuronal signals to be confined in a functional subspace, while actions depend on the transit of activities in an orthogonal space. This dynamics is characterized by a threshold mechanism finally allowing the translation of the motor plan into overt action.

Abstract

To understand the cortical neuronal dynamics behind movement generation and control, most studies have focused on tasks where actions were planned and then executed using different instances of visuomotor transformations. However, to fully understand the dynamics related to movement control, one must also study how movements are actively inhibited. Inhibition, indeed, represents the first level of control both when different alternatives are available and only one solution could be adopted and when it is necessary to maintain the current position. We recorded neuronal activity from a multielectrode array in the dorsal premotor cortex (PMd) of monkeys performing a countermanding reaching task that requires, in a subset of trials, them to cancel a planned movement before its onset. In the analysis of the neuronal state space of PMd, we found a subspace in which activities conveying temporal information were confined during active inhibition and position holding. Movement execution required activities to escape from this subspace toward an orthogonal subspace and, furthermore, surpass a threshold associated with the maturation of the motor plan. These results revealed further details in the neuronal dynamics underlying movement control, extending the hypothesis that neuronal computation confined in an “output-null” subspace does not produce movements.