Oscillatory activity in rostral middle frontal gyrus encodes proactive response restraint in cortico-subcortical motor control network

Abstract

Proactive control refers to preparatory mechanisms that facilitate action inhibition (i.e. enables a person to act with restraint), while reactive response inhibition is a sudden stopping triggered by an external stimulus. Most research has focused on the reactive paradigm, with more limited investigation of proactive control mechanisms. We studied electrophysiologic activity in multiple cortical and subthalamic nucleus (STN) regions in 17 patients with Parkinson’s disease using subdural electrocorticography and deep brain stimulation electrodes. Subjects performed a Go/NoGo task and a simpler Go task. Proactive control was assessed by contrasting Go trials in the context of two tasks. In the rostral middle frontal gyrus, we found increased beta oscillations during movement preparation in Go trials of the Go/NoGo task compared to the Go task. We interpret this activity as a reflection of the role of this region in proactively restraining anticipated responses. Conversely, inferior frontal gyrus and ventral STN were primarily engaged during post‑cue action control. Specifically, withholding of action after the NoGo signal was accompanied by increased theta activity in these regions (significant only before multiple comparison correction based on cluster size). Beta modulation within the STN mirrored those of sensorimotor cortex during successful inhibition and movement execution. In both regions, beta activity decreased during movement and was higher when movement was withheld. Interestingly, beta activity in the middle frontal gyrus was modulated in the opposite direction compared to the STN and sensorimotor cortex. We conclude that communication within the motor control network is frequency dependent, with key nodes promoting specific functions.