Oscillatory activity in rostral middle frontal gyrus and subthalamic nucleus encode proactive inhibition in cortico-subcortical motor control network

Abstract

The current model of the action inhibition network includes the prefrontal cortex and the subthalamic nucleus (STN) connected via the prefrontal hyperdirect pathway. Proactive inhibition refers to preparatory mechanisms that facilitate action inhibition (i.e. enables a person to act with restraint), while reactive inhibition is a sudden stopping triggered by an external stimulus. Most research has focused on the reactive paradigm, with more limited investigation of proactive inhibition. We studied electrophysiologic activity in multiple cortical and STN regions in 17 patients with Parkinsons disease using high-resolution intracranial electrodes. Subjects performed a Go/NoGo task and a simpler Go task. Proactive inhibition 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. A similar but weaker, preparatory beta modulation was observed in dorsal STN, while central STN was associated with significant modulation in theta power prior to movement. We interpret this activity as a reflection of the role of these regions in proactively restraining anticipated responses. Conversely, inferior frontal gyrus and ventral STN were primarily engaged during rapid post-cue action control. Specifically, withholding of action after the NoGo signal was accompanied by increased theta activity in these regions. 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. We conclude that communication within the hypothesized motor control network is frequency dependent, with key nodes promoting specific functions.