The rhythm of the executive gate of speech: subthalamic low-frequency oscillations increase during verbal generation.

Abstract

We investigated neurophysiological mechanisms of subthalamic nucleus involvement in verbal fluency through a verbal generation task. The subthalamic nucleus is thought to act as a behavioural go/no-go instance by means of oscillatory communication in the theta band with the prefrontal cortex. Because subthalamic alpha-theta frequency stimulation has been shown to exert beneficial effects on verbal fluency in Parkinson's disease, we hypothesized that an alpha-theta oscillatory network involving the subthalamic nucleus underlies verbal generation task performance as a gating instance for speech execution. Postoperative subthalamic local field potential recordings were performed during a verbal generation compared to a control task. Time-frequency analysis revealed a significant alpha-theta power increase and enhanced alpha-theta coherence between the subthalamic nucleus and the frontal surface EEG during the verbal generation task. Beta and gamma oscillations were not significantly modulated by the task. Power increase significantly correlated with verbal generation performance. Our results provide experimental evidence for local alpha-theta oscillatory activity in the subthalamic nucleus and coherence to frontal associative areas as a neurophysiological mechanism underlying a verbal generation task. Thus, verbal fluency improvement during subthalamic alpha-theta stimulation in Parkinson's disease is likely due to an enhancement of alpha-theta oscillatory network activity. Alpha-theta oscillations can be interpreted as the rhythmic gating signature in a speech executing subthalamic-prefrontal network.