Neurons of the human subthalamic nucleus engage with local delta frequency processes during action cancellation

Abstract The subthalamic nucleus (STN) is a key regulator of inhibitory control, implicated in decision making under conflict and impulsivity. Delta frequency oscillations, both in the STN and in frontal cortices have been associated with such active decision processes. However, it is yet unclear how neurons of the human STN are linked to local delta frequencies during response inhibition. Here, we recorded STN neurons and local field potentials (LFP) in human patients with Parkinson’s disease (PD) while they performed a stop-signal reaction time task during deep brain stimulation implantation surgery. Delta band LFP activity increased during stimulus processing in the STN. We found that half of the STN neurons responded to a diverse set of behaviorally relevant events that included go and stop signals, with a subset of neurons showing differential responses in successful and unsuccessful attempts at response cancelling. Failure to stop was associated with stronger go signal-related firing increase of STN neurons and their stronger coupling to local delta band LFP activity. Furthermore, a specific population of bursting STN neurons showed increased delta coupling. These suggest that the STN integrates go and stop signal-related information. Increased engagement of STN neurons with local delta band activity during stimulus processing impaired the ability to cancel the ongoing response. This effect may be linked to the disease-related rise in STN neuronal bursting. These findings may shed light on a potential neuronal mechanism linking cortical delta band processes with STN activity, both of which are critical elements in inhibitory control.