Cortico-basal ganglia dynamics of global and selective response inhibition in humans

Overview

Investigation of how the fronto-subthalamic network implements selective versus global response inhibition in humans. Intracranial subthalamic local field potentials (LFPs) and concurrent scalp EEG were recorded during a task that dissociated stimulus-selectivity (signals that should vs. should not trigger inhibition) and response-selectivity (signals that require stopping all responses vs. only some). The principal finding is that all salient signals initially invoke a common, rapid fronto-subthalamic inhibitory event indexed by β-band bursting, but the temporal evolution of that activity diverges by context: global stopping is associated with an early and sustained increase in subthalamic β-bursts, whereas selective stopping exhibits delayed and transient β-burst persistence permitting continuation of non-targeted actions. Frontal cortical and subthalamic β-band activity remain temporally coupled throughout these phases.

Methods and approach

Human participants performed a novel task presenting salient signals that required global stopping, response-selective stopping, or ignoring the signal to maintain ongoing actions. Intracranial recordings targeted the subthalamic nucleus to capture local field potentials; simultaneous scalp EEG provided cortical β-band measurements. Analyses emphasized burst-based metrics in the β frequency band rather than sustained power alone, temporal dynamics of burst rates before and after signals, and metrics of cortico-subthalamic coupling across conditions. Comparisons focused on latency, duration, and amplitude of β-bursts and on cross-structure coherence/time-locking during the post-signal epoch.

Key Findings

All signal types produced an early, rapid increase in β-burst incidence within frontal cortex and subthalamic recordings, indicating a common initial inhibitory engagement. In the global-stop condition, subthalamic β-bursting increased further and remained elevated for over one second post-signal. In the response-selective condition, the secondary elevation of subthalamic β-bursting was delayed and shorter in duration, providing a temporal window of relative disinhibition that permitted continuation of non-targeted responses. The ignore-signals produced the initial burst but did not evoke prolonged subthalamic β activity. Throughout these dynamics, frontal cortical and subthalamic β-band signals exhibited tight temporal coupling, consistent with coordinated fronto-subthalamic engagement.

Implications

Selective inhibition is implemented via rapid, context-dependent recruitment and release of fronto-subthalamic β-band inhibitory processes rather than by wholly distinct mechanisms for global versus selective stopping. The protracted duration of subthalamic β activity, particularly for global stopping, exceeds durations assumed in classic computational race models, supporting models that posit extended inhibitory control during action-stopping. These findings refine mechanistic accounts of inhibitory control and have implications for interpreting pathophysiology and therapeutic modulation of subthalamic circuits in clinical populations characterized by impaired response inhibition.