Distinct roles of the human subthalamic nucleus and dorsal pallidum in Parkinson’s disease impulsivity

Abstract Background Impulsivity and impulse control disorders (ICDs) are common in Parkinson’s disease (PD) and lead to increased morbidity and reduced quality of life. Impulsivity is thought to arise from aberrant reward processing and inhibitory control, but it is unclear why deep brain stimulation (DBS) of either the subthalamic nucleus (STN) or globus pallidus internus (GPi) impacts levels of impulsivity. Our aim was to assess the role of the STN and GPi in impulsivity using invasive local field potential (LFP) recordings from DBS electrodes. Methods We measured LFPs during a simple rewarding Go/No-Go paradigm in 39 female and male human PD patients manifesting variable amounts of impulsivity that were undergoing unilateral DBS of either the STN (18 nuclei) or GPi (28 nuclei). We identified reward-specific LFP event-related potentials and correlated them to impulsivity severity. Results LFPs in both structures modulated during reward-specific Go and No-Go stimulus evaluation, reward feedback, and loss feedback. Motor and limbic functions were anatomically separable in the GPi but not the STN. Across participants, LFP reward processing responses in the STN and GPi uniquely depended on the severity of impulsivity. Conclusion This study establishes LFP correlates of impulsivity within the STN and GPi regions and we propose a model for basal ganglia reward processing which includes the bottom-up role of the GPi in reward salience and the top-down role of the STN in cognitive control.