Robert S Eisinger1, Jackson N Cagle2, Jose D Alcantara2, Enrico Opri2, Stephanie Cernera2, Anh Le3, Elena M Torres Ponce3, Joseph Lanese3, Brawn Nelson3, Janine Lopes4, Christopher Hundley3, Tasmeah Ravy3, Samuel S Wu5, Kelly D Foote6, Michael S Okun7, Aysegul Gunduz8. 1. Department of Neuroscience, University of Florida, Gainesville, Florida. Electronic address: eisinger@ufl.edu. 2. J. Crayton Pruitt Department of Biomedical Engineering, University of Florida, Gainesville, Florida. 3. Department of Neuroscience, University of Florida, Gainesville, Florida. 4. Department of Neurology, Norman Fixel Institute for Neurological Diseases, University of Florida, Gainesville, Florida. 5. Department of Biostatistics, University of Florida, Gainesville, Florida. 6. Department of Neurosurgery, Norman Fixel Institute for Neurological Diseases, University of Florida, Gainesville, Florida. 7. Department of Neuroscience, University of Florida, Gainesville, Florida; Department of Neurology, Norman Fixel Institute for Neurological Diseases, University of Florida, Gainesville, Florida; Department of Neurosurgery, Norman Fixel Institute for Neurological Diseases, University of Florida, Gainesville, Florida. 8. Department of Neuroscience, University of Florida, Gainesville, Florida; J. Crayton Pruitt Department of Biomedical Engineering, University of Florida, Gainesville, Florida.
Abstract
BACKGROUND: Impulsivity and impulse control disorders are common in Parkinson's disease 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 of either the subthalamic nucleus (STN) or globus pallidus internus (GPi) affects 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 deep brain stimulation electrodes. METHODS: We measured LFPs during a simple rewarding Go/NoGo paradigm in 39 female and male human patients with Parkinson's disease manifesting variable amounts of impulsivity who were undergoing unilateral deep brain stimulation 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 NoGo stimulus evaluation, reward feedback, and loss feedback. Motor and limbic functions were anatomically separable in the GPi but not in the STN. Across participants, LFP reward processing responses in the STN and GPi uniquely depended on the severity of impulsivity. CONCLUSIONS: This study establishes LFP correlates of impulsivity within the STN and GPi regions. We propose a model for basal ganglia reward processing that includes the bottom-up role of the GPi in reward salience and the top-down role of the STN in cognitive control.
BACKGROUND: Impulsivity and impulse control disorders are common in Parkinson's disease 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 of either the subthalamic nucleus (STN) or globus pallidus internus (GPi) affects 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 deep brain stimulation electrodes. METHODS: We measured LFPs during a simple rewarding Go/NoGo paradigm in 39 female and male human patients with Parkinson's disease manifesting variable amounts of impulsivity who were undergoing unilateral deep brain stimulation 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 NoGo stimulus evaluation, reward feedback, and loss feedback. Motor and limbic functions were anatomically separable in the GPi but not in the STN. Across participants, LFP reward processing responses in the STN and GPi uniquely depended on the severity of impulsivity. CONCLUSIONS: This study establishes LFP correlates of impulsivity within the STN and GPi regions. We propose a model for basal ganglia reward processing that includes the bottom-up role of the GPi in reward salience and the top-down role of the STN in cognitive control.
Keywords:
Deep brain stimulation; Globus pallidus; Impulse control disorder; Impulsivity; Local field potentials; Parkinson’s disease; Reward processing; Subthalamic nucleus
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