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Cortical and Subthalamic Nucleus Spectral Changes During Limb Movements in Parkinson's Disease Patients with and Without Dystonia

BACKGROUND: Dystonia is an understudied motor feature of Parkinson's disease (PD). Although considerable efforts have focused on brain oscillations related to the cardinal symptoms of PD, whether dystonia is associated with specific electrophysiological features is unclear. OBJECTIVE: The objec...

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Autores principales: Olson, Joseph W., Nakhmani, Arie, Irwin, Zachary T., Edwards, Lloyd J., Gonzalez, Christopher L., Wade, Melissa H., Black, Sarah D., Awad, Mohammad Z., Kuhman, Daniel J., Hurt, Christopher P., Guthrie, Bart L., Walker, Harrison C.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: John Wiley & Sons, Inc. 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9541849/
https://www.ncbi.nlm.nih.gov/pubmed/35702056
http://dx.doi.org/10.1002/mds.29057
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author Olson, Joseph W.
Nakhmani, Arie
Irwin, Zachary T.
Edwards, Lloyd J.
Gonzalez, Christopher L.
Wade, Melissa H.
Black, Sarah D.
Awad, Mohammad Z.
Kuhman, Daniel J.
Hurt, Christopher P.
Guthrie, Bart L.
Walker, Harrison C.
author_facet Olson, Joseph W.
Nakhmani, Arie
Irwin, Zachary T.
Edwards, Lloyd J.
Gonzalez, Christopher L.
Wade, Melissa H.
Black, Sarah D.
Awad, Mohammad Z.
Kuhman, Daniel J.
Hurt, Christopher P.
Guthrie, Bart L.
Walker, Harrison C.
author_sort Olson, Joseph W.
collection PubMed
description BACKGROUND: Dystonia is an understudied motor feature of Parkinson's disease (PD). Although considerable efforts have focused on brain oscillations related to the cardinal symptoms of PD, whether dystonia is associated with specific electrophysiological features is unclear. OBJECTIVE: The objective of this study was to investigate subcortical and cortical field potentials at rest and during contralateral hand and foot movements in patients with PD with and without dystonia. METHODS: We examined the prevalence and distribution of dystonia in patients with PD undergoing deep brain stimulation surgery.  During surgery, we recorded intracranial electrophysiology from the motor cortex and directional electrodes in the subthalamic nucleus (STN) both at rest and during self‐paced repetitive contralateral hand and foot movements. Wavelet transforms and mixed models characterized changes in spectral content in patients with and without dystonia. RESULTS: Dystonia was highly prevalent at enrollment (61%) and occurred most commonly in the foot. Regardless of dystonia status, cortical recordings display beta (13–30 Hz) desynchronization during movements versus rest, while STN signals show increased power in low frequencies (6.0 ± 3.3 and 4.2 ± 2.9 Hz peak frequencies for hand and foot movements, respectively). Patients with PD with dystonia during deep brain stimulation surgery displayed greater M1 beta power at rest and STN low‐frequency power during movements versus those without dystonia. CONCLUSIONS: Spectral power in motor cortex and STN field potentials differs markedly during repetitive limb movements, with cortical beta desynchronization and subcortical low‐frequency synchronization, especially in patients with PD with dystonia. Greater knowledge on field potential dynamics in human motor circuits can inform dystonia pathophysiology in PD and guide novel approaches to therapy. © 2022 The Authors. Movement Disorders published by Wiley Periodicals LLC on behalf of International Parkinson and Movement Disorder Society
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spelling pubmed-95418492022-10-14 Cortical and Subthalamic Nucleus Spectral Changes During Limb Movements in Parkinson's Disease Patients with and Without Dystonia Olson, Joseph W. Nakhmani, Arie Irwin, Zachary T. Edwards, Lloyd J. Gonzalez, Christopher L. Wade, Melissa H. Black, Sarah D. Awad, Mohammad Z. Kuhman, Daniel J. Hurt, Christopher P. Guthrie, Bart L. Walker, Harrison C. Mov Disord Regular Issue Articles BACKGROUND: Dystonia is an understudied motor feature of Parkinson's disease (PD). Although considerable efforts have focused on brain oscillations related to the cardinal symptoms of PD, whether dystonia is associated with specific electrophysiological features is unclear. OBJECTIVE: The objective of this study was to investigate subcortical and cortical field potentials at rest and during contralateral hand and foot movements in patients with PD with and without dystonia. METHODS: We examined the prevalence and distribution of dystonia in patients with PD undergoing deep brain stimulation surgery.  During surgery, we recorded intracranial electrophysiology from the motor cortex and directional electrodes in the subthalamic nucleus (STN) both at rest and during self‐paced repetitive contralateral hand and foot movements. Wavelet transforms and mixed models characterized changes in spectral content in patients with and without dystonia. RESULTS: Dystonia was highly prevalent at enrollment (61%) and occurred most commonly in the foot. Regardless of dystonia status, cortical recordings display beta (13–30 Hz) desynchronization during movements versus rest, while STN signals show increased power in low frequencies (6.0 ± 3.3 and 4.2 ± 2.9 Hz peak frequencies for hand and foot movements, respectively). Patients with PD with dystonia during deep brain stimulation surgery displayed greater M1 beta power at rest and STN low‐frequency power during movements versus those without dystonia. CONCLUSIONS: Spectral power in motor cortex and STN field potentials differs markedly during repetitive limb movements, with cortical beta desynchronization and subcortical low‐frequency synchronization, especially in patients with PD with dystonia. Greater knowledge on field potential dynamics in human motor circuits can inform dystonia pathophysiology in PD and guide novel approaches to therapy. © 2022 The Authors. Movement Disorders published by Wiley Periodicals LLC on behalf of International Parkinson and Movement Disorder Society John Wiley & Sons, Inc. 2022-06-14 2022-08 /pmc/articles/PMC9541849/ /pubmed/35702056 http://dx.doi.org/10.1002/mds.29057 Text en © 2022 The Authors. Movement Disorders published by Wiley Periodicals LLC on behalf of International Parkinson and Movement Disorder Society https://creativecommons.org/licenses/by/4.0/This is an open access article under the terms of the http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited.
spellingShingle Regular Issue Articles
Olson, Joseph W.
Nakhmani, Arie
Irwin, Zachary T.
Edwards, Lloyd J.
Gonzalez, Christopher L.
Wade, Melissa H.
Black, Sarah D.
Awad, Mohammad Z.
Kuhman, Daniel J.
Hurt, Christopher P.
Guthrie, Bart L.
Walker, Harrison C.
Cortical and Subthalamic Nucleus Spectral Changes During Limb Movements in Parkinson's Disease Patients with and Without Dystonia
title Cortical and Subthalamic Nucleus Spectral Changes During Limb Movements in Parkinson's Disease Patients with and Without Dystonia
title_full Cortical and Subthalamic Nucleus Spectral Changes During Limb Movements in Parkinson's Disease Patients with and Without Dystonia
title_fullStr Cortical and Subthalamic Nucleus Spectral Changes During Limb Movements in Parkinson's Disease Patients with and Without Dystonia
title_full_unstemmed Cortical and Subthalamic Nucleus Spectral Changes During Limb Movements in Parkinson's Disease Patients with and Without Dystonia
title_short Cortical and Subthalamic Nucleus Spectral Changes During Limb Movements in Parkinson's Disease Patients with and Without Dystonia
title_sort cortical and subthalamic nucleus spectral changes during limb movements in parkinson's disease patients with and without dystonia
topic Regular Issue Articles
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9541849/
https://www.ncbi.nlm.nih.gov/pubmed/35702056
http://dx.doi.org/10.1002/mds.29057
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