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Altered Pallidocortical Low-Beta Oscillations During Self-Initiated Movements in Parkinson Disease

BACKGROUND: Parkinson disease (PD) patients have difficulty with self-initiated (SI) movements, presumably related to basal ganglia thalamocortical (BGTC) circuit dysfunction, while showing less impairment with externally cued (EC) movements. OBJECTIVES: We investigate the role of BGTC in movement i...

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Autores principales: Choi, Jeong Woo, Malekmohammadi, Mahsa, Sparks, Hiro, Kashanian, Alon, Cross, Katy A., Bordelon, Yvette, Pouratian, Nader
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2020
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7390921/
https://www.ncbi.nlm.nih.gov/pubmed/32792918
http://dx.doi.org/10.3389/fnsys.2020.00054
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author Choi, Jeong Woo
Malekmohammadi, Mahsa
Sparks, Hiro
Kashanian, Alon
Cross, Katy A.
Bordelon, Yvette
Pouratian, Nader
author_facet Choi, Jeong Woo
Malekmohammadi, Mahsa
Sparks, Hiro
Kashanian, Alon
Cross, Katy A.
Bordelon, Yvette
Pouratian, Nader
author_sort Choi, Jeong Woo
collection PubMed
description BACKGROUND: Parkinson disease (PD) patients have difficulty with self-initiated (SI) movements, presumably related to basal ganglia thalamocortical (BGTC) circuit dysfunction, while showing less impairment with externally cued (EC) movements. OBJECTIVES: We investigate the role of BGTC in movement initiation and the neural underpinning of impaired SI compared to EC movements in PD using multifocal intracranial recordings and correlating signals with symptom severity. METHODS: We compared time-resolved neural activities within and between globus pallidus internus (GPi) and motor cortex during between SI and EC movements recorded invasively in 13 PD patients undergoing deep brain stimulation implantation. We compared cortical (but not subcortical) dynamics with those recorded in 10 essential tremor (ET) patients, who do not have impairments in movement initiation. RESULTS: SI movements in PD are associated with greater low-beta (13–20 Hz) power suppression during pre-movement period in GPi and motor cortex compared to EC movements in PD and compared to SI movements in ET (motor cortex only). SI movements in PD are uniquely associated with significant low-beta pallidocortical coherence suppression during movement execution that correlates with bradykinesia severity. In ET, motor cortex neural dynamics during EC movements do not significantly differ from that observed in PD and do not significantly differ between SI and EC movements. CONCLUSION: These findings implicate low beta BGTC oscillations in impaired SI movements in PD. These results provide a physiological basis for the strategy of using EC movements in PD, circumventing diseased neural circuits associated with SI movements and instead engaging circuits that function similarly to those without PD.
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spelling pubmed-73909212020-08-12 Altered Pallidocortical Low-Beta Oscillations During Self-Initiated Movements in Parkinson Disease Choi, Jeong Woo Malekmohammadi, Mahsa Sparks, Hiro Kashanian, Alon Cross, Katy A. Bordelon, Yvette Pouratian, Nader Front Syst Neurosci Neuroscience BACKGROUND: Parkinson disease (PD) patients have difficulty with self-initiated (SI) movements, presumably related to basal ganglia thalamocortical (BGTC) circuit dysfunction, while showing less impairment with externally cued (EC) movements. OBJECTIVES: We investigate the role of BGTC in movement initiation and the neural underpinning of impaired SI compared to EC movements in PD using multifocal intracranial recordings and correlating signals with symptom severity. METHODS: We compared time-resolved neural activities within and between globus pallidus internus (GPi) and motor cortex during between SI and EC movements recorded invasively in 13 PD patients undergoing deep brain stimulation implantation. We compared cortical (but not subcortical) dynamics with those recorded in 10 essential tremor (ET) patients, who do not have impairments in movement initiation. RESULTS: SI movements in PD are associated with greater low-beta (13–20 Hz) power suppression during pre-movement period in GPi and motor cortex compared to EC movements in PD and compared to SI movements in ET (motor cortex only). SI movements in PD are uniquely associated with significant low-beta pallidocortical coherence suppression during movement execution that correlates with bradykinesia severity. In ET, motor cortex neural dynamics during EC movements do not significantly differ from that observed in PD and do not significantly differ between SI and EC movements. CONCLUSION: These findings implicate low beta BGTC oscillations in impaired SI movements in PD. These results provide a physiological basis for the strategy of using EC movements in PD, circumventing diseased neural circuits associated with SI movements and instead engaging circuits that function similarly to those without PD. Frontiers Media S.A. 2020-07-23 /pmc/articles/PMC7390921/ /pubmed/32792918 http://dx.doi.org/10.3389/fnsys.2020.00054 Text en Copyright © 2020 Choi, Malekmohammadi, Sparks, Kashanian, Cross, Bordelon and Pouratian. http://creativecommons.org/licenses/by/4.0/ This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.
spellingShingle Neuroscience
Choi, Jeong Woo
Malekmohammadi, Mahsa
Sparks, Hiro
Kashanian, Alon
Cross, Katy A.
Bordelon, Yvette
Pouratian, Nader
Altered Pallidocortical Low-Beta Oscillations During Self-Initiated Movements in Parkinson Disease
title Altered Pallidocortical Low-Beta Oscillations During Self-Initiated Movements in Parkinson Disease
title_full Altered Pallidocortical Low-Beta Oscillations During Self-Initiated Movements in Parkinson Disease
title_fullStr Altered Pallidocortical Low-Beta Oscillations During Self-Initiated Movements in Parkinson Disease
title_full_unstemmed Altered Pallidocortical Low-Beta Oscillations During Self-Initiated Movements in Parkinson Disease
title_short Altered Pallidocortical Low-Beta Oscillations During Self-Initiated Movements in Parkinson Disease
title_sort altered pallidocortical low-beta oscillations during self-initiated movements in parkinson disease
topic Neuroscience
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7390921/
https://www.ncbi.nlm.nih.gov/pubmed/32792918
http://dx.doi.org/10.3389/fnsys.2020.00054
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