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Movement-Modulation of Local Power and Phase Amplitude Coupling in Bilateral Globus Pallidus Interna in Parkinson Disease

There is converging evidence that bilateral basal ganglia motor networks jointly support normal movement behaviors including unilateral movements. The extent and manner in which these networks interact during lateralized movement remains unclear. In this study, simultaneously recorded bilateral Glob...

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Autores principales: AuYong, Nicholas, Malekmohammadi, Mahsa, Ricks-Oddie, Joni, Pouratian, Nader
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2018
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6046436/
https://www.ncbi.nlm.nih.gov/pubmed/30038563
http://dx.doi.org/10.3389/fnhum.2018.00270
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author AuYong, Nicholas
Malekmohammadi, Mahsa
Ricks-Oddie, Joni
Pouratian, Nader
author_facet AuYong, Nicholas
Malekmohammadi, Mahsa
Ricks-Oddie, Joni
Pouratian, Nader
author_sort AuYong, Nicholas
collection PubMed
description There is converging evidence that bilateral basal ganglia motor networks jointly support normal movement behaviors including unilateral movements. The extent and manner in which these networks interact during lateralized movement remains unclear. In this study, simultaneously recorded bilateral Globus Pallidus interna (GPi) local field potentials (LFP) were examined from 19 subjects with idiopathic Parkinson disease (PD), while undergoing awake deep brain stimulation (DBS) implantation. Recordings were carried out during two behavioral states; rest and cued left hand movement (finger tapping). The state-dependent effects on α- β oscillatory power and β phase-encoded phase amplitude coupling (PAC), including symmetrical and assymetrical changes between hemispheres, were identified. Unilateral hand movement resulted in symmetrical oscillatory power suppression within bilateral GPi at α (8–12 Hz) and high β (21–35 Hz) and increase in power of high frequency oscillations (HFO, 200–300 Hz) frequency bands. Asymmetrical attenuation was also observed at both low β (13–20 Hz) and low γ (40–80 Hz) bands within the contralateral GPi (P = 0.009). In addition, unilateral movement effects on PAC were confined to the contralateral GPi with attenuation of both low β-low γ and β-HFO PAC (P < 0.05). Further analysis showed that the lateralized attenuation of low β and low γ power did not correlate with low β-low γ PAC changes. The overall coherence between bilateral GPi was not significantly altered with unilateral movement, however the preferred phase difference in the high β range increased from 0.23 (±1.31) radians during rest to 1.99 (±0.78) radians during movement execution. Together, the present results suggest that unilateral motor control involves bilateral basal ganglia networks with movement features differentially encoded by distinct frequency bands. The lateralization of low β and low γ attenuation with movement suggests that these frequency bands are specific to the motor act whereas symmetrical expression of α, high β, and HFO oscillations best correspond to motor state. The restriction of movement-related PAC modulation to the contralateral GPi indicates that cross-frequency interactions appear to be associated with lateralized movements. Despite no significant movement-related changes in the interhemispheric coherence, the increase in phase difference suggests that the communication between bilateral GPi is altered with unilateral movement.
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spelling pubmed-60464362018-07-23 Movement-Modulation of Local Power and Phase Amplitude Coupling in Bilateral Globus Pallidus Interna in Parkinson Disease AuYong, Nicholas Malekmohammadi, Mahsa Ricks-Oddie, Joni Pouratian, Nader Front Hum Neurosci Neuroscience There is converging evidence that bilateral basal ganglia motor networks jointly support normal movement behaviors including unilateral movements. The extent and manner in which these networks interact during lateralized movement remains unclear. In this study, simultaneously recorded bilateral Globus Pallidus interna (GPi) local field potentials (LFP) were examined from 19 subjects with idiopathic Parkinson disease (PD), while undergoing awake deep brain stimulation (DBS) implantation. Recordings were carried out during two behavioral states; rest and cued left hand movement (finger tapping). The state-dependent effects on α- β oscillatory power and β phase-encoded phase amplitude coupling (PAC), including symmetrical and assymetrical changes between hemispheres, were identified. Unilateral hand movement resulted in symmetrical oscillatory power suppression within bilateral GPi at α (8–12 Hz) and high β (21–35 Hz) and increase in power of high frequency oscillations (HFO, 200–300 Hz) frequency bands. Asymmetrical attenuation was also observed at both low β (13–20 Hz) and low γ (40–80 Hz) bands within the contralateral GPi (P = 0.009). In addition, unilateral movement effects on PAC were confined to the contralateral GPi with attenuation of both low β-low γ and β-HFO PAC (P < 0.05). Further analysis showed that the lateralized attenuation of low β and low γ power did not correlate with low β-low γ PAC changes. The overall coherence between bilateral GPi was not significantly altered with unilateral movement, however the preferred phase difference in the high β range increased from 0.23 (±1.31) radians during rest to 1.99 (±0.78) radians during movement execution. Together, the present results suggest that unilateral motor control involves bilateral basal ganglia networks with movement features differentially encoded by distinct frequency bands. The lateralization of low β and low γ attenuation with movement suggests that these frequency bands are specific to the motor act whereas symmetrical expression of α, high β, and HFO oscillations best correspond to motor state. The restriction of movement-related PAC modulation to the contralateral GPi indicates that cross-frequency interactions appear to be associated with lateralized movements. Despite no significant movement-related changes in the interhemispheric coherence, the increase in phase difference suggests that the communication between bilateral GPi is altered with unilateral movement. Frontiers Media S.A. 2018-07-09 /pmc/articles/PMC6046436/ /pubmed/30038563 http://dx.doi.org/10.3389/fnhum.2018.00270 Text en Copyright © 2018 AuYong, Malekmohammadi, Ricks-Oddie 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
AuYong, Nicholas
Malekmohammadi, Mahsa
Ricks-Oddie, Joni
Pouratian, Nader
Movement-Modulation of Local Power and Phase Amplitude Coupling in Bilateral Globus Pallidus Interna in Parkinson Disease
title Movement-Modulation of Local Power and Phase Amplitude Coupling in Bilateral Globus Pallidus Interna in Parkinson Disease
title_full Movement-Modulation of Local Power and Phase Amplitude Coupling in Bilateral Globus Pallidus Interna in Parkinson Disease
title_fullStr Movement-Modulation of Local Power and Phase Amplitude Coupling in Bilateral Globus Pallidus Interna in Parkinson Disease
title_full_unstemmed Movement-Modulation of Local Power and Phase Amplitude Coupling in Bilateral Globus Pallidus Interna in Parkinson Disease
title_short Movement-Modulation of Local Power and Phase Amplitude Coupling in Bilateral Globus Pallidus Interna in Parkinson Disease
title_sort movement-modulation of local power and phase amplitude coupling in bilateral globus pallidus interna in parkinson disease
topic Neuroscience
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6046436/
https://www.ncbi.nlm.nih.gov/pubmed/30038563
http://dx.doi.org/10.3389/fnhum.2018.00270
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