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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Main Authors: Nicholas AuYong, Mahsa Malekmohammadi, Joni Ricks-Oddie, Nader Pouratian
Format: Article
Language:English
Published: Frontiers Media S.A. 2018-07-01
Series:Frontiers in Human Neuroscience
Subjects:
Online Access:https://www.frontiersin.org/article/10.3389/fnhum.2018.00270/full
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spelling doaj-fb64b3fed36f44e8ad58e8bbe2e4be022020-11-25T02:49:27ZengFrontiers Media S.A.Frontiers in Human Neuroscience1662-51612018-07-011210.3389/fnhum.2018.00270365499Movement-Modulation of Local Power and Phase Amplitude Coupling in Bilateral Globus Pallidus Interna in Parkinson DiseaseNicholas AuYong0Mahsa Malekmohammadi1Joni Ricks-Oddie2Nader Pouratian3Nader Pouratian4Nader Pouratian5Department of Neurosurgery, University of California, Los Angeles, Los Angeles, CA, United StatesDepartment of Neurosurgery, University of California, Los Angeles, Los Angeles, CA, United StatesInstitute for Digital Research and Education, University of California, Los Angeles, Los Angeles, CA, United StatesDepartment of Neurosurgery, University of California, Los Angeles, Los Angeles, CA, United StatesNeuroscience Interdepartmental Program, University of California, Los Angeles, Los Angeles, CA, United StatesBrain Research Institute, University of California, Los Angeles, Los Angeles, CA, United StatesThere 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.https://www.frontiersin.org/article/10.3389/fnhum.2018.00270/fullParkinson diseaseβ oscillationsphase amplitude couplinginterhemispheric coordinationglobus pallidus interna
collection DOAJ
language English
format Article
sources DOAJ
author Nicholas AuYong
Mahsa Malekmohammadi
Joni Ricks-Oddie
Nader Pouratian
Nader Pouratian
Nader Pouratian
spellingShingle Nicholas AuYong
Mahsa Malekmohammadi
Joni Ricks-Oddie
Nader Pouratian
Nader Pouratian
Nader Pouratian
Movement-Modulation of Local Power and Phase Amplitude Coupling in Bilateral Globus Pallidus Interna in Parkinson Disease
Frontiers in Human Neuroscience
Parkinson disease
β oscillations
phase amplitude coupling
interhemispheric coordination
globus pallidus interna
author_facet Nicholas AuYong
Mahsa Malekmohammadi
Joni Ricks-Oddie
Nader Pouratian
Nader Pouratian
Nader Pouratian
author_sort Nicholas AuYong
title 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_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_sort movement-modulation of local power and phase amplitude coupling in bilateral globus pallidus interna in parkinson disease
publisher Frontiers Media S.A.
series Frontiers in Human Neuroscience
issn 1662-5161
publishDate 2018-07-01
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.
topic Parkinson disease
β oscillations
phase amplitude coupling
interhemispheric coordination
globus pallidus interna
url https://www.frontiersin.org/article/10.3389/fnhum.2018.00270/full
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