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Cross-frequency phase-amplitude coupling in repetitive movements in patients with Parkinson’s disease

Bradykinesia is a cardinal motor symptom in Parkinson’s disease (PD), the pathophysiology of which is not fully understood. We analyzed the role of cross-frequency coupling of oscillatory cortical activity in motor impairment in patients with PD and healthy controls. High-density EEG signals were re...

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Autores principales: Gong, Ruxue, Mühlberg, Christoph, Wegscheider, Mirko, Fricke, Christopher, Rumpf, Jost-Julian, Knösche, Thomas R., Classen, Joseph
Formato: Online Artículo Texto
Lenguaje:English
Publicado: American Physiological Society 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9190732/
https://www.ncbi.nlm.nih.gov/pubmed/35544757
http://dx.doi.org/10.1152/jn.00541.2021
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author Gong, Ruxue
Mühlberg, Christoph
Wegscheider, Mirko
Fricke, Christopher
Rumpf, Jost-Julian
Knösche, Thomas R.
Classen, Joseph
author_facet Gong, Ruxue
Mühlberg, Christoph
Wegscheider, Mirko
Fricke, Christopher
Rumpf, Jost-Julian
Knösche, Thomas R.
Classen, Joseph
author_sort Gong, Ruxue
collection PubMed
description Bradykinesia is a cardinal motor symptom in Parkinson’s disease (PD), the pathophysiology of which is not fully understood. We analyzed the role of cross-frequency coupling of oscillatory cortical activity in motor impairment in patients with PD and healthy controls. High-density EEG signals were recorded during various motor activities and at rest. Patients performed a repetitive finger-pressing task normally, but were slower than controls during tapping. Phase-amplitude coupling (PAC) between β (13–30 Hz) and broadband γ (50–150 Hz) was computed from individual EEG source signals in the premotor, primary motor, and primary somatosensory cortices, and the primary somatosensory complex. In all four regions, averaging the entire movement period resulted in higher PAC in patients than in controls for the resting condition and the pressing task (similar performance between groups). However, this was not the case for the tapping tasks where patients performed slower. This suggests the strength of state-related β-γ PAC does not determine Parkinsonian bradykinesia. Examination of the dynamics of oscillatory EEG signals during motor transitions revealed a distinctive motif of PAC rise and decay around press onset. This pattern was also present at press offset and slow tapping onset, linking such idiosyncratic PAC changes to transitions between different movement states. The transition-related PAC modulation in patients was similar to controls in the pressing task but flattened during slow tapping, which related to normal and abnormal performance, respectively. These findings suggest that the dysfunctional evolution of neuronal population dynamics during movement execution is an important component of the pathophysiology of Parkinsonian bradykinesia. NEW & NOTEWORTHY Our findings using noninvasive EEG recordings provide evidence that PAC dynamics might play a role in the physiological cortical control of movement execution and may encode transitions between movement states. Results in patients with Parkinson’s disease suggest that bradykinesia is related to a deficit of the dynamic regulation of PAC during movement execution rather than its absolute strength. Our findings may contribute to the development of a new concept of the pathophysiology of bradykinesia.
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spelling pubmed-91907322022-07-06 Cross-frequency phase-amplitude coupling in repetitive movements in patients with Parkinson’s disease Gong, Ruxue Mühlberg, Christoph Wegscheider, Mirko Fricke, Christopher Rumpf, Jost-Julian Knösche, Thomas R. Classen, Joseph J Neurophysiol Research Article Bradykinesia is a cardinal motor symptom in Parkinson’s disease (PD), the pathophysiology of which is not fully understood. We analyzed the role of cross-frequency coupling of oscillatory cortical activity in motor impairment in patients with PD and healthy controls. High-density EEG signals were recorded during various motor activities and at rest. Patients performed a repetitive finger-pressing task normally, but were slower than controls during tapping. Phase-amplitude coupling (PAC) between β (13–30 Hz) and broadband γ (50–150 Hz) was computed from individual EEG source signals in the premotor, primary motor, and primary somatosensory cortices, and the primary somatosensory complex. In all four regions, averaging the entire movement period resulted in higher PAC in patients than in controls for the resting condition and the pressing task (similar performance between groups). However, this was not the case for the tapping tasks where patients performed slower. This suggests the strength of state-related β-γ PAC does not determine Parkinsonian bradykinesia. Examination of the dynamics of oscillatory EEG signals during motor transitions revealed a distinctive motif of PAC rise and decay around press onset. This pattern was also present at press offset and slow tapping onset, linking such idiosyncratic PAC changes to transitions between different movement states. The transition-related PAC modulation in patients was similar to controls in the pressing task but flattened during slow tapping, which related to normal and abnormal performance, respectively. These findings suggest that the dysfunctional evolution of neuronal population dynamics during movement execution is an important component of the pathophysiology of Parkinsonian bradykinesia. NEW & NOTEWORTHY Our findings using noninvasive EEG recordings provide evidence that PAC dynamics might play a role in the physiological cortical control of movement execution and may encode transitions between movement states. Results in patients with Parkinson’s disease suggest that bradykinesia is related to a deficit of the dynamic regulation of PAC during movement execution rather than its absolute strength. Our findings may contribute to the development of a new concept of the pathophysiology of bradykinesia. American Physiological Society 2022-06-01 2022-05-11 /pmc/articles/PMC9190732/ /pubmed/35544757 http://dx.doi.org/10.1152/jn.00541.2021 Text en Copyright © 2022 The Authors https://creativecommons.org/licenses/by/4.0/Licensed under Creative Commons Attribution CC-BY 4.0 (https://creativecommons.org/licenses/by/4.0/) . Published by the American Physiological Society.
spellingShingle Research Article
Gong, Ruxue
Mühlberg, Christoph
Wegscheider, Mirko
Fricke, Christopher
Rumpf, Jost-Julian
Knösche, Thomas R.
Classen, Joseph
Cross-frequency phase-amplitude coupling in repetitive movements in patients with Parkinson’s disease
title Cross-frequency phase-amplitude coupling in repetitive movements in patients with Parkinson’s disease
title_full Cross-frequency phase-amplitude coupling in repetitive movements in patients with Parkinson’s disease
title_fullStr Cross-frequency phase-amplitude coupling in repetitive movements in patients with Parkinson’s disease
title_full_unstemmed Cross-frequency phase-amplitude coupling in repetitive movements in patients with Parkinson’s disease
title_short Cross-frequency phase-amplitude coupling in repetitive movements in patients with Parkinson’s disease
title_sort cross-frequency phase-amplitude coupling in repetitive movements in patients with parkinson’s disease
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9190732/
https://www.ncbi.nlm.nih.gov/pubmed/35544757
http://dx.doi.org/10.1152/jn.00541.2021
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