Cargando…
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...
Autores principales: | , , , , , , |
---|---|
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 |
_version_ | 1784725856462045184 |
---|---|
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. |
format | Online Article Text |
id | pubmed-9190732 |
institution | National Center for Biotechnology Information |
language | English |
publishDate | 2022 |
publisher | American Physiological Society |
record_format | MEDLINE/PubMed |
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 |
work_keys_str_mv | AT gongruxue crossfrequencyphaseamplitudecouplinginrepetitivemovementsinpatientswithparkinsonsdisease AT muhlbergchristoph crossfrequencyphaseamplitudecouplinginrepetitivemovementsinpatientswithparkinsonsdisease AT wegscheidermirko crossfrequencyphaseamplitudecouplinginrepetitivemovementsinpatientswithparkinsonsdisease AT frickechristopher crossfrequencyphaseamplitudecouplinginrepetitivemovementsinpatientswithparkinsonsdisease AT rumpfjostjulian crossfrequencyphaseamplitudecouplinginrepetitivemovementsinpatientswithparkinsonsdisease AT knoschethomasr crossfrequencyphaseamplitudecouplinginrepetitivemovementsinpatientswithparkinsonsdisease AT classenjoseph crossfrequencyphaseamplitudecouplinginrepetitivemovementsinpatientswithparkinsonsdisease |