Dopaminergic Modulation of Local Non-oscillatory Activity and Global-Network Properties in Parkinson’s Disease: An EEG Study

Dopaminergic medication for Parkinson’s disease (PD) modulates neuronal oscillations and functional connectivity (FC) across the basal ganglia-thalamic-cortical circuit. However, the non-oscillatory component of the neuronal activity, potentially indicating a state of excitation/inhibition balance,...

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Main Authors: Juanli Zhang, Arno Villringer, Vadim V. Nikulin
Format: Article
Language:English
Published: Frontiers Media S.A. 2022-04-01
Series:Frontiers in Aging Neuroscience
Subjects:
Online Access:https://www.frontiersin.org/articles/10.3389/fnagi.2022.846017/full
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author Juanli Zhang
Juanli Zhang
Arno Villringer
Arno Villringer
Vadim V. Nikulin
Vadim V. Nikulin
author_facet Juanli Zhang
Juanli Zhang
Arno Villringer
Arno Villringer
Vadim V. Nikulin
Vadim V. Nikulin
author_sort Juanli Zhang
collection DOAJ
description Dopaminergic medication for Parkinson’s disease (PD) modulates neuronal oscillations and functional connectivity (FC) across the basal ganglia-thalamic-cortical circuit. However, the non-oscillatory component of the neuronal activity, potentially indicating a state of excitation/inhibition balance, has not yet been investigated and previous studies have shown inconsistent changes of cortico-cortical connectivity as a response to dopaminergic medication. To further elucidate changes of regional non-oscillatory component of the neuronal power spectra, FC, and to determine which aspects of network organization obtained with graph theory respond to dopaminergic medication, we analyzed a resting-state electroencephalography (EEG) dataset including 15 PD patients during OFF and ON medication conditions. We found that the spectral slope, typically used to quantify the broadband non-oscillatory component of power spectra, steepened particularly in the left central region in the ON compared to OFF condition. In addition, using lagged coherence as a FC measure, we found that the FC in the beta frequency range between centro-parietal and frontal regions was enhanced in the ON compared to the OFF condition. After applying graph theory analysis, we observed that at the lower level of topology the node degree was increased, particularly in the centro-parietal area. Yet, results showed no significant difference in global topological organization between the two conditions: either in global efficiency or clustering coefficient for measuring global and local integration, respectively. Interestingly, we found a close association between local/global spectral slope and functional network global efficiency in the OFF condition, suggesting a crucial role of local non-oscillatory dynamics in forming the functional global integration which characterizes PD. These results provide further evidence and a more complete picture for the engagement of multiple cortical regions at various levels in response to dopaminergic medication in PD.
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spelling doaj.art-e31e00c53cfa42969b83faa267b2b5082022-12-22T02:56:07ZengFrontiers Media S.A.Frontiers in Aging Neuroscience1663-43652022-04-011410.3389/fnagi.2022.846017846017Dopaminergic Modulation of Local Non-oscillatory Activity and Global-Network Properties in Parkinson’s Disease: An EEG StudyJuanli Zhang0Juanli Zhang1Arno Villringer2Arno Villringer3Vadim V. Nikulin4Vadim V. Nikulin5Department of Neurology, Max Planck Institute for Human Cognitive and Brain Sciences, Leipzig, GermanyDepartment of Neurology, Charité – Universitätsmedizin Berlin, Berlin, GermanyDepartment of Neurology, Max Planck Institute for Human Cognitive and Brain Sciences, Leipzig, GermanyDepartment of Cognitive Neurology, University Hospital Leipzig, Leipzig, GermanyDepartment of Neurology, Max Planck Institute for Human Cognitive and Brain Sciences, Leipzig, GermanyNeurophysics Group, Department of Neurology, Charité – Universitätsmedizin Berlin, Berlin, GermanyDopaminergic medication for Parkinson’s disease (PD) modulates neuronal oscillations and functional connectivity (FC) across the basal ganglia-thalamic-cortical circuit. However, the non-oscillatory component of the neuronal activity, potentially indicating a state of excitation/inhibition balance, has not yet been investigated and previous studies have shown inconsistent changes of cortico-cortical connectivity as a response to dopaminergic medication. To further elucidate changes of regional non-oscillatory component of the neuronal power spectra, FC, and to determine which aspects of network organization obtained with graph theory respond to dopaminergic medication, we analyzed a resting-state electroencephalography (EEG) dataset including 15 PD patients during OFF and ON medication conditions. We found that the spectral slope, typically used to quantify the broadband non-oscillatory component of power spectra, steepened particularly in the left central region in the ON compared to OFF condition. In addition, using lagged coherence as a FC measure, we found that the FC in the beta frequency range between centro-parietal and frontal regions was enhanced in the ON compared to the OFF condition. After applying graph theory analysis, we observed that at the lower level of topology the node degree was increased, particularly in the centro-parietal area. Yet, results showed no significant difference in global topological organization between the two conditions: either in global efficiency or clustering coefficient for measuring global and local integration, respectively. Interestingly, we found a close association between local/global spectral slope and functional network global efficiency in the OFF condition, suggesting a crucial role of local non-oscillatory dynamics in forming the functional global integration which characterizes PD. These results provide further evidence and a more complete picture for the engagement of multiple cortical regions at various levels in response to dopaminergic medication in PD.https://www.frontiersin.org/articles/10.3389/fnagi.2022.846017/fullParkinson’s diseasedopaminergic medicationspectral slopefunctional connectivitygraph theory
spellingShingle Juanli Zhang
Juanli Zhang
Arno Villringer
Arno Villringer
Vadim V. Nikulin
Vadim V. Nikulin
Dopaminergic Modulation of Local Non-oscillatory Activity and Global-Network Properties in Parkinson’s Disease: An EEG Study
Frontiers in Aging Neuroscience
Parkinson’s disease
dopaminergic medication
spectral slope
functional connectivity
graph theory
title Dopaminergic Modulation of Local Non-oscillatory Activity and Global-Network Properties in Parkinson’s Disease: An EEG Study
title_full Dopaminergic Modulation of Local Non-oscillatory Activity and Global-Network Properties in Parkinson’s Disease: An EEG Study
title_fullStr Dopaminergic Modulation of Local Non-oscillatory Activity and Global-Network Properties in Parkinson’s Disease: An EEG Study
title_full_unstemmed Dopaminergic Modulation of Local Non-oscillatory Activity and Global-Network Properties in Parkinson’s Disease: An EEG Study
title_short Dopaminergic Modulation of Local Non-oscillatory Activity and Global-Network Properties in Parkinson’s Disease: An EEG Study
title_sort dopaminergic modulation of local non oscillatory activity and global network properties in parkinson s disease an eeg study
topic Parkinson’s disease
dopaminergic medication
spectral slope
functional connectivity
graph theory
url https://www.frontiersin.org/articles/10.3389/fnagi.2022.846017/full
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