Neuronal biomarkers of Parkinson's disease are present in healthy aging

The prevalence of Parkinson's disease (PD) increases with aging and both processes share similar cellular mechanisms and alterations in the dopaminergic system. Yet it remains to be investigated whether aging can also demonstrate electrophysiological neuronal signatures typically associated wit...

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Main Authors: Juanli Zhang, Mina Jamshidi Idaji, Arno Villringer, Vadim V. Nikulin
Format: Article
Language:English
Published: Elsevier 2021-11-01
Series:NeuroImage
Subjects:
Online Access:http://www.sciencedirect.com/science/article/pii/S1053811921007850
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author Juanli Zhang
Mina Jamshidi Idaji
Arno Villringer
Vadim V. Nikulin
author_facet Juanli Zhang
Mina Jamshidi Idaji
Arno Villringer
Vadim V. Nikulin
author_sort Juanli Zhang
collection DOAJ
description The prevalence of Parkinson's disease (PD) increases with aging and both processes share similar cellular mechanisms and alterations in the dopaminergic system. Yet it remains to be investigated whether aging can also demonstrate electrophysiological neuronal signatures typically associated with PD. Previous work has shown that phase-amplitude coupling (PAC) between the phase of beta oscillations and the amplitude of gamma oscillations as well as beta bursts features can serve as electrophysiological biomarkers for PD. Here we hypothesize that these metrics are also present in apparently healthy elderly subjects. Using resting state multichannel EEG measurements, we show that PAC between beta oscillation and broadband gamma activity (50–150 Hz) is elevated in a group of elderly (59–77 years) compared to young volunteers (20–35 years) without PD. Importantly, the increase of PAC is statistically significant even after ruling out confounds relating to changes in spectral power and non-sinusoidal shape of beta oscillation. Moreover, a trend for a higher percentage of longer beta bursts (> 0.2 s) along with the increase in their incidence rate is also observed for elderly subjects. Using inverse modeling, we further show that elevated PAC and longer beta bursts are most pronounced in the sensorimotor areas. Moreover, we show that PAC and longer beta bursts might reflect distinct mechanisms, since their spatial patterns only partially overlap and the correlation between them is weak. Taken together, our findings provide novel evidence that electrophysiological biomarkers of PD may already occur in apparently healthy elderly subjects. We hypothesize that PAC and beta bursts characteristics in aging might reflect a pre-clinical state of PD and suggest their predictive value to be tested in prospective longitudinal studies.
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spelling doaj.art-293ab344b42347488e19334f8a753cad2022-12-21T19:16:57ZengElsevierNeuroImage1095-95722021-11-01243118512Neuronal biomarkers of Parkinson's disease are present in healthy agingJuanli Zhang0Mina Jamshidi Idaji1Arno Villringer2Vadim V. Nikulin3Department of Neurology, Max Planck Institute for Human Cognitive and Brain Sciences, Leipzig, Germany; Department of Neurology, Charité – Universitätsmedizin Berlin, Berlin, Germany; Corresponding authors.Department of Neurology, Max Planck Institute for Human Cognitive and Brain Sciences, Leipzig, Germany; Machine Learning Group, Technical University of Berlin, Berlin, Germany; International Max Planck Research School NeuroCom, Leipzig, GermanyDepartment of Neurology, Max Planck Institute for Human Cognitive and Brain Sciences, Leipzig, Germany; Department of Cognitive Neurology, University Hospital Leipzig, Leipzig, GermanyDepartment of Neurology, Max Planck Institute for Human Cognitive and Brain Sciences, Leipzig, Germany; Centre for Cognition and Decision Making, Institute for Cognitive Neuroscience, National Research University Higher School of Economics, Moscow, Russian Federation; Neurophysics Group, Department of Neurology, Charité – Universitätsmedizin Berlin, Berlin, Germany; Corresponding authors.The prevalence of Parkinson's disease (PD) increases with aging and both processes share similar cellular mechanisms and alterations in the dopaminergic system. Yet it remains to be investigated whether aging can also demonstrate electrophysiological neuronal signatures typically associated with PD. Previous work has shown that phase-amplitude coupling (PAC) between the phase of beta oscillations and the amplitude of gamma oscillations as well as beta bursts features can serve as electrophysiological biomarkers for PD. Here we hypothesize that these metrics are also present in apparently healthy elderly subjects. Using resting state multichannel EEG measurements, we show that PAC between beta oscillation and broadband gamma activity (50–150 Hz) is elevated in a group of elderly (59–77 years) compared to young volunteers (20–35 years) without PD. Importantly, the increase of PAC is statistically significant even after ruling out confounds relating to changes in spectral power and non-sinusoidal shape of beta oscillation. Moreover, a trend for a higher percentage of longer beta bursts (> 0.2 s) along with the increase in their incidence rate is also observed for elderly subjects. Using inverse modeling, we further show that elevated PAC and longer beta bursts are most pronounced in the sensorimotor areas. Moreover, we show that PAC and longer beta bursts might reflect distinct mechanisms, since their spatial patterns only partially overlap and the correlation between them is weak. Taken together, our findings provide novel evidence that electrophysiological biomarkers of PD may already occur in apparently healthy elderly subjects. We hypothesize that PAC and beta bursts characteristics in aging might reflect a pre-clinical state of PD and suggest their predictive value to be tested in prospective longitudinal studies.http://www.sciencedirect.com/science/article/pii/S1053811921007850Resting state EEGHealthy agingParkinson's diseasePACBeta burst
spellingShingle Juanli Zhang
Mina Jamshidi Idaji
Arno Villringer
Vadim V. Nikulin
Neuronal biomarkers of Parkinson's disease are present in healthy aging
NeuroImage
Resting state EEG
Healthy aging
Parkinson's disease
PAC
Beta burst
title Neuronal biomarkers of Parkinson's disease are present in healthy aging
title_full Neuronal biomarkers of Parkinson's disease are present in healthy aging
title_fullStr Neuronal biomarkers of Parkinson's disease are present in healthy aging
title_full_unstemmed Neuronal biomarkers of Parkinson's disease are present in healthy aging
title_short Neuronal biomarkers of Parkinson's disease are present in healthy aging
title_sort neuronal biomarkers of parkinson s disease are present in healthy aging
topic Resting state EEG
Healthy aging
Parkinson's disease
PAC
Beta burst
url http://www.sciencedirect.com/science/article/pii/S1053811921007850
work_keys_str_mv AT juanlizhang neuronalbiomarkersofparkinsonsdiseasearepresentinhealthyaging
AT minajamshidiidaji neuronalbiomarkersofparkinsonsdiseasearepresentinhealthyaging
AT arnovillringer neuronalbiomarkersofparkinsonsdiseasearepresentinhealthyaging
AT vadimvnikulin neuronalbiomarkersofparkinsonsdiseasearepresentinhealthyaging