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Average beta burst duration profiles provide a signature of dynamical changes between the ON and OFF medication states in Parkinson’s disease

Parkinson’s disease motor symptoms are associated with an increase in subthalamic nucleus beta band oscillatory power. However, these oscillations are phasic, and there is a growing body of evidence suggesting that beta burst duration may be of critical importance to motor symptoms. This makes insig...

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Autores principales: Duchet, Benoit, Ghezzi, Filippo, Weerasinghe, Gihan, Tinkhauser, Gerd, Kühn, Andrea A., Brown, Peter, Bick, Christian, Bogacz, Rafal
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Public Library of Science 2021
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8263069/
https://www.ncbi.nlm.nih.gov/pubmed/34233347
http://dx.doi.org/10.1371/journal.pcbi.1009116
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author Duchet, Benoit
Ghezzi, Filippo
Weerasinghe, Gihan
Tinkhauser, Gerd
Kühn, Andrea A.
Brown, Peter
Bick, Christian
Bogacz, Rafal
author_facet Duchet, Benoit
Ghezzi, Filippo
Weerasinghe, Gihan
Tinkhauser, Gerd
Kühn, Andrea A.
Brown, Peter
Bick, Christian
Bogacz, Rafal
author_sort Duchet, Benoit
collection PubMed
description Parkinson’s disease motor symptoms are associated with an increase in subthalamic nucleus beta band oscillatory power. However, these oscillations are phasic, and there is a growing body of evidence suggesting that beta burst duration may be of critical importance to motor symptoms. This makes insights into the dynamics of beta bursting generation valuable, in particular to refine closed-loop deep brain stimulation in Parkinson’s disease. In this study, we ask the question “Can average burst duration reveal how dynamics change between the ON and OFF medication states?”. Our analysis of local field potentials from the subthalamic nucleus demonstrates using linear surrogates that the system generating beta oscillations is more likely to act in a non-linear regime OFF medication and that the change in a non-linearity measure is correlated with motor impairment. In addition, we pinpoint the simplest dynamical changes that could be responsible for changes in the temporal patterning of beta oscillations between medication states by fitting to data biologically inspired models, and simpler beta envelope models. Finally, we show that the non-linearity can be directly extracted from average burst duration profiles under the assumption of constant noise in envelope models. This reveals that average burst duration profiles provide a window into burst dynamics, which may underlie the success of burst duration as a biomarker. In summary, we demonstrate a relationship between average burst duration profiles, dynamics of the system generating beta oscillations, and motor impairment, which puts us in a better position to understand the pathology and improve therapies such as deep brain stimulation.
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spelling pubmed-82630692021-07-19 Average beta burst duration profiles provide a signature of dynamical changes between the ON and OFF medication states in Parkinson’s disease Duchet, Benoit Ghezzi, Filippo Weerasinghe, Gihan Tinkhauser, Gerd Kühn, Andrea A. Brown, Peter Bick, Christian Bogacz, Rafal PLoS Comput Biol Research Article Parkinson’s disease motor symptoms are associated with an increase in subthalamic nucleus beta band oscillatory power. However, these oscillations are phasic, and there is a growing body of evidence suggesting that beta burst duration may be of critical importance to motor symptoms. This makes insights into the dynamics of beta bursting generation valuable, in particular to refine closed-loop deep brain stimulation in Parkinson’s disease. In this study, we ask the question “Can average burst duration reveal how dynamics change between the ON and OFF medication states?”. Our analysis of local field potentials from the subthalamic nucleus demonstrates using linear surrogates that the system generating beta oscillations is more likely to act in a non-linear regime OFF medication and that the change in a non-linearity measure is correlated with motor impairment. In addition, we pinpoint the simplest dynamical changes that could be responsible for changes in the temporal patterning of beta oscillations between medication states by fitting to data biologically inspired models, and simpler beta envelope models. Finally, we show that the non-linearity can be directly extracted from average burst duration profiles under the assumption of constant noise in envelope models. This reveals that average burst duration profiles provide a window into burst dynamics, which may underlie the success of burst duration as a biomarker. In summary, we demonstrate a relationship between average burst duration profiles, dynamics of the system generating beta oscillations, and motor impairment, which puts us in a better position to understand the pathology and improve therapies such as deep brain stimulation. Public Library of Science 2021-07-07 /pmc/articles/PMC8263069/ /pubmed/34233347 http://dx.doi.org/10.1371/journal.pcbi.1009116 Text en © 2021 Duchet et al https://creativecommons.org/licenses/by/4.0/This is an open access article distributed under the terms of the Creative Commons Attribution License (https://creativecommons.org/licenses/by/4.0/) , which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
spellingShingle Research Article
Duchet, Benoit
Ghezzi, Filippo
Weerasinghe, Gihan
Tinkhauser, Gerd
Kühn, Andrea A.
Brown, Peter
Bick, Christian
Bogacz, Rafal
Average beta burst duration profiles provide a signature of dynamical changes between the ON and OFF medication states in Parkinson’s disease
title Average beta burst duration profiles provide a signature of dynamical changes between the ON and OFF medication states in Parkinson’s disease
title_full Average beta burst duration profiles provide a signature of dynamical changes between the ON and OFF medication states in Parkinson’s disease
title_fullStr Average beta burst duration profiles provide a signature of dynamical changes between the ON and OFF medication states in Parkinson’s disease
title_full_unstemmed Average beta burst duration profiles provide a signature of dynamical changes between the ON and OFF medication states in Parkinson’s disease
title_short Average beta burst duration profiles provide a signature of dynamical changes between the ON and OFF medication states in Parkinson’s disease
title_sort average beta burst duration profiles provide a signature of dynamical changes between the on and off medication states in parkinson’s disease
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8263069/
https://www.ncbi.nlm.nih.gov/pubmed/34233347
http://dx.doi.org/10.1371/journal.pcbi.1009116
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