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Periodic flashing coordinated reset stimulation paradigm reduces sensitivity to ON and OFF period durations

Pathological synchronization in the basal ganglia network has been considered an important component of Parkinson’s disease pathophysiology. An established treatment for some patients with Parkinson’s disease is deep brain stimulation, in which a tonic high-frequency pulse train is delivered to targ...

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Autores principales: Tyulmankov, Danil, Tass, Peter A., Bokil, Hemant
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Public Library of Science 2018
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6128645/
https://www.ncbi.nlm.nih.gov/pubmed/30192855
http://dx.doi.org/10.1371/journal.pone.0203782
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author Tyulmankov, Danil
Tass, Peter A.
Bokil, Hemant
author_facet Tyulmankov, Danil
Tass, Peter A.
Bokil, Hemant
author_sort Tyulmankov, Danil
collection PubMed
description Pathological synchronization in the basal ganglia network has been considered an important component of Parkinson’s disease pathophysiology. An established treatment for some patients with Parkinson’s disease is deep brain stimulation, in which a tonic high-frequency pulse train is delivered to target regions of the brain. In recent years, a novel neuromodulation paradigm called coordinated reset stimulation has been proposed, which aims to reverse the pathological synchrony by sequentially delivering short high-frequency bursts to distinct sub-regions of the pathologically synchronized network, with an average intra-burst interval for each sub-region corresponding to period of the pathological oscillation. It has further been proposed that the resultant desynchronization can be enhanced when stimulation is interrupted periodically, and that it is particularly beneficial to precisely tune the stimulation ON and OFF time-windows to the underlying pathological frequency. Pre-clinical and clinical studies of coordinated reset stimulation have relied on these proposals for their stimulation protocols. In this study, we present a modified ON-OFF coordinated reset stimulation paradigm called periodic flashing and study its behavior through computational modeling using the Kuramoto coupled phase oscillator model. We demonstrate that in contrast to conventional coordinated reset stimulation, the periodic flashing variation does not exhibit a need for precise turning of the ON-OFF periods to the pathological frequency, and demonstrates desynchronization for a wide range of ON and OFF periods. We provide a mechanistic explanation for the previously observed sensitivities and demonstrate that they are an artifact of the specific ON-OFF cycling paradigm used. As a practical consequence, the periodic flashing paradigm simplifies the tuning of optimal stimulation parameters by decreasing the dimension of the search space. It also suggests new, more flexible ways of delivering coordinated reset stimulation.
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spelling pubmed-61286452018-09-15 Periodic flashing coordinated reset stimulation paradigm reduces sensitivity to ON and OFF period durations Tyulmankov, Danil Tass, Peter A. Bokil, Hemant PLoS One Research Article Pathological synchronization in the basal ganglia network has been considered an important component of Parkinson’s disease pathophysiology. An established treatment for some patients with Parkinson’s disease is deep brain stimulation, in which a tonic high-frequency pulse train is delivered to target regions of the brain. In recent years, a novel neuromodulation paradigm called coordinated reset stimulation has been proposed, which aims to reverse the pathological synchrony by sequentially delivering short high-frequency bursts to distinct sub-regions of the pathologically synchronized network, with an average intra-burst interval for each sub-region corresponding to period of the pathological oscillation. It has further been proposed that the resultant desynchronization can be enhanced when stimulation is interrupted periodically, and that it is particularly beneficial to precisely tune the stimulation ON and OFF time-windows to the underlying pathological frequency. Pre-clinical and clinical studies of coordinated reset stimulation have relied on these proposals for their stimulation protocols. In this study, we present a modified ON-OFF coordinated reset stimulation paradigm called periodic flashing and study its behavior through computational modeling using the Kuramoto coupled phase oscillator model. We demonstrate that in contrast to conventional coordinated reset stimulation, the periodic flashing variation does not exhibit a need for precise turning of the ON-OFF periods to the pathological frequency, and demonstrates desynchronization for a wide range of ON and OFF periods. We provide a mechanistic explanation for the previously observed sensitivities and demonstrate that they are an artifact of the specific ON-OFF cycling paradigm used. As a practical consequence, the periodic flashing paradigm simplifies the tuning of optimal stimulation parameters by decreasing the dimension of the search space. It also suggests new, more flexible ways of delivering coordinated reset stimulation. Public Library of Science 2018-09-07 /pmc/articles/PMC6128645/ /pubmed/30192855 http://dx.doi.org/10.1371/journal.pone.0203782 Text en © 2018 Tyulmankov et al http://creativecommons.org/licenses/by/4.0/ This is an open access article distributed under the terms of the Creative Commons Attribution License (http://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
Tyulmankov, Danil
Tass, Peter A.
Bokil, Hemant
Periodic flashing coordinated reset stimulation paradigm reduces sensitivity to ON and OFF period durations
title Periodic flashing coordinated reset stimulation paradigm reduces sensitivity to ON and OFF period durations
title_full Periodic flashing coordinated reset stimulation paradigm reduces sensitivity to ON and OFF period durations
title_fullStr Periodic flashing coordinated reset stimulation paradigm reduces sensitivity to ON and OFF period durations
title_full_unstemmed Periodic flashing coordinated reset stimulation paradigm reduces sensitivity to ON and OFF period durations
title_short Periodic flashing coordinated reset stimulation paradigm reduces sensitivity to ON and OFF period durations
title_sort periodic flashing coordinated reset stimulation paradigm reduces sensitivity to on and off period durations
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6128645/
https://www.ncbi.nlm.nih.gov/pubmed/30192855
http://dx.doi.org/10.1371/journal.pone.0203782
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