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Beta-triggered adaptive deep brain stimulation during reaching movement in Parkinson’s disease

Subthalamic nucleus (STN) beta-triggered adaptive deep brain stimulation (ADBS) has been shown to provide clinical improvement comparable to conventional continuous DBS (CDBS) with less energy delivered to the brain and less stimulation induced side effects. However, several questions remain unanswe...

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Autores principales: He, Shenghong, Baig, Fahd, Merla, Anca, Torrecillos, Flavie, Perera, Andrea, Wiest, Christoph, Debarros, Jean, Benjaber, Moaad, Hart, Michael G, Ricciardi, Lucia, Morgante, Francesca, Hasegawa, Harutomo, Samuel, Michael, Edwards, Mark, Denison, Timothy, Pogosyan, Alek, Ashkan, Keyoumars, Pereira, Erlick, Tan, Huiling
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Oxford University Press 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10690014/
https://www.ncbi.nlm.nih.gov/pubmed/37433037
http://dx.doi.org/10.1093/brain/awad233
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author He, Shenghong
Baig, Fahd
Merla, Anca
Torrecillos, Flavie
Perera, Andrea
Wiest, Christoph
Debarros, Jean
Benjaber, Moaad
Hart, Michael G
Ricciardi, Lucia
Morgante, Francesca
Hasegawa, Harutomo
Samuel, Michael
Edwards, Mark
Denison, Timothy
Pogosyan, Alek
Ashkan, Keyoumars
Pereira, Erlick
Tan, Huiling
author_facet He, Shenghong
Baig, Fahd
Merla, Anca
Torrecillos, Flavie
Perera, Andrea
Wiest, Christoph
Debarros, Jean
Benjaber, Moaad
Hart, Michael G
Ricciardi, Lucia
Morgante, Francesca
Hasegawa, Harutomo
Samuel, Michael
Edwards, Mark
Denison, Timothy
Pogosyan, Alek
Ashkan, Keyoumars
Pereira, Erlick
Tan, Huiling
author_sort He, Shenghong
collection PubMed
description Subthalamic nucleus (STN) beta-triggered adaptive deep brain stimulation (ADBS) has been shown to provide clinical improvement comparable to conventional continuous DBS (CDBS) with less energy delivered to the brain and less stimulation induced side effects. However, several questions remain unanswered. First, there is a normal physiological reduction of STN beta band power just prior to and during voluntary movement. ADBS systems will therefore reduce or cease stimulation during movement in people with Parkinson’s disease and could therefore compromise motor performance compared to CDBS. Second, beta power was smoothed and estimated over a time period of 400 ms in most previous ADBS studies, but a shorter smoothing period could have the advantage of being more sensitive to changes in beta power, which could enhance motor performance. In this study, we addressed these two questions by evaluating the effectiveness of STN beta-triggered ADBS using a standard 400 ms and a shorter 200 ms smoothing window during reaching movements. Results from 13 people with Parkinson’s disease showed that reducing the smoothing window for quantifying beta did lead to shortened beta burst durations by increasing the number of beta bursts shorter than 200 ms and more frequent switching on/off of the stimulator but had no behavioural effects. Both ADBS and CDBS improved motor performance to an equivalent extent compared to no DBS. Secondary analysis revealed that there were independent effects of a decrease in beta power and an increase in gamma power in predicting faster movement speed, while a decrease in beta event related desynchronization (ERD) predicted quicker movement initiation. CDBS suppressed both beta and gamma more than ADBS, whereas beta ERD was reduced to a similar level during CDBS and ADBS compared with no DBS, which together explained the achieved similar performance improvement in reaching movements during CDBS and ADBS. In addition, ADBS significantly improved tremor compared with no DBS but was not as effective as CDBS. These results suggest that STN beta-triggered ADBS is effective in improving motor performance during reaching movements in people with Parkinson’s disease, and that shortening of the smoothing window does not result in any additional behavioural benefit. When developing ADBS systems for Parkinson’s disease, it might not be necessary to track very fast beta dynamics; combining beta, gamma, and information from motor decoding might be more beneficial with additional biomarkers needed for optimal treatment of tremor.
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spelling pubmed-106900142023-12-02 Beta-triggered adaptive deep brain stimulation during reaching movement in Parkinson’s disease He, Shenghong Baig, Fahd Merla, Anca Torrecillos, Flavie Perera, Andrea Wiest, Christoph Debarros, Jean Benjaber, Moaad Hart, Michael G Ricciardi, Lucia Morgante, Francesca Hasegawa, Harutomo Samuel, Michael Edwards, Mark Denison, Timothy Pogosyan, Alek Ashkan, Keyoumars Pereira, Erlick Tan, Huiling Brain Original Article Subthalamic nucleus (STN) beta-triggered adaptive deep brain stimulation (ADBS) has been shown to provide clinical improvement comparable to conventional continuous DBS (CDBS) with less energy delivered to the brain and less stimulation induced side effects. However, several questions remain unanswered. First, there is a normal physiological reduction of STN beta band power just prior to and during voluntary movement. ADBS systems will therefore reduce or cease stimulation during movement in people with Parkinson’s disease and could therefore compromise motor performance compared to CDBS. Second, beta power was smoothed and estimated over a time period of 400 ms in most previous ADBS studies, but a shorter smoothing period could have the advantage of being more sensitive to changes in beta power, which could enhance motor performance. In this study, we addressed these two questions by evaluating the effectiveness of STN beta-triggered ADBS using a standard 400 ms and a shorter 200 ms smoothing window during reaching movements. Results from 13 people with Parkinson’s disease showed that reducing the smoothing window for quantifying beta did lead to shortened beta burst durations by increasing the number of beta bursts shorter than 200 ms and more frequent switching on/off of the stimulator but had no behavioural effects. Both ADBS and CDBS improved motor performance to an equivalent extent compared to no DBS. Secondary analysis revealed that there were independent effects of a decrease in beta power and an increase in gamma power in predicting faster movement speed, while a decrease in beta event related desynchronization (ERD) predicted quicker movement initiation. CDBS suppressed both beta and gamma more than ADBS, whereas beta ERD was reduced to a similar level during CDBS and ADBS compared with no DBS, which together explained the achieved similar performance improvement in reaching movements during CDBS and ADBS. In addition, ADBS significantly improved tremor compared with no DBS but was not as effective as CDBS. These results suggest that STN beta-triggered ADBS is effective in improving motor performance during reaching movements in people with Parkinson’s disease, and that shortening of the smoothing window does not result in any additional behavioural benefit. When developing ADBS systems for Parkinson’s disease, it might not be necessary to track very fast beta dynamics; combining beta, gamma, and information from motor decoding might be more beneficial with additional biomarkers needed for optimal treatment of tremor. Oxford University Press 2023-07-11 /pmc/articles/PMC10690014/ /pubmed/37433037 http://dx.doi.org/10.1093/brain/awad233 Text en © The Author(s) 2023. Published by Oxford University Press on behalf of the Guarantors of Brain. 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 reuse, distribution, and reproduction in any medium, provided the original work is properly cited.
spellingShingle Original Article
He, Shenghong
Baig, Fahd
Merla, Anca
Torrecillos, Flavie
Perera, Andrea
Wiest, Christoph
Debarros, Jean
Benjaber, Moaad
Hart, Michael G
Ricciardi, Lucia
Morgante, Francesca
Hasegawa, Harutomo
Samuel, Michael
Edwards, Mark
Denison, Timothy
Pogosyan, Alek
Ashkan, Keyoumars
Pereira, Erlick
Tan, Huiling
Beta-triggered adaptive deep brain stimulation during reaching movement in Parkinson’s disease
title Beta-triggered adaptive deep brain stimulation during reaching movement in Parkinson’s disease
title_full Beta-triggered adaptive deep brain stimulation during reaching movement in Parkinson’s disease
title_fullStr Beta-triggered adaptive deep brain stimulation during reaching movement in Parkinson’s disease
title_full_unstemmed Beta-triggered adaptive deep brain stimulation during reaching movement in Parkinson’s disease
title_short Beta-triggered adaptive deep brain stimulation during reaching movement in Parkinson’s disease
title_sort beta-triggered adaptive deep brain stimulation during reaching movement in parkinson’s disease
topic Original Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10690014/
https://www.ncbi.nlm.nih.gov/pubmed/37433037
http://dx.doi.org/10.1093/brain/awad233
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