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Electrocorticography is superior to subthalamic local field potentials for movement decoding in Parkinson’s disease

Brain signal decoding promises significant advances in the development of clinical brain computer interfaces (BCI). In Parkinson’s disease (PD), first bidirectional BCI implants for adaptive deep brain stimulation (DBS) are now available. Brain signal decoding can extend the clinical utility of adap...

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Autores principales: Merk, Timon, Peterson, Victoria, Lipski, Witold J, Blankertz, Benjamin, Turner, Robert S, Li, Ningfei, Horn, Andreas, Richardson, Robert Mark, Neumann, Wolf-Julian
Formato: Online Artículo Texto
Lenguaje:English
Publicado: eLife Sciences Publications, Ltd 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9142148/
https://www.ncbi.nlm.nih.gov/pubmed/35621994
http://dx.doi.org/10.7554/eLife.75126
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author Merk, Timon
Peterson, Victoria
Lipski, Witold J
Blankertz, Benjamin
Turner, Robert S
Li, Ningfei
Horn, Andreas
Richardson, Robert Mark
Neumann, Wolf-Julian
author_facet Merk, Timon
Peterson, Victoria
Lipski, Witold J
Blankertz, Benjamin
Turner, Robert S
Li, Ningfei
Horn, Andreas
Richardson, Robert Mark
Neumann, Wolf-Julian
author_sort Merk, Timon
collection PubMed
description Brain signal decoding promises significant advances in the development of clinical brain computer interfaces (BCI). In Parkinson’s disease (PD), first bidirectional BCI implants for adaptive deep brain stimulation (DBS) are now available. Brain signal decoding can extend the clinical utility of adaptive DBS but the impact of neural source, computational methods and PD pathophysiology on decoding performance are unknown. This represents an unmet need for the development of future neurotechnology. To address this, we developed an invasive brain-signal decoding approach based on intraoperative sensorimotor electrocorticography (ECoG) and subthalamic LFP to predict grip-force, a representative movement decoding application, in 11 PD patients undergoing DBS. We demonstrate that ECoG is superior to subthalamic LFP for accurate grip-force decoding. Gradient boosted decision trees (XGBOOST) outperformed other model architectures. ECoG based decoding performance negatively correlated with motor impairment, which could be attributed to subthalamic beta bursts in the motor preparation and movement period. This highlights the impact of PD pathophysiology on the neural capacity to encode movement vigor. Finally, we developed a connectomic analysis that could predict grip-force decoding performance of individual ECoG channels across patients by using their connectomic fingerprints. Our study provides a neurophysiological and computational framework for invasive brain signal decoding to aid the development of an individualized precision-medicine approach to intelligent adaptive DBS.
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spelling pubmed-91421482022-05-28 Electrocorticography is superior to subthalamic local field potentials for movement decoding in Parkinson’s disease Merk, Timon Peterson, Victoria Lipski, Witold J Blankertz, Benjamin Turner, Robert S Li, Ningfei Horn, Andreas Richardson, Robert Mark Neumann, Wolf-Julian eLife Computational and Systems Biology Brain signal decoding promises significant advances in the development of clinical brain computer interfaces (BCI). In Parkinson’s disease (PD), first bidirectional BCI implants for adaptive deep brain stimulation (DBS) are now available. Brain signal decoding can extend the clinical utility of adaptive DBS but the impact of neural source, computational methods and PD pathophysiology on decoding performance are unknown. This represents an unmet need for the development of future neurotechnology. To address this, we developed an invasive brain-signal decoding approach based on intraoperative sensorimotor electrocorticography (ECoG) and subthalamic LFP to predict grip-force, a representative movement decoding application, in 11 PD patients undergoing DBS. We demonstrate that ECoG is superior to subthalamic LFP for accurate grip-force decoding. Gradient boosted decision trees (XGBOOST) outperformed other model architectures. ECoG based decoding performance negatively correlated with motor impairment, which could be attributed to subthalamic beta bursts in the motor preparation and movement period. This highlights the impact of PD pathophysiology on the neural capacity to encode movement vigor. Finally, we developed a connectomic analysis that could predict grip-force decoding performance of individual ECoG channels across patients by using their connectomic fingerprints. Our study provides a neurophysiological and computational framework for invasive brain signal decoding to aid the development of an individualized precision-medicine approach to intelligent adaptive DBS. eLife Sciences Publications, Ltd 2022-05-27 /pmc/articles/PMC9142148/ /pubmed/35621994 http://dx.doi.org/10.7554/eLife.75126 Text en © 2022, Merk et al https://creativecommons.org/licenses/by/4.0/This article is distributed under the terms of the Creative Commons Attribution License (https://creativecommons.org/licenses/by/4.0/) , which permits unrestricted use and redistribution provided that the original author and source are credited.
spellingShingle Computational and Systems Biology
Merk, Timon
Peterson, Victoria
Lipski, Witold J
Blankertz, Benjamin
Turner, Robert S
Li, Ningfei
Horn, Andreas
Richardson, Robert Mark
Neumann, Wolf-Julian
Electrocorticography is superior to subthalamic local field potentials for movement decoding in Parkinson’s disease
title Electrocorticography is superior to subthalamic local field potentials for movement decoding in Parkinson’s disease
title_full Electrocorticography is superior to subthalamic local field potentials for movement decoding in Parkinson’s disease
title_fullStr Electrocorticography is superior to subthalamic local field potentials for movement decoding in Parkinson’s disease
title_full_unstemmed Electrocorticography is superior to subthalamic local field potentials for movement decoding in Parkinson’s disease
title_short Electrocorticography is superior to subthalamic local field potentials for movement decoding in Parkinson’s disease
title_sort electrocorticography is superior to subthalamic local field potentials for movement decoding in parkinson’s disease
topic Computational and Systems Biology
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9142148/
https://www.ncbi.nlm.nih.gov/pubmed/35621994
http://dx.doi.org/10.7554/eLife.75126
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