Subthalamic beta-targeted neurofeedback speeds up movement initiation but increases tremor in Parkinsonian patients

Previous studies have explored neurofeedback training for Parkinsonian patients to suppress beta oscillations in the subthalamic nucleus (STN). However, its impacts on movements and Parkinsonian tremor are unclear. We developed a neurofeedback paradigm targeting STN beta bursts and investigated whet...

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Main Authors: Shenghong He, Abteen Mostofi, Emilie Syed, Flavie Torrecillos, Gerd Tinkhauser, Petra Fischer, Alek Pogosyan, Harutomo Hasegawa, Yuanqing Li, Keyoumars Ashkan, Erlick Pereira, Peter Brown, Huiling Tan
Format: Article
Language:English
Published: eLife Sciences Publications Ltd 2020-11-01
Series:eLife
Subjects:
Online Access:https://elifesciences.org/articles/60979
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author Shenghong He
Abteen Mostofi
Emilie Syed
Flavie Torrecillos
Gerd Tinkhauser
Petra Fischer
Alek Pogosyan
Harutomo Hasegawa
Yuanqing Li
Keyoumars Ashkan
Erlick Pereira
Peter Brown
Huiling Tan
author_facet Shenghong He
Abteen Mostofi
Emilie Syed
Flavie Torrecillos
Gerd Tinkhauser
Petra Fischer
Alek Pogosyan
Harutomo Hasegawa
Yuanqing Li
Keyoumars Ashkan
Erlick Pereira
Peter Brown
Huiling Tan
author_sort Shenghong He
collection DOAJ
description Previous studies have explored neurofeedback training for Parkinsonian patients to suppress beta oscillations in the subthalamic nucleus (STN). However, its impacts on movements and Parkinsonian tremor are unclear. We developed a neurofeedback paradigm targeting STN beta bursts and investigated whether neurofeedback training could improve motor initiation in Parkinson’s disease compared to passive observation. Our task additionally allowed us to test which endogenous changes in oscillatory STN activities are associated with trial-to-trial motor performance. Neurofeedback training reduced beta synchrony and increased gamma activity within the STN, and reduced beta band coupling between the STN and motor cortex. These changes were accompanied by reduced reaction times in subsequently cued movements. However, in Parkinsonian patients with pre-existing symptoms of tremor, successful volitional beta suppression was associated with an amplification of tremor which correlated with theta band activity in STN local field potentials, suggesting an additional cross-frequency interaction between STN beta and theta activities.
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spelling doaj.art-03fe1beb28b24276bf5406c6b80220042022-12-22T04:32:29ZengeLife Sciences Publications LtdeLife2050-084X2020-11-01910.7554/eLife.60979Subthalamic beta-targeted neurofeedback speeds up movement initiation but increases tremor in Parkinsonian patientsShenghong He0https://orcid.org/0000-0002-5269-1902Abteen Mostofi1Emilie Syed2Flavie Torrecillos3Gerd Tinkhauser4Petra Fischer5https://orcid.org/0000-0001-5585-8977Alek Pogosyan6Harutomo Hasegawa7Yuanqing Li8Keyoumars Ashkan9Erlick Pereira10Peter Brown11https://orcid.org/0000-0002-5201-3044Huiling Tan12https://orcid.org/0000-0001-8038-3029MRC Brain Network Dynamics Unit at the University of Oxford, Oxford, United Kingdom; Nuffield Department of Clinical Neurosciences, University of Oxford, Oxford, United KingdomNeurosciences Research Centre, Molecular and Clinical Sciences Research Institute, St George’s University of London, London, United KingdomMRC Brain Network Dynamics Unit at the University of Oxford, Oxford, United KingdomMRC Brain Network Dynamics Unit at the University of Oxford, Oxford, United Kingdom; Nuffield Department of Clinical Neurosciences, University of Oxford, Oxford, United KingdomMRC Brain Network Dynamics Unit at the University of Oxford, Oxford, United Kingdom; Department of Neurology, Bern University Hospital and University of Bern, Bern, SwitzerlandMRC Brain Network Dynamics Unit at the University of Oxford, Oxford, United Kingdom; Nuffield Department of Clinical Neurosciences, University of Oxford, Oxford, United KingdomMRC Brain Network Dynamics Unit at the University of Oxford, Oxford, United Kingdom; Nuffield Department of Clinical Neurosciences, University of Oxford, Oxford, United KingdomDepartment of Neurosurgery, King's College Hospital NHS Foundation Trust, King's Health Partners, London, United KingdomSchool of Automation Science and Engineering, South China University of Technology, Guangzhou, ChinaDepartment of Neurosurgery, King's College Hospital NHS Foundation Trust, King's Health Partners, London, United KingdomNeurosciences Research Centre, Molecular and Clinical Sciences Research Institute, St George’s University of London, London, United KingdomMRC Brain Network Dynamics Unit at the University of Oxford, Oxford, United Kingdom; Nuffield Department of Clinical Neurosciences, University of Oxford, Oxford, United KingdomMRC Brain Network Dynamics Unit at the University of Oxford, Oxford, United Kingdom; Nuffield Department of Clinical Neurosciences, University of Oxford, Oxford, United KingdomPrevious studies have explored neurofeedback training for Parkinsonian patients to suppress beta oscillations in the subthalamic nucleus (STN). However, its impacts on movements and Parkinsonian tremor are unclear. We developed a neurofeedback paradigm targeting STN beta bursts and investigated whether neurofeedback training could improve motor initiation in Parkinson’s disease compared to passive observation. Our task additionally allowed us to test which endogenous changes in oscillatory STN activities are associated with trial-to-trial motor performance. Neurofeedback training reduced beta synchrony and increased gamma activity within the STN, and reduced beta band coupling between the STN and motor cortex. These changes were accompanied by reduced reaction times in subsequently cued movements. However, in Parkinsonian patients with pre-existing symptoms of tremor, successful volitional beta suppression was associated with an amplification of tremor which correlated with theta band activity in STN local field potentials, suggesting an additional cross-frequency interaction between STN beta and theta activities.https://elifesciences.org/articles/60979beta oscillationsneurofeedbackbeta burstparkinson's diseaseparkinsonian tremor
spellingShingle Shenghong He
Abteen Mostofi
Emilie Syed
Flavie Torrecillos
Gerd Tinkhauser
Petra Fischer
Alek Pogosyan
Harutomo Hasegawa
Yuanqing Li
Keyoumars Ashkan
Erlick Pereira
Peter Brown
Huiling Tan
Subthalamic beta-targeted neurofeedback speeds up movement initiation but increases tremor in Parkinsonian patients
eLife
beta oscillations
neurofeedback
beta burst
parkinson's disease
parkinsonian tremor
title Subthalamic beta-targeted neurofeedback speeds up movement initiation but increases tremor in Parkinsonian patients
title_full Subthalamic beta-targeted neurofeedback speeds up movement initiation but increases tremor in Parkinsonian patients
title_fullStr Subthalamic beta-targeted neurofeedback speeds up movement initiation but increases tremor in Parkinsonian patients
title_full_unstemmed Subthalamic beta-targeted neurofeedback speeds up movement initiation but increases tremor in Parkinsonian patients
title_short Subthalamic beta-targeted neurofeedback speeds up movement initiation but increases tremor in Parkinsonian patients
title_sort subthalamic beta targeted neurofeedback speeds up movement initiation but increases tremor in parkinsonian patients
topic beta oscillations
neurofeedback
beta burst
parkinson's disease
parkinsonian tremor
url https://elifesciences.org/articles/60979
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