Subthalamic nucleus activity dynamics and limb movement prediction in Parkinson's disease.


Journal

Brain : a journal of neurology
ISSN: 1460-2156
Titre abrégé: Brain
Pays: England
ID NLM: 0372537

Informations de publication

Date de publication:
01 02 2020
Historique:
received: 19 08 2019
revised: 21 10 2019
accepted: 19 11 2019
entrez: 11 2 2020
pubmed: 11 2 2020
medline: 7 7 2020
Statut: ppublish

Résumé

Whilst exaggerated bursts of beta frequency band oscillatory synchronization in the subthalamic nucleus have been associated with motor impairment in Parkinson's disease, a plausible mechanism linking the two phenomena has been lacking. Here we test the hypothesis that increased synchronization denoted by beta bursting might compromise information coding capacity in basal ganglia networks. To this end we recorded local field potential activity in the subthalamic nucleus of 18 patients with Parkinson's disease as they executed cued upper and lower limb movements. We used the accuracy of local field potential-based classification of the limb to be moved on each trial as an index of the information held by the system with respect to intended action. Machine learning using the naïve Bayes conditional probability model was used for classification. Local field potential dynamics allowed accurate prediction of intended movements well ahead of their execution, with an area under the receiver operator characteristic curve of 0.80 ± 0.04 before imperative cues when the demanded action was known ahead of time. The presence of bursts of local field potential activity in the alpha, and even more so, in the beta frequency band significantly compromised the prediction of the limb to be moved. We conclude that low frequency bursts, particularly those in the beta band, restrict the capacity of the basal ganglia system to encode physiologically relevant information about intended actions. The current findings are also important as they suggest that local subthalamic activity may potentially be decoded to enable effector selection, in addition to force control in restorative brain-machine interface applications.

Identifiants

pubmed: 32040563
pii: 5732989
doi: 10.1093/brain/awz417
pmc: PMC7009471
doi:

Types de publication

Journal Article Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Pagination

582-596

Subventions

Organisme : Medical Research Council
ID : MR/K005464/1
Pays : United Kingdom
Organisme : Medical Research Council
ID : MC_UU_12024/1
Pays : United Kingdom
Organisme : Medical Research Council
ID : MC_UU_00003/2
Pays : United Kingdom
Organisme : Wellcome Trust
Pays : United Kingdom
Organisme : Medical Research Council
ID : MR/L023784/2
Pays : United Kingdom

Informations de copyright

© The Author(s) (2020). Published by Oxford University Press on behalf of the Guarantors of Brain.

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Auteurs

Saed Khawaldeh (S)

MRC Brain Network Dynamics Unit, University of Oxford, UK.
Nuffield Department of Clinical Neurosciences, University of Oxford, UK.
Oxford Centre for Human Brain Activity, Wellcome Centre for Integrative Neuroimaging, University of Oxford, UK.

Gerd Tinkhauser (G)

MRC Brain Network Dynamics Unit, University of Oxford, UK.
Nuffield Department of Clinical Neurosciences, University of Oxford, UK.
Department of Neurology, Bern University Hospital and University of Bern, Switzerland.

Syed Ahmar Shah (SA)

MRC Brain Network Dynamics Unit, University of Oxford, UK.
Nuffield Department of Clinical Neurosciences, University of Oxford, UK.
Usher Institute of Population Health Sciences and Informatics, Edinburgh Medical School, The University of Edinburgh, Edinburgh, UK.

Katrin Peterman (K)

Department of Neurology, Bern University Hospital and University of Bern, Switzerland.

Ines Debove (I)

Department of Neurology, Bern University Hospital and University of Bern, Switzerland.

T A Khoa Nguyen (TAK)

Department of Neurosurgery, Bern University Hospital and University of Bern, Switzerland.

Andreas Nowacki (A)

Department of Neurosurgery, Bern University Hospital and University of Bern, Switzerland.

M Lenard Lachenmayer (ML)

Department of Neurology, Bern University Hospital and University of Bern, Switzerland.

Michael Schuepbach (M)

Department of Neurology, Bern University Hospital and University of Bern, Switzerland.

Claudio Pollo (C)

Department of Neurosurgery, Bern University Hospital and University of Bern, Switzerland.

Paul Krack (P)

Department of Neurology, Bern University Hospital and University of Bern, Switzerland.

Mark Woolrich (M)

Nuffield Department of Clinical Neurosciences, University of Oxford, UK.
Oxford Centre for Human Brain Activity, Wellcome Centre for Integrative Neuroimaging, University of Oxford, UK.

Peter Brown (P)

MRC Brain Network Dynamics Unit, University of Oxford, UK.
Nuffield Department of Clinical Neurosciences, University of Oxford, UK.

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