Movement-related coupling of human subthalamic nucleus spikes to cortical gamma

Cortico-basal ganglia interactions continuously shape the way we move. Ideas about how this circuit works are based largely on models those consider only firing rate as the mechanism of information transfer. A distinct feature of neural activity accompanying movement, however, is increased motor cor...

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Main Authors: Petra Fischer, Witold J Lipski, Wolf-Julian Neumann, Robert S Turner, Pascal Fries, Peter Brown, R Mark Richardson
Format: Article
Language:English
Published: eLife Sciences Publications Ltd 2020-03-01
Series:eLife
Subjects:
Online Access:https://elifesciences.org/articles/51956
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author Petra Fischer
Witold J Lipski
Wolf-Julian Neumann
Robert S Turner
Pascal Fries
Peter Brown
R Mark Richardson
author_facet Petra Fischer
Witold J Lipski
Wolf-Julian Neumann
Robert S Turner
Pascal Fries
Peter Brown
R Mark Richardson
author_sort Petra Fischer
collection DOAJ
description Cortico-basal ganglia interactions continuously shape the way we move. Ideas about how this circuit works are based largely on models those consider only firing rate as the mechanism of information transfer. A distinct feature of neural activity accompanying movement, however, is increased motor cortical and basal ganglia gamma synchrony. To investigate the relationship between neuronal firing in the basal ganglia and cortical gamma activity during movement, we analysed human ECoG and subthalamic nucleus (STN) unit activity during hand gripping. We found that fast reaction times were preceded by enhanced STN spike-to-cortical gamma phase coupling, indicating a role in motor preparation. Importantly, increased gamma phase coupling occurred independent of changes in mean STN firing rates, and the relative timing of STN spikes was offset by half a gamma cycle for ipsilateral vs. contralateral movements, indicating that relative spike timing is as relevant as firing rate for understanding cortico-basal ganglia information transfer.
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spelling doaj.art-53f158ff278646829a20ecc8759714032022-12-22T03:52:58ZengeLife Sciences Publications LtdeLife2050-084X2020-03-01910.7554/eLife.51956Movement-related coupling of human subthalamic nucleus spikes to cortical gammaPetra Fischer0https://orcid.org/0000-0001-5585-8977Witold J Lipski1https://orcid.org/0000-0003-1499-6569Wolf-Julian Neumann2https://orcid.org/0000-0002-6758-9708Robert S Turner3https://orcid.org/0000-0002-6074-4365Pascal Fries4https://orcid.org/0000-0002-4270-1468Peter Brown5https://orcid.org/0000-0002-5201-3044R Mark Richardson6https://orcid.org/0000-0003-2620-7387Medical Research Council Brain Network Dynamics Unit, University of Oxford, Oxford, United Kingdom; Nuffield Department of Clinical Neurosciences, John Radcliffe Hospital, University of Oxford, Oxford, United KingdomNeurological Surgery, University of Pittsburgh School of Medicine, Pittsburgh, United StatesDepartment of Neurology, Campus Mitte, Charite - Universitaetsmedizin Berlin, Berlin, GermanyDepartment of Neurobiology, University of Pittsburgh, Pittsburgh, United States; Center for the Neural Basis of Cognition, University of Pittsburgh, Pittsburgh, United StatesErnst Strüngmann Institute (ESI) for Neuroscience in Cooperation with Max Planck Society, Frankfurt, Germany; Donders Institute for Brain, Cognition and Behaviour, Nijmegen, NetherlandsMedical Research Council Brain Network Dynamics Unit, University of Oxford, Oxford, United Kingdom; Nuffield Department of Clinical Neurosciences, John Radcliffe Hospital, University of Oxford, Oxford, United KingdomDepartment of Neurosurgery, Massachusetts General Hospital, Boston, United States; Harvard Medical School, Boston, United StatesCortico-basal ganglia interactions continuously shape the way we move. Ideas about how this circuit works are based largely on models those consider only firing rate as the mechanism of information transfer. A distinct feature of neural activity accompanying movement, however, is increased motor cortical and basal ganglia gamma synchrony. To investigate the relationship between neuronal firing in the basal ganglia and cortical gamma activity during movement, we analysed human ECoG and subthalamic nucleus (STN) unit activity during hand gripping. We found that fast reaction times were preceded by enhanced STN spike-to-cortical gamma phase coupling, indicating a role in motor preparation. Importantly, increased gamma phase coupling occurred independent of changes in mean STN firing rates, and the relative timing of STN spikes was offset by half a gamma cycle for ipsilateral vs. contralateral movements, indicating that relative spike timing is as relevant as firing rate for understanding cortico-basal ganglia information transfer.https://elifesciences.org/articles/51956Parkinson's diseasesubthalamic nucleusmotor controlgamma oscillationsECoGspike coupling
spellingShingle Petra Fischer
Witold J Lipski
Wolf-Julian Neumann
Robert S Turner
Pascal Fries
Peter Brown
R Mark Richardson
Movement-related coupling of human subthalamic nucleus spikes to cortical gamma
eLife
Parkinson's disease
subthalamic nucleus
motor control
gamma oscillations
ECoG
spike coupling
title Movement-related coupling of human subthalamic nucleus spikes to cortical gamma
title_full Movement-related coupling of human subthalamic nucleus spikes to cortical gamma
title_fullStr Movement-related coupling of human subthalamic nucleus spikes to cortical gamma
title_full_unstemmed Movement-related coupling of human subthalamic nucleus spikes to cortical gamma
title_short Movement-related coupling of human subthalamic nucleus spikes to cortical gamma
title_sort movement related coupling of human subthalamic nucleus spikes to cortical gamma
topic Parkinson's disease
subthalamic nucleus
motor control
gamma oscillations
ECoG
spike coupling
url https://elifesciences.org/articles/51956
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