1. Neuroscience

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

  1. Petra Fischer  Is a corresponding author
  2. Witold J Lipski
  3. Wolf-Julian Neumann
  4. Robert S Turner
  5. Pascal Fries
  6. Peter Brown
  7. Robert Mark Richardson  Is a corresponding author
  1. University of Oxford, United Kingdom
  2. University of Pittsburgh, United States
  3. Charité - Universitätsmedizin Berlin, Germany
  4. Ernst Strüngmann Institute (ESI) for Neuroscience in Cooperation with Max Planck Society, Germany
  5. Massachusetts General Hospital and Harvard Medical School, United States
https://doi.org/10.7554/eLife.51956
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Cite this article
  1. Petra Fischer
  2. Witold J Lipski
  3. Wolf-Julian Neumann
  4. Robert S Turner
  5. Pascal Fries
  6. Peter Brown
  7. Robert Mark Richardson
(2020)
Movement-related coupling of human subthalamic nucleus spikes to cortical gamma
eLife 9:e51956.
https://doi.org/10.7554/eLife.51956
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Abstract

Cortico-basal ganglia interactions continuously shape the way we move. Ideas about how this circuit works are based largely on models that 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.

Data availability

We have provided the data and the code (including the functions to run the cluster-based permutation statistics) with which one can generate the time-frequency figures in the main manuscript and in the supplementary figures (Fig. 3, 4, Fig. 3- figure supplement 5 and Fig. 4-figure supplement 2).

Article and author information

Author details

  1. Petra Fischer

    Nuffield Department of Clinical Neurosciences, John Radcliffe Hospital, University of Oxford, Oxford, United Kingdom
    For correspondence
    petra.fischer@ndcn.ox.ac.uk
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-5585-8977

  2. Witold J Lipski

    Neurosurgery, University of Pittsburgh, Pittsburgh, United States
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-1499-6569

  3. Wolf-Julian Neumann

    Department of Neurology, Charité - Universitätsmedizin Berlin, Berlin, Germany
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-6758-9708

  4. Robert S Turner

    Department of Neurobiology, University of Pittsburgh, Pittsburgh, United States
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-6074-4365

  5. Pascal Fries

    Ernst Strüngmann Institute (ESI) for Neuroscience in Cooperation with Max Planck Society, Frankfurt, Germany
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-4270-1468

  6. Peter Brown

    Nuffield Department of Clinical Neurosciences, John Radcliffe Hospital, University of Oxford, Oxford, United Kingdom
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-5201-3044

  7. Robert Mark Richardson

    Department of Neurosurgery, Massachusetts General Hospital and Harvard Medical School, Boston, United States
    For correspondence
    Mark.Richardson@mgh.harvard.edu
    Competing interests
    The authors declare that no competing interests exist.

Funding

Medical Research Council (MC_UU_12024/1)

  • Petra Fischer
  • Peter Brown

National Institute for Health Research (R01 NS091853-01A1)

  • Robert S Turner

National Institute for Health Research (R01 NS110424-01 CRCNS)

  • Robert S Turner
  • Robert Mark Richardson

National Institute of Mental Health (R01MH107797)

  • Witold J Lipski
  • Robert Mark Richardson

Deutsche Forschungsgemeinschaft (SPP 1665,FOR 1847,FR2557/5-1-CORNET,FR2557/6-1-NeuroTMR)

  • Pascal Fries

National Institute for Health Research (1U54MH091657-WU-Minn-Consortium-HCP)

  • Pascal Fries

LOEWE Zentrum AdRIA (NeFF)

  • Pascal Fries

The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.

Ethics

Human subjects: Patients provided written, informed consent in accordance with a protocol approved by the Institutional Review Board of the University of Pittsburgh (IRB Protocol no. PRO13110420).

Reviewing Editor

  1. Nicole C Swann, University of Oregon, United States

Version history

  1. Received: September 17, 2019
  2. Accepted: March 11, 2020
  3. Accepted Manuscript published: March 11, 2020 (version 1)
  4. Version of Record published: March 25, 2020 (version 2)

Copyright

© 2020, Fischer et al.

This article is distributed under the terms of the Creative Commons Attribution License permitting unrestricted use and redistribution provided that the original author and source are credited.

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  1. Petra Fischer
  2. Witold J Lipski
  3. Wolf-Julian Neumann
  4. Robert S Turner
  5. Pascal Fries
  6. Peter Brown
  7. Robert Mark Richardson
(2020)
Movement-related coupling of human subthalamic nucleus spikes to cortical gamma
eLife 9:e51956.
https://doi.org/10.7554/eLife.51956

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