Movement-related coupling of human subthalamic nucleus spikes to cortical gamma
- University of Oxford, United Kingdom
- University of Pittsburgh, United States
- Charité - Universitätsmedizin Berlin, Germany
- Ernst Strüngmann Institute (ESI) for Neuroscience in Cooperation with Max Planck Society, Germany
- Massachusetts General Hospital and Harvard Medical School, United States
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
Wolf-Julian Neumann
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.
Reviewing Editor
- Nicole C Swann, University of Oregon, United States
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).
Version history
- Received: September 17, 2019
- Accepted: March 11, 2020
- Accepted Manuscript published: March 11, 2020 (version 1)
- 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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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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