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

Author:

Fischer Petra12ORCID,Lipski Witold J3ORCID,Neumann Wolf-Julian4ORCID,Turner Robert S56ORCID,Fries Pascal78ORCID,Brown Peter12ORCID,Richardson R Mark910ORCID

Affiliation:

1. Medical Research Council Brain Network Dynamics Unit, University of Oxford, Oxford, United Kingdom

2. Nuffield Department of Clinical Neurosciences, John Radcliffe Hospital, University of Oxford, Oxford, United Kingdom

3. Neurological Surgery, University of Pittsburgh School of Medicine, Pittsburgh, United States

4. Department of Neurology, Campus Mitte, Charite - Universitaetsmedizin Berlin, Berlin, Germany

5. Department of Neurobiology, University of Pittsburgh, Pittsburgh, United States

6. Center for the Neural Basis of Cognition, University of Pittsburgh, Pittsburgh, United States

7. Ernst Strüngmann Institute (ESI) for Neuroscience in Cooperation with Max Planck Society, Frankfurt, Germany

8. Donders Institute for Brain, Cognition and Behaviour, Nijmegen, Netherlands

9. Department of Neurosurgery, Massachusetts General Hospital, Boston, United States

10. Harvard Medical School, Boston, United States

Abstract

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.

Funder

Medical Research Council

National Institute for Health Research

National Institute of Mental Health

Deutsche Forschungsgemeinschaft

LOEWE Zentrum AdRIA

Pittsburgh Foundation

European Union 7th Framework Programme

Publisher

eLife Sciences Publications, Ltd

Subject

General Immunology and Microbiology,General Biochemistry, Genetics and Molecular Biology,General Medicine,General Neuroscience

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