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Subthalamic nucleus stimulation restores the efferent cortical drive to muscle in parallel to functional motor improvement

Authors

  • Daniel Weiss,

    1. German Centre of Neurodegenerative Diseases, Tübingen, Germany
    2. Department for Neurodegenerative Diseases, Hertie Institute for Clinical Brain Research, University of Tübingen, Tübingen, Germany
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  • Sorin Breit,

    1. German Centre of Neurodegenerative Diseases, Tübingen, Germany
    2. Department for Neurodegenerative Diseases, Hertie Institute for Clinical Brain Research, University of Tübingen, Tübingen, Germany
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  • Julia Hoppe,

    1. Brain Imaging and Neurostimulation Laboratory, Department of Neurology, University Medical Center Hamburg-Eppendorf, Hamburg, Germany
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  • Ann-Kathrin Hauser,

    1. German Centre of Neurodegenerative Diseases, Tübingen, Germany
    2. Department for Neurodegenerative Diseases, Hertie Institute for Clinical Brain Research, University of Tübingen, Tübingen, Germany
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  • Dirk Freudenstein,

    1. Department of Functional and Stereotactic Neurosurgery, Medical Center Ludwigsburg, Ludwigsburg, Germany
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  • Rejko Krüger,

    1. German Centre of Neurodegenerative Diseases, Tübingen, Germany
    2. Department for Neurodegenerative Diseases, Hertie Institute for Clinical Brain Research, University of Tübingen, Tübingen, Germany
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  • Paul Sauseng,

    1. Brain Imaging and Neurostimulation Laboratory, Department of Neurology, University Medical Center Hamburg-Eppendorf, Hamburg, Germany
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  • Rathinaswamy B. Govindan,

    1. Division of Fetal and Transitional Medicine, Children’s National Medical Center, Washington, DC, USA
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  • Christian Gerloff

    1. Brain Imaging and Neurostimulation Laboratory, Department of Neurology, University Medical Center Hamburg-Eppendorf, Hamburg, Germany
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Dr D. Weiss, Center of Neurology and Hertie Institute for Clinical Brain Research, and German Center for Neurodegenerative Diseases, University of Tübingen, Hoppe-Seyler-Str. 3, D-72076 Tübingen, Germany.
E-mail: daniel.weiss@klinikum.uni-tuebingen.de

Abstract

Pathological synchronization in large-scale motor networks constitutes a pathophysiological hallmark of Parkinson’s disease (PD). Corticomuscular synchronization in PD is pronounced in lower frequency bands (< 10 Hz), whereas efficient cortical motor integration in healthy persons is driven in the beta frequency range. Electroencephalogram and electromyogram recordings at rest and during an isometric precision grip task were performed in four perioperative sessions in 10 patients with PD undergoing subthalamic nucleus deep-brain stimulation: (i) 1 day before (D0); (ii) 1 day after (D1); (iii) 8 days after implantation of macroelectrodes with stimulation off (D8StimOff); and (iv) on (D8StimOn). Analyses of coherence and phase delays were performed in order to challenge the effects of microlesion and stimulation on corticomuscular coherence (CMC). Additionally, local field potentials recorded from the subthalamic nucleus on D1 allowed comprehensive mapping of motor-related synchronization in subthalamocortical and cerebromuscular networks. Motor performance improved at D8StimOn compared with D0 and D8StimOff paralleled by a reduction of muscular activity and CMC in the theta band (3.9–7.8 Hz) and by an increase of CMC in the low-beta band (13.7–19.5 Hz). Efferent motor cortical drives to muscle presented mainly below 10 Hz on D8StimOff that were suppressed on D8StimOn and occurred on higher frequencies from 13 to 45 Hz. On D1, coherence of the high-beta band (20.5–30.2 Hz) increased during movement compared with rest in subthalamomuscular and corticomuscular projections, whereas it was attenuated in subcorticocortical projections. The present findings lend further support to the concept of pathological network synchronization in PD that is beneficially modulated by stimulation.

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