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Featured ArticleResearch Articles, Systems/Circuits

Cortico-Cerebellar Connectivity Underlying Motor Control in Chronic Poststroke Individuals

Raghavan Gopalakrishnan, David A. Cunningham, Olivia Hogue, Madeleine Schroedel, Brett A. Campbell, Ela B. Plow, Kenneth B. Baker and Andre G. Machado
Journal of Neuroscience 29 June 2022, 42 (26) 5186-5197; DOI: https://doi.org/10.1523/JNEUROSCI.2443-21.2022
Raghavan Gopalakrishnan
1Center for Neurological Restoration, Neurological Institute, Cleveland Clinic, Cleveland, Ohio 44195
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David A. Cunningham
2Physical Medicine and Rehabilitation, School of Medicine, Case Western Reserve University, Cleveland, Ohio 44195
9Physical Medicine and Rehabilitation, MetroHealth Center for Rehabilitation Research, Cleveland, Ohio 44109
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Olivia Hogue
3Department of Quantitative Health Sciences, Lerner Research Institute, Cleveland Clinic, Cleveland, Ohio 44195
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Madeleine Schroedel
4Department of Neurosciences, Lerner Research Institute, Cleveland Clinic, Cleveland, Ohio 44195
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Brett A. Campbell
4Department of Neurosciences, Lerner Research Institute, Cleveland Clinic, Cleveland, Ohio 44195
5Department of Biomedical Engineering, Case Western Reserve University, Cleveland, Ohio 44195
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Ela B. Plow
6Department of Biomedical Engineering, Lerner Research Institute, Cleveland Clinic, Cleveland, Ohio 44195
8Physical Medicine and Rehabilitation, Neurological Institute, Cleveland Clinic, Cleveland OH 44195
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Kenneth B. Baker
4Department of Neurosciences, Lerner Research Institute, Cleveland Clinic, Cleveland, Ohio 44195
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Andre G. Machado
1Center for Neurological Restoration, Neurological Institute, Cleveland Clinic, Cleveland, Ohio 44195
7Department of Neurosurgery, Neurological Institute, Cleveland Clinic, Cleveland, Ohio 44195
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Abstract

The robust, reciprocal anatomic connections between the cerebellum and contralateral sensorimotor cerebral hemisphere underscore the strong physiological interdependence between these two regions in relation to human behavior. Previous studies have shown that damage to sensorimotor cortex can result in a lasting reduction of cerebellar metabolism, the magnitude of which has been linked to poor rehabilitative outcomes. A better understanding of movement-related cerebellar physiology as well as cortico-cerebellar coherence (CCC) in the chronic, poststroke state may be key to developing novel neuromodulatory techniques that promote upper limb motor rehabilitation. As a part of the first in-human phase I trial investigating the effects of deep brain stimulation of the cerebellar dentate nucleus (DN) on chronic poststroke motor rehabilitation, we collected invasive recordings from DN and scalp EEG in participants (both sexes) with middle cerebral artery stroke during a visuo-motor tracking task. We investigated the excitability of ipsilesional cortex, DN, and their interaction as a function of motor impairment and performance. Our results indicate the following: (1) event-related oscillations in the ipsilesional cortex and DN were significantly correlated at movement onset in the low beta band, with moderately and severely impaired participants showing desynchronization and synchronization, respectively; and (2) significant CCC was observed during the isometric hold period in the low beta band, which was critical for maintaining task accuracy. Our findings support a strong coupling between ipsilesional cortex and DN in the low beta band during motor control across all impairment levels, which encourages the exploitation of the cerebello–thalamo–cortical pathway as a neuromodulation target to promote rehabilitation.

SIGNIFICANCE STATEMENT Cerebral infarct because of stroke can lead to lasting reduction in cerebellar metabolism, resulting in poor rehabilitative outcomes. Thorough investigation of the cerebellar electrophysiology, as well as cortico-cerebellar connectivity in humans that could provide key insights to facilitate the development of novel neuromodulatory technologies, has been lacking. As a part of the first in-human phase I trial investigating deep brain stimulation of the cerebellar dentate nucleus (DN) for chronic, poststroke motor rehabilitation, we collected invasive recordings from DN and scalp EEG while stroke survivors performed a motor task. Our data indicate strong coupling between ipsilesional sensorimotor cortex and DN in the low beta band across all impairment levels encouraging the exploration of electrical stimulation of the DN.

  • cortico-cerebellar coherence
  • deep brain stimulation
  • dentate nucleus
  • invasive electrophysiology
  • stroke

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The Journal of Neuroscience: 42 (26)
Journal of Neuroscience
Vol. 42, Issue 26
29 Jun 2022
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Cortico-Cerebellar Connectivity Underlying Motor Control in Chronic Poststroke Individuals
Raghavan Gopalakrishnan, David A. Cunningham, Olivia Hogue, Madeleine Schroedel, Brett A. Campbell, Ela B. Plow, Kenneth B. Baker, Andre G. Machado
Journal of Neuroscience 29 June 2022, 42 (26) 5186-5197; DOI: 10.1523/JNEUROSCI.2443-21.2022

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Cortico-Cerebellar Connectivity Underlying Motor Control in Chronic Poststroke Individuals
Raghavan Gopalakrishnan, David A. Cunningham, Olivia Hogue, Madeleine Schroedel, Brett A. Campbell, Ela B. Plow, Kenneth B. Baker, Andre G. Machado
Journal of Neuroscience 29 June 2022, 42 (26) 5186-5197; DOI: 10.1523/JNEUROSCI.2443-21.2022
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Keywords

  • cortico-cerebellar coherence
  • deep brain stimulation
  • dentate nucleus
  • invasive electrophysiology
  • stroke

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