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Rare phenomena of central rhythm and pattern generation in a case of complete spinal cord injury

Author

Listed:
  • Karen Minassian

    (Medical University of Vienna)

  • Aymeric Bayart

    (Medical University of Vienna)

  • Peter Lackner

    (Neurological Center, Clinic Penzing
    Clinic Floridsdorf)

  • Heinrich Binder

    (Neurological Center, Clinic Penzing)

  • Brigitta Freundl

    (Neurological Center, Clinic Penzing)

  • Ursula S. Hofstoetter

    (Medical University of Vienna)

Abstract

Lumbar central pattern generators (CPGs) control the basic rhythm and coordinate muscle activation underlying hindlimb locomotion in quadrupedal mammals. The existence and function of CPGs in humans have remained controversial. Here, we investigated a case of a male individual with complete thoracic spinal cord injury who presented with a rare form of self-sustained rhythmic spinal myoclonus in the legs and rhythmic activities induced by epidural electrical stimulation (EES). Analysis of muscle activation patterns suggested that the myoclonus tapped into spinal circuits that generate muscle spasms, rather than reflecting locomotor CPG activity as previously thought. The EES-induced patterns were fundamentally different in that they included flexor-extensor and left-right alternations, hallmarks of locomotor CPGs, and showed spontaneous errors in rhythmicity. These motor deletions, with preserved cycle frequency and period when rhythmic activity resumed, were previously reported only in animal studies and suggest a separation between rhythm generation and pattern formation. Spinal myoclonus and the EES-induced activity demonstrate that the human lumbar spinal cord contains distinct mechanisms for generating rhythmic multi-muscle patterns.

Suggested Citation

  • Karen Minassian & Aymeric Bayart & Peter Lackner & Heinrich Binder & Brigitta Freundl & Ursula S. Hofstoetter, 2023. "Rare phenomena of central rhythm and pattern generation in a case of complete spinal cord injury," Nature Communications, Nature, vol. 14(1), pages 1-15, December.
  • Handle: RePEc:nat:natcom:v:14:y:2023:i:1:d:10.1038_s41467-023-39034-y
    DOI: 10.1038/s41467-023-39034-y
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    1. Hansruedi Mathys & Jose Davila-Velderrain & Zhuyu Peng & Fan Gao & Shahin Mohammadi & Jennie Z. Young & Madhvi Menon & Liang He & Fatema Abdurrob & Xueqiao Jiang & Anthony J. Martorell & Richard M. Ra, 2019. "Author Correction: Single-cell transcriptomic analysis of Alzheimer’s disease," Nature, Nature, vol. 571(7763), pages 1-1, July.
    2. Claudia Kathe & Michael A. Skinnider & Thomas H. Hutson & Nicola Regazzi & Matthieu Gautier & Robin Demesmaeker & Salif Komi & Steven Ceto & Nicholas D. James & Newton Cho & Laetitia Baud & Katia Gala, 2022. "The neurons that restore walking after paralysis," Nature, Nature, vol. 611(7936), pages 540-547, November.
    3. Hansruedi Mathys & Jose Davila-Velderrain & Zhuyu Peng & Fan Gao & Shahin Mohammadi & Jennie Z. Young & Madhvi Menon & Liang He & Fatema Abdurrob & Xueqiao Jiang & Anthony J. Martorell & Richard M. Ra, 2019. "Single-cell transcriptomic analysis of Alzheimer’s disease," Nature, Nature, vol. 570(7761), pages 332-337, June.
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