IDEAS home Printed from https://ideas.repec.org/a/nat/natcom/v14y2023i1d10.1038_s41467-023-39034-y.html
   My bibliography  Save this article

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
    as

    Download full text from publisher

    File URL: https://www.nature.com/articles/s41467-023-39034-y
    File Function: Abstract
    Download Restriction: no

    File URL: https://libkey.io/10.1038/s41467-023-39034-y?utm_source=ideas
    LibKey link: if access is restricted and if your library uses this service, LibKey will redirect you to where you can use your library subscription to access this item
    ---><---

    References listed on IDEAS

    as
    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. 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.
    3. 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.
    Full references (including those not matched with items on IDEAS)

    Most related items

    These are the items that most often cite the same works as this one and are cited by the same works as this one.
    1. Hyun-Sik Yang & Ling Teng & Daniel Kang & Vilas Menon & Tian Ge & Hilary K. Finucane & Aaron P. Schultz & Michael Properzi & Hans-Ulrich Klein & Lori B. Chibnik & Julie A. Schneider & David A. Bennett, 2023. "Cell-type-specific Alzheimer’s disease polygenic risk scores are associated with distinct disease processes in Alzheimer’s disease," Nature Communications, Nature, vol. 14(1), pages 1-13, December.
    2. Chang Su & Zichun Xu & Xinning Shan & Biao Cai & Hongyu Zhao & Jingfei Zhang, 2023. "Cell-type-specific co-expression inference from single cell RNA-sequencing data," Nature Communications, Nature, vol. 14(1), pages 1-12, December.
    3. Osama Al-Dalahmah & Michael G. Argenziano & Adithya Kannan & Aayushi Mahajan & Julia Furnari & Fahad Paryani & Deborah Boyett & Akshay Save & Nelson Humala & Fatima Khan & Juncheng Li & Hong Lu & Yu S, 2023. "Re-convolving the compositional landscape of primary and recurrent glioblastoma reveals prognostic and targetable tissue states," Nature Communications, Nature, vol. 14(1), pages 1-18, December.
    4. Elaine T. Lim & Yingleong Chan & Pepper Dawes & Xiaoge Guo & Serkan Erdin & Derek J. C. Tai & Songlei Liu & Julia M. Reichert & Mannix J. Burns & Ying Kai Chan & Jessica J. Chiang & Katharina Meyer & , 2022. "Orgo-Seq integrates single-cell and bulk transcriptomic data to identify cell type specific-driver genes associated with autism spectrum disorder," Nature Communications, Nature, vol. 13(1), pages 1-14, December.
    5. Logan Brase & Shih-Feng You & Ricardo D’Oliveira Albanus & Jorge L. Del-Aguila & Yaoyi Dai & Brenna C. Novotny & Carolina Soriano-Tarraga & Taitea Dykstra & Maria Victoria Fernandez & John P. Budde & , 2023. "Single-nucleus RNA-sequencing of autosomal dominant Alzheimer disease and risk variant carriers," Nature Communications, Nature, vol. 14(1), pages 1-19, December.
    6. Torben Johann Hausrat & Philipp C. Janiesch & Petra Breiden & David Lutz & Sabine Hoffmeister-Ullerich & Irm Hermans-Borgmeyer & Antonio Virgilio Failla & Matthias Kneussel, 2022. "Disruption of tubulin-alpha4a polyglutamylation prevents aggregation of hyper-phosphorylated tau and microglia activation in mice," Nature Communications, Nature, vol. 13(1), pages 1-18, December.
    7. Ying Lei & Mengnan Cheng & Zihao Li & Zhenkun Zhuang & Liang Wu & Yunong sun & Lei Han & Zhihao Huang & Yuzhou Wang & Zifei Wang & Liqin Xu & Yue Yuan & Shang Liu & Taotao Pan & Jiarui Xie & Chuanyu L, 2022. "Spatially resolved gene regulatory and disease-related vulnerability map of the adult Macaque cortex," Nature Communications, Nature, vol. 13(1), pages 1-20, December.
    8. Thomas S. Wingo & Yue Liu & Ekaterina S. Gerasimov & Selina M. Vattathil & Meghan E. Wynne & Jiaqi Liu & Adriana Lori & Victor Faundez & David A. Bennett & Nicholas T. Seyfried & Allan I. Levey & Aliz, 2022. "Shared mechanisms across the major psychiatric and neurodegenerative diseases," Nature Communications, Nature, vol. 13(1), pages 1-19, December.
    9. Manik Kuchroo & Marcello DiStasio & Eric Song & Eda Calapkulu & Le Zhang & Maryam Ige & Amar H. Sheth & Abdelilah Majdoubi & Madhvi Menon & Alexander Tong & Abhinav Godavarthi & Yu Xing & Scott Gigant, 2023. "Single-cell analysis reveals inflammatory interactions driving macular degeneration," Nature Communications, Nature, vol. 14(1), pages 1-22, December.
    10. Nelson Johansen & Hongru Hu & Gerald Quon, 2023. "Projecting RNA measurements onto single cell atlases to extract cell type-specific expression profiles using scProjection," Nature Communications, Nature, vol. 14(1), pages 1-15, December.
    11. Hannah Drew Rickner & Lulu Jiang & Rui Hong & Nicholas K. O’Neill & Chromewell A. Mojica & Benjamin J. Snyder & Lushuang Zhang & Dipan Shaw & Maria Medalla & Benjamin Wolozin & Christine S. Cheng, 2022. "Single cell transcriptomic profiling of a neuron-astrocyte assembloid tauopathy model," Nature Communications, Nature, vol. 13(1), pages 1-22, December.
    12. Zoeb Jiwaji & Sachin S. Tiwari & Rolando X. Avilés-Reyes & Monique Hooley & David Hampton & Megan Torvell & Delinda A. Johnson & Jamie McQueen & Paul Baxter & Kayalvizhi Sabari-Sankar & Jing Qiu & Xin, 2022. "Reactive astrocytes acquire neuroprotective as well as deleterious signatures in response to Tau and Aß pathology," Nature Communications, Nature, vol. 13(1), pages 1-23, December.
    13. Zu-Qiang Liu & Hao Dai & Lu Yao & Wei-Feng Chen & Yun Wang & Li-Yun Ma & Xiao-Qing Li & Sheng-Li Lin & Meng-Jiang He & Ping-Ting Gao & Xin-Yang Liu & Jia-Xin Xu & Xiao-Yue Xu & Ke-Hao Wang & Li Wang &, 2023. "A single-cell transcriptional landscape of immune cells shows disease-specific changes of T cell and macrophage populations in human achalasia," Nature Communications, Nature, vol. 14(1), pages 1-19, December.
    14. Jia-Ru Wei & Zhao-Zhe Hao & Chuan Xu & Mengyao Huang & Lei Tang & Nana Xu & Ruifeng Liu & Yuhui Shen & Sarah A. Teichmann & Zhichao Miao & Sheng Liu, 2022. "Identification of visual cortex cell types and species differences using single-cell RNA sequencing," Nature Communications, Nature, vol. 13(1), pages 1-21, December.
    15. Nicola A. Kearns & Artemis Iatrou & Daniel J. Flood & Sashini Tissera & Zachary M. Mullaney & Jishu Xu & Chris Gaiteri & David A. Bennett & Yanling Wang, 2023. "Dissecting the human leptomeninges at single-cell resolution," Nature Communications, Nature, vol. 14(1), pages 1-16, December.
    16. BaDoi N. Phan & Madelyn H. Ray & Xiangning Xue & Chen Fu & Robert J. Fenster & Stephen J. Kohut & Jack Bergman & Suzanne N. Haber & Kenneth M. McCullough & Madeline K. Fish & Jill R. Glausier & Qiao S, 2024. "Single nuclei transcriptomics in human and non-human primate striatum in opioid use disorder," Nature Communications, Nature, vol. 15(1), pages 1-19, December.
    17. Malosree Maitra & Haruka Mitsuhashi & Reza Rahimian & Anjali Chawla & Jennie Yang & Laura M. Fiori & Maria Antonietta Davoli & Kelly Perlman & Zahia Aouabed & Deborah C. Mash & Matthew Suderman & Nagu, 2023. "Cell type specific transcriptomic differences in depression show similar patterns between males and females but implicate distinct cell types and genes," Nature Communications, Nature, vol. 14(1), pages 1-18, December.
    18. Juan F. Quintana & Praveena Chandrasegaran & Matthew C. Sinton & Emma M. Briggs & Thomas D. Otto & Rhiannon Heslop & Calum Bentley-Abbot & Colin Loney & Luis de Lecea & Neil A. Mabbott & Annette MacLe, 2022. "Single cell and spatial transcriptomic analyses reveal microglia-plasma cell crosstalk in the brain during Trypanosoma brucei infection," Nature Communications, Nature, vol. 13(1), pages 1-19, December.
    19. Shinya Tasaki & Jishu Xu & Denis R. Avey & Lynnaun Johnson & Vladislav A. Petyuk & Robert J. Dawe & David A. Bennett & Yanling Wang & Chris Gaiteri, 2022. "Inferring protein expression changes from mRNA in Alzheimer’s dementia using deep neural networks," Nature Communications, Nature, vol. 13(1), pages 1-15, December.
    20. Anna Podleśny-Drabiniok & Gloriia Novikova & Yiyuan Liu & Josefine Dunst & Rose Temizer & Chiara Giannarelli & Samuele Marro & Taras Kreslavsky & Edoardo Marcora & Alison Mary Goate, 2024. "BHLHE40/41 regulate microglia and peripheral macrophage responses associated with Alzheimer’s disease and other disorders of lipid-rich tissues," Nature Communications, Nature, vol. 15(1), pages 1-19, December.

    More about this item

    Statistics

    Access and download statistics

    Corrections

    All material on this site has been provided by the respective publishers and authors. You can help correct errors and omissions. When requesting a correction, please mention this item's handle: RePEc:nat:natcom:v:14:y:2023:i:1:d:10.1038_s41467-023-39034-y. See general information about how to correct material in RePEc.

    If you have authored this item and are not yet registered with RePEc, we encourage you to do it here. This allows to link your profile to this item. It also allows you to accept potential citations to this item that we are uncertain about.

    If CitEc recognized a bibliographic reference but did not link an item in RePEc to it, you can help with this form .

    If you know of missing items citing this one, you can help us creating those links by adding the relevant references in the same way as above, for each refering item. If you are a registered author of this item, you may also want to check the "citations" tab in your RePEc Author Service profile, as there may be some citations waiting for confirmation.

    For technical questions regarding this item, or to correct its authors, title, abstract, bibliographic or download information, contact: Sonal Shukla or Springer Nature Abstracting and Indexing (email available below). General contact details of provider: http://www.nature.com .

    Please note that corrections may take a couple of weeks to filter through the various RePEc services.

    IDEAS is a RePEc service. RePEc uses bibliographic data supplied by the respective publishers.