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Intraoperative electrical stimulation of the human dorsal spinal cord reveals a map of arm and hand muscle responses

View ORCID ProfileJames R. McIntosh, View ORCID ProfileEvan. F. Joiner, View ORCID ProfileJacob L. Goldberg, View ORCID ProfileLynda M. Murray, View ORCID ProfileBushra Yasin, View ORCID ProfileAnil Mendiratta, View ORCID ProfileSteven C. Karceski, View ORCID ProfileEarl Thuet, View ORCID ProfileOleg Modik, View ORCID ProfileEvgeny Shelkov, View ORCID ProfileJoseph M. Lombardi, View ORCID ProfileZeeshan M. Sardar, View ORCID ProfileRonald A. Lehman, View ORCID ProfileChristopher Mandigo, View ORCID ProfileK. Daniel Riew, View ORCID ProfileNoam Y. Harel, View ORCID ProfileMichael S. Virk, View ORCID ProfileJason B. Carmel
doi: https://doi.org/10.1101/2022.01.29.478182
James R. McIntosh
aDept. of Orthopedic Surgery, Columbia University, 650 W. 168th St, New York, NY, 10032, USA
dDept. of Neurological Surgery, Weill Cornell Medicine - New York Presbyterian, Och Spine, 1300 York Ave, New York, NY 10065
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  • ORCID record for James R. McIntosh
  • For correspondence: jason.carmel@columbia.edu j.mcintsoh@columbia.edu
Evan. F. Joiner
bDept. of Neurological Surgery, Columbia University, 650 W. 168th St, New York, NY, 10032, USA
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  • ORCID record for Evan. F. Joiner
Jacob L. Goldberg
dDept. of Neurological Surgery, Weill Cornell Medicine - New York Presbyterian, Och Spine, 1300 York Ave, New York, NY 10065
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  • ORCID record for Jacob L. Goldberg
Lynda M. Murray
hRehabil. and Human Performance, Icahn Sch. of Med. at Mount Sinai, One Gustave L. Levy Place, New York, NY 10029
iJames J. Peters VA Med. Ctr., 130 West Kingsbridge Road, Bronx, NY 10468
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Bushra Yasin
aDept. of Orthopedic Surgery, Columbia University, 650 W. 168th St, New York, NY, 10032, USA
dDept. of Neurological Surgery, Weill Cornell Medicine - New York Presbyterian, Och Spine, 1300 York Ave, New York, NY 10065
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Anil Mendiratta
cDept. of Neurology, Columbia University, 650 W. 168th St, New York, NY, 10032, USA
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  • ORCID record for Anil Mendiratta
Steven C. Karceski
eDept. of Neurology, Weill Cornell Medicine - New York Presbyterian, Och Spine, 1300 York Ave, New York, NY 10065
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Earl Thuet
fNew York Presbyterian, The Och Spine Hospital, 5141 Broadway, New York, NY 10034
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  • ORCID record for Earl Thuet
Oleg Modik
eDept. of Neurology, Weill Cornell Medicine - New York Presbyterian, Och Spine, 1300 York Ave, New York, NY 10065
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Evgeny Shelkov
eDept. of Neurology, Weill Cornell Medicine - New York Presbyterian, Och Spine, 1300 York Ave, New York, NY 10065
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Joseph M. Lombardi
aDept. of Orthopedic Surgery, Columbia University, 650 W. 168th St, New York, NY, 10032, USA
fNew York Presbyterian, The Och Spine Hospital, 5141 Broadway, New York, NY 10034
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Zeeshan M. Sardar
aDept. of Orthopedic Surgery, Columbia University, 650 W. 168th St, New York, NY, 10032, USA
fNew York Presbyterian, The Och Spine Hospital, 5141 Broadway, New York, NY 10034
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Ronald A. Lehman
aDept. of Orthopedic Surgery, Columbia University, 650 W. 168th St, New York, NY, 10032, USA
fNew York Presbyterian, The Och Spine Hospital, 5141 Broadway, New York, NY 10034
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Christopher Mandigo
bDept. of Neurological Surgery, Columbia University, 650 W. 168th St, New York, NY, 10032, USA
fNew York Presbyterian, The Och Spine Hospital, 5141 Broadway, New York, NY 10034
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K. Daniel Riew
aDept. of Orthopedic Surgery, Columbia University, 650 W. 168th St, New York, NY, 10032, USA
dDept. of Neurological Surgery, Weill Cornell Medicine - New York Presbyterian, Och Spine, 1300 York Ave, New York, NY 10065
fNew York Presbyterian, The Och Spine Hospital, 5141 Broadway, New York, NY 10034
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Noam Y. Harel
gDepartments of Neurol., Icahn Sch. of Med. at Mount Sinai, One Gustave L. Levy Place, New York, NY 10029
hRehabil. and Human Performance, Icahn Sch. of Med. at Mount Sinai, One Gustave L. Levy Place, New York, NY 10029
iJames J. Peters VA Med. Ctr., 130 West Kingsbridge Road, Bronx, NY 10468
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Michael S. Virk
dDept. of Neurological Surgery, Weill Cornell Medicine - New York Presbyterian, Och Spine, 1300 York Ave, New York, NY 10065
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Jason B. Carmel
aDept. of Orthopedic Surgery, Columbia University, 650 W. 168th St, New York, NY, 10032, USA
cDept. of Neurology, Columbia University, 650 W. 168th St, New York, NY, 10032, USA
dDept. of Neurological Surgery, Weill Cornell Medicine - New York Presbyterian, Och Spine, 1300 York Ave, New York, NY 10065
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  • For correspondence: jason.carmel@columbia.edu j.mcintsoh@columbia.edu
  • Abstract
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Abstract

While epidural stimulation of the lumbar spinal cord has emerged as a powerful modality for recovery of movement, how it should be targeted to the cervical spinal cord to activate arm and hand muscles is not well-understood, particularly in humans. We sought to map muscle responses to posterior epidural cervical spinal cord stimulation in humans. We hypothesized that lateral stimulation over the dorsal root entry zone would be most effective, and responses would be strongest in the muscles innervated by the stimulated segment. Twenty-five people undergoing clinically indicated cervical spine surgery were consented to map motor responses. During surgery, stimulation was performed in midline and lateral positions at multiple exposed segments; six arm and three leg muscles were recorded on each side of the body. Across all segments and muscles tested, lateral stimulation produced stronger muscle responses than midline despite similar latency and shape of responses. Muscles innervated at a cervical segment had the largest responses from stimulation at that segment, but responses were also observed in muscles innervated at other cervical segments and in leg muscles. The cervical responses were clustered in rostral (C4-C6) and caudal (C7-T1) cervical segments. Strong responses to lateral stimulation are likely due to the proximity of stimulation to afferent axons. Small changes in response sizes to stimulation of adjacent cervical segments argues for local circuit integration, and distant muscle responses suggest activation of long propriospinal connections. This map can help guide cervical stimulation to improve arm and hand function.

New and noteworthy A map of muscle responses to cervical epidural stimulation during clinically indicated surgery revealed strongest activation when stimulating laterally compared to midline, and differences to be weaker than expected across different segments. In contrast, waveform shapes and latencies were most similar when stimulating midline and laterally indicating activation of overlapping circuitry. Thus, a map of the cervical spinal cord reveals organization and may help guide stimulation to activate arm and hand muscles strongly and selectively.

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Competing Interest Statement

Jason B. Carmel is a Founder and stock holder in BackStop Neural and a scientific advisor for SharperSense. Michael S. Virk has been a consultant and has received honorarium from Depuy Synthes, Globus Medical and BrainLab. Noam Y. Harel is a consultant for RubiconMD. K. Daniel Riew: Consulting: Happe Spine (Nonfinancial), Nuvasive; Royalties: Biomet; Speaking and/or Teaching Arrangements: Biomet, Medtronic (Travel Expense Reimbursement); Stock Ownership: Amedica, Axiomed, Benvenue, Expanding Orthopedics, Osprey, Paradigm Spine, Spinal Kinetics, Spineology, Vertiflex. The other authors have nothing to disclose.

Footnotes

  • ↵* J. B. Carmel and M. S. Virk should be considered joint senior authors.

  • https://doi.org/10.6084/m9.figshare.19891966

  • Abbreviations

    mJOA
    Modified Japanese Orthopaedic Association;
    MEP
    Motor Evoked Potential;
    TA
    Tibialis Anterior;
    EDB
    Extensor Digitorum Brevis;
    AH
    Abductor Hallucis;
    AUC
    Area Under the Curve;
    SCI
    Spinal Cord Injury;
    SEM
    Standard Error of the Mean.
  • Copyright 
    The copyright holder for this preprint is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under a CC-BY-NC-ND 4.0 International license.
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    Intraoperative electrical stimulation of the human dorsal spinal cord reveals a map of arm and hand muscle responses
    James R. McIntosh, Evan. F. Joiner, Jacob L. Goldberg, Lynda M. Murray, Bushra Yasin, Anil Mendiratta, Steven C. Karceski, Earl Thuet, Oleg Modik, Evgeny Shelkov, Joseph M. Lombardi, Zeeshan M. Sardar, Ronald A. Lehman, Christopher Mandigo, K. Daniel Riew, Noam Y. Harel, Michael S. Virk, Jason B. Carmel
    bioRxiv 2022.01.29.478182; doi: https://doi.org/10.1101/2022.01.29.478182
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    Intraoperative electrical stimulation of the human dorsal spinal cord reveals a map of arm and hand muscle responses
    James R. McIntosh, Evan. F. Joiner, Jacob L. Goldberg, Lynda M. Murray, Bushra Yasin, Anil Mendiratta, Steven C. Karceski, Earl Thuet, Oleg Modik, Evgeny Shelkov, Joseph M. Lombardi, Zeeshan M. Sardar, Ronald A. Lehman, Christopher Mandigo, K. Daniel Riew, Noam Y. Harel, Michael S. Virk, Jason B. Carmel
    bioRxiv 2022.01.29.478182; doi: https://doi.org/10.1101/2022.01.29.478182

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