Long ascending propriospinal neurons provide flexible, context-specific control of interlimb coordination

Abstract

Within the cervical and lumbar spinal enlargements, central pattern generating (CPG) circuitry produces the rhythmic output necessary for limb coordination during locomotion. Long propriospinal neurons that inter-connect these CPGs are thought to secure hindlimb-forelimb coordination, ensuring that diagonal limb pairs move synchronously while the ipsilateral limb pairs move out-of-phase during stepping. Here, we show that silencing long ascending propriospinal neurons (LAPNs) that interconnect the lumbar and cervical CPGs disrupts left-right limb coupling of each limb pair in the adult rat during overground locomotion on a high-friction surface. These perturbations occurred independent of the locomotor rhythm, intralimb coordination, and speed-dependent (or any other) principal features of locomotion. Strikingly, the functional consequences of silencing LAPNs are highly context-dependent; the phenotype was not expressed during swimming, treadmill stepping, exploratory locomotion, or walking on an uncoated, slick surface. These data reveal surprising flexibility and context-dependence in the control of interlimb coordination during locomotion.

Data availability

Source data has been provided for: Figures 2, 3, 4 and 5, Figure 1 figure supplement 1 and Figure 4 figure supplement 2

Article and author information

Author details

  1. Amanda M Pocratsky

    Anatomical Sciences and Neurobiology, University of Louisville, Louisville, United States
    Competing interests
    The authors declare that no competing interests exist.
  2. Courtney T Shepard

    Anatomical Sciences and Neurobiology, University of Louisville, Louisville, United States
    Competing interests
    The authors declare that no competing interests exist.
  3. Johnny R Morehouse

    Neurological Surgery, University of Louisville, Louisville, United States
    Competing interests
    The authors declare that no competing interests exist.
  4. Darlene A Burke

    Neurological Surgery, University of Louisville, Louisville, United States
    Competing interests
    The authors declare that no competing interests exist.
  5. Amberley S Riegler

    Neurological Surgery, University of Louisville, Louisville, United States
    Competing interests
    The authors declare that no competing interests exist.
  6. Josiah T Hardin

    J B Speed School of Engineering, University of Louisville, Louisville, United States
    Competing interests
    The authors declare that no competing interests exist.
  7. Jason E Beare

    Neurological Surgery, University of Louisville, Louisville, United States
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-3988-1223
  8. Casey Hainline

    Neurological Surgery, University of Louisville, Louisville, United States
    Competing interests
    The authors declare that no competing interests exist.
  9. Gregory JR States

    Anatomical Sciences and Neurobiology, University of Louisville, Louisville, United States
    Competing interests
    The authors declare that no competing interests exist.
  10. Brandon L Brown

    Neurological Surgery, University of Louisville, Louisville, United States
    Competing interests
    The authors declare that no competing interests exist.
  11. Scott R Whittemore

    Neurological Surgery, University of Louisville, Louisville, United States
    Competing interests
    The authors declare that no competing interests exist.
  12. David SK Magnuson

    Neurological Surgery and Anatomical Sciences and Neurobiology, University of Louisville, Louisville, United States
    For correspondence
    dsmagn01@louisville.edu
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-3816-3676

Funding

National Institute of Neurological Disorders and Stroke (R01 NS089324)

  • Scott R Whittemore
  • David SK Magnuson

National Institute of Neurological Disorders and Stroke (P30 GM103507)

  • Scott R Whittemore
  • David SK Magnuson

Kentucky Spinal Cord and Head Injury Research Trust (13-14)

  • Scott R Whittemore
  • David SK Magnuson

The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.

Ethics

Animal experimentation: This study was performed in strict accordance with the recommendations in the Guide for the Care and Use of Laboratory Animals of the National Institutes of Health. All of the animals were handled according to the approved institutional animal care and use committee (IACUC) protocol (#16669) of the University of Louisville. All surgery was performed under sodium pentobarbital or isoflurane anesthesia, and every effort was made to minimize suffering.

Reviewing Editor

  1. Ronald L Calabrese, Emory University, United States

Publication history

  1. Received: November 13, 2019
  2. Accepted: September 8, 2020
  3. Accepted Manuscript published: September 9, 2020 (version 1)
  4. Version of Record published: September 30, 2020 (version 2)

Copyright

© 2020, Pocratsky et al.

This article is distributed under the terms of the Creative Commons Attribution License permitting unrestricted use and redistribution provided that the original author and source are credited.

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  1. Amanda M Pocratsky
  2. Courtney T Shepard
  3. Johnny R Morehouse
  4. Darlene A Burke
  5. Amberley S Riegler
  6. Josiah T Hardin
  7. Jason E Beare
  8. Casey Hainline
  9. Gregory JR States
  10. Brandon L Brown
  11. Scott R Whittemore
  12. David SK Magnuson
(2020)
Long ascending propriospinal neurons provide flexible, context-specific control of interlimb coordination
eLife 9:e53565.
https://doi.org/10.7554/eLife.53565

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