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Motoneurons regulate the central pattern generator during drug-induced locomotor-like activity in the neonatal mouse

  1. Melanie Falgairolle  Is a corresponding author
  2. Joshua G Puhl
  3. Avinash Pujala
  4. Wenfang Liu
  5. Michael James O'Donovan
  1. National Institute of Neurological Disorders and Stroke, National Institutes of Health, United States
  2. University of Minnesota, United States
  3. Howard Hughes Medical Institute, United States
Research Article
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Cite this article as: eLife 2017;6:e26622 doi: 10.7554/eLife.26622

Abstract

Motoneurons are traditionally viewed as the output of the spinal cord that do not influence locomotor rhythmogenesis. We assessed the role of motoneuron firing during ongoing locomotor-like activity in neonatal mice expressing archaerhopsin-3 (Arch), halorhodopsin (eNpHR), or channelrhodopsin-2 (ChR2) in Choline acetyltransferase expressing neurons (ChAT+) or the LIM-homeodomain transcription factor Isl1+ neurons. Illumination of the lumbar cord in mice expressing eNpHR or Arch in ChAT+ or Isl1+ neurons, depressed motoneuron discharge, transiently decreased the frequency, and perturbed the phasing of the locomotor-like rhythm. When the light was turned off motoneuron firing and locomotor frequency both transiently increased. These effects were not due to cholinergic neurotransmission, persisted during partial blockade of gap junctions and were mediated, in part, by AMPAergic transmission. In spinal cords expressing ChR2, illumination increased motoneuron discharge and transiently accelerated the rhythm. We conclude that motoneurons provide feedback to the central pattern generator (CPG) during drug-induced locomotor-like activity.

Article and author information

Author details

  1. Melanie Falgairolle

    Developmental Neurobiology section, National Institute of Neurological Disorders and Stroke, National Institutes of Health, Bethesda, United States
    For correspondence
    melanie.falgairolle@nih.gov
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-5243-4714
  2. Joshua G Puhl

    Department of Entomology, University of Minnesota, Saint Paul, United States
    Competing interests
    The authors declare that no competing interests exist.
  3. Avinash Pujala

    Janelia Farm Research Campus, Howard Hughes Medical Institute, Ashburn, United States
    Competing interests
    The authors declare that no competing interests exist.
  4. Wenfang Liu

    Developmental Neurobiology Section, National Institute of Neurological Disorders and Stroke, National Institutes of Health, Bethesda, United States
    Competing interests
    The authors declare that no competing interests exist.
  5. Michael James O'Donovan

    Developmental Neurobiology Section, National Institute of Neurological Disorders and Stroke, National Institutes of Health, Bethesda, United States
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-2487-7547

Funding

National Institutes of Health (NINDS Intramural program)

  • Melanie Falgairolle

National Institutes of Health (NINDS Intramural program)

  • Michael James O'Donovan

National Institutes of Health (NINDS Intramural program)

  • Joshua G Puhl

National Institutes of Health (NINDS Intramural NRSA)

  • Joshua G Puhl

National Institutes of Health (NINDS Intramural program)

  • Wenfang Liu

National Institutes of Health (NINDS Intramural program)

  • Avinash Pujala

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

Ethics

Animal experimentation: All experiments were carried out in compliance with the National Institutes of Neurological Disorders and Stroke Animal Care and Use Committee (Animal Protocol Number 1267-12 and 1267-15).

Reviewing Editor

  1. Ole Kiehn, Karolinska Institutet, Sweden

Publication history

  1. Received: March 9, 2017
  2. Accepted: June 30, 2017
  3. Accepted Manuscript published: July 3, 2017 (version 1)
  4. Version of Record published: August 9, 2017 (version 2)

Copyright

This is an open-access article, free of all copyright, and may be freely reproduced, distributed, transmitted, modified, built upon, or otherwise used by anyone for any lawful purpose. The work is made available under the Creative Commons CC0 public domain dedication.

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