1. Neuroscience
Download icon

The recovery of standing and locomotion after spinal cord injury does not require task-specific training

Research Article
  • Cited 8
  • Views 2,159
  • Annotations
Cite this article as: eLife 2019;8:e50134 doi: 10.7554/eLife.50134

Abstract

After complete spinal cord injury, mammals, including mice, rats and cats, recover hindlimb locomotion with treadmill training. The premise is that sensory cues consistent with locomotion reorganize spinal sensorimotor circuits. Here, we show that hindlimb standing and locomotion recover after spinal transection in cats without task-specific training. Spinal-transected cats recovered full weight bearing standing and locomotion after five weeks of rhythmic manual stimulation of triceps surae muscles (non-specific training) and without any intervention. Moreover, cats modulated locomotor speed and performed split-belt locomotion six weeks after spinal transection, functions that were not trained or tested in the weeks prior. This indicates that spinal networks controlling standing and locomotion and their interactions with sensory feedback from the limbs remain largely intact after complete spinal cord injury. We conclude that standing and locomotor recovery is due to the return of neuronal excitability within spinal sensorimotor circuits that do not require task-specific activity-dependent plasticity.

Data availability

A source data file has been provided with the article.

Article and author information

Author details

  1. Jonathan Harnie

    Department of Pharmacology-Physiology, Université de Sherbrooke, Sherbrooke, Canada
    Competing interests
    The authors declare that no competing interests exist.
  2. Adam Doelman

    Department of Pharmacology-Physiology, Université de Sherbrooke, Sherbrooke, Canada
    Competing interests
    The authors declare that no competing interests exist.
  3. Emmanuelle de Vette

    Department of Pharmacology-Physiology, Université de Sherbrooke, Sherbrooke, Canada
    Competing interests
    The authors declare that no competing interests exist.
  4. Johannie Audet

    Department of Pharmacology-Physiology, Université de Sherbrooke, Sherbrooke, Canada
    Competing interests
    The authors declare that no competing interests exist.
  5. Etienne Desrochers

    Department of Pharmacology-Physiology, Université de Sherbrooke, Sherbrooke, Canada
    Competing interests
    The authors declare that no competing interests exist.
  6. Nathalie Gaudreault

    School of Rehabilitation, Université de Sherbrooke, Sherbrooke, Canada
    Competing interests
    The authors declare that no competing interests exist.
  7. Alain Frigon

    Department of Pharmacology-Physiology, Université de Sherbrooke, Sherbrooke, Canada
    For correspondence
    Alain.Frigon@USherbrooke.ca
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-9259-2706

Funding

Canadian Institutes of Health Research (PJT-156296)

  • Alain Frigon

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 procedures were approved by the Animal Care Committee of the Université de Sherbrooke and were in accordance with policies and directives of the Canadian Council on Animal Care (Protocol 442-18). Twelve adult cats (> 1 year of age at time of experimentation), 5 males and 7 females, weighing between 3.6 kg and 4.7 kg were used in the present study. Our study followed the ARRIVE guidelines for animal studies (Kilkenny et al. 2010).

Reviewing Editor

  1. Jan-Marino Ramirez, Seattle Children's Research Institute, United States

Publication history

  1. Received: July 11, 2019
  2. Accepted: December 8, 2019
  3. Accepted Manuscript published: December 11, 2019 (version 1)
  4. Version of Record published: December 20, 2019 (version 2)

Copyright

© 2019, Harnie 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.

Metrics

  • 2,159
    Page views
  • 269
    Downloads
  • 8
    Citations

Article citation count generated by polling the highest count across the following sources: Crossref, PubMed Central, Scopus.

Download links

A two-part list of links to download the article, or parts of the article, in various formats.

Downloads (link to download the article as PDF)

Download citations (links to download the citations from this article in formats compatible with various reference manager tools)

Open citations (links to open the citations from this article in various online reference manager services)

Further reading

    1. Neuroscience
    Sahana Sitaraman et al.
    Research Article

    Gap junctions between neurons serve as electrical synapses, in addition to conducting metabolites and signaling molecules. During development, early-appearing gap junctions are thought to prefigure chemical synapses, which appear much later. We present evidence for this idea at a central, glutamatergic synapse and provide some mechanistic insights. Loss or reduction in the levels of the gap junction protein Gjd2b decreased the frequency of glutamatergic miniature excitatory postsynaptic currents (mEPSCs) in cerebellar Purkinje neurons (PNs) in larval zebrafish. Ultrastructural analysis in the molecular layer showed decreased synapse density. Further, mEPSCs had faster kinetics and larger amplitudes in mutant PNs, consistent with their stunted dendritic arbors. Time-lapse microscopy in wild type and mutant PNs reveals that Gjd2b puncta promote the elongation of branches and that CaMKII may be a critical mediator of this process. These results demonstrate that Gjd2b-mediated gap junctions regulate glutamatergic synapse formation and dendritic elaboration in PNs.

    1. Neuroscience
    Amicia D Elliott et al.
    Research Article Updated

    Identifying neural substrates of behavior requires defining actions in terms that map onto brain activity. Brain and muscle activity naturally correlate via the output of motor neurons, but apart from simple movements it has been difficult to define behavior in terms of muscle contractions. By mapping the musculature of the pupal fruit fly and comprehensively imaging muscle activation at single-cell resolution, we here describe a multiphasic behavioral sequence in Drosophila. Our characterization identifies a previously undescribed behavioral phase and permits extraction of major movements by a convolutional neural network. We deconstruct movements into a syllabary of co-active muscles and identify specific syllables that are sensitive to neuromodulatory manipulations. We find that muscle activity shows considerable variability, with sequential increases in stereotypy dependent upon neuromodulation. Our work provides a platform for studying whole-animal behavior, quantifying its variability across multiple spatiotemporal scales, and analyzing its neuromodulatory regulation at cellular resolution.