Spontaneous neural synchrony links intrinsic spinal sensory and motor networks during unconsciousness

  1. Jacob Graves McPherson  Is a corresponding author
  2. Maria F Bandres
  1. Washington University School of Medicine, United States

Abstract

Non-random functional connectivity during unconsciousness is a defining feature of supraspinal networks. However, its generalizability to intrinsic spinal networks remains incompletely understood. Previously, Barry et al. (2014) used fMRI to reveal bilateral resting state functional connectivity within sensory-dominant and, separately, motor-dominant regions of the spinal cord. Here, we record spike trains from large populations of spinal interneurons in vivo in rats and demonstrate that spontaneous functional connectivity also links sensory- and motor-dominant regions during unconsciousness. The spatiotemporal patterns of connectivity could not be explained by latent afferent activity or by populations of interconnected neurons spiking randomly. We also document connection latencies compatible with mono- and di-synaptic interactions and putative excitatory and inhibitory connections. The observed activity is consistent with the hypothesis that salient, experience-dependent patterns of neural transmission introduced during behavior or by injury/disease are reactivated during unconsciousness. Such a spinal replay mechanism could shape circuit-level connectivity and ultimately behavior.

Data availability

All data analyzed for this study are included in the manuscript and supporting files, including raw data superimposed upon group data in images. Source data for Figs. 2,5,6,7, and 8, as well as detailed statistical tables, are also included as supporting files.

Article and author information

Author details

  1. Jacob Graves McPherson

    Physical Therapy, Anesthesiology, Washington University School of Medicine, St Louis, United States
    For correspondence
    mcpherson.jacob@wustl.edu
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-4554-7531
  2. Maria F Bandres

    Biomedical Engineering, Washington University School of Medicine, St Louis, United States
    Competing interests
    The authors declare that no competing interests exist.

Funding

National Institute of Neurological Disorders and Stroke (7R01NS111234-02)

  • Jacob Graves McPherson

Eunice Kennedy Shriver National Institute of Child Health and Human Development (K12HD073945)

  • Jacob Graves McPherson

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

Reviewing Editor

  1. Jeffrey C Smith, National Institute of Neurological Disorders and Stroke, United States

Ethics

Animal experimentation: This study was performed in accordance with the guidelines of the Institutional Animal Care and Usage Committees (IACUC) of Florida International University (FIU) and Washington University in St. Louis School of Medicine (WUSM). The studies were approved under IACUC protocols: 16-049 and 19-013 at FIU and 19-1052 at WUSM. All experiments were performed under deep, surgical grade anesthesia and animals were humanely euthanized in accordance with American Veterinary Medical Association Guidelines.

Version history

  1. Received: January 15, 2021
  2. Accepted: May 26, 2021
  3. Accepted Manuscript published: May 27, 2021 (version 1)
  4. Version of Record published: June 4, 2021 (version 2)

Copyright

© 2021, McPherson & Bandres

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. Jacob Graves McPherson
  2. Maria F Bandres
(2021)
Spontaneous neural synchrony links intrinsic spinal sensory and motor networks during unconsciousness
eLife 10:e66308.
https://doi.org/10.7554/eLife.66308

Share this article

https://doi.org/10.7554/eLife.66308

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