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

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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

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.

"This ORCID iD identifies the author of this article:" 0000-0002-4554-7531
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.

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.

Copyright

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.