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 disynaptic 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.

Highlights

  • Synchronous neural activity across functionally and spatially distinct brain structures, i.e., functional connectivity, is a hallmark of sensorimotor integration, cognition, and behavior during periods of attentive wakefulness

  • We found that connections within the deep dorsal horn (dDH), within the intermediate gray (IG), and within the ventral horn (VH) contained the highest proportion of putative inhibitory connections (22.7±5.3%, 24.1±7.3%, 37.8±9.0%, respectively), with the dDH containing the highest proportion of excitatory connections

  • Functional neural transmission during unconsciousness involves patterned activity within local and regional circuits as well as communication between functionally and spatially distributed neural structures.(Demertzi et al, 2019; Fox et al, 2005; Greicius et al, 2003; Mashour and Hudetz, 2018; Raichle et al, 2001; Steriade et al, 1993; Wenzel et al, 2019) we reasoned that persistence of correlated discharge at multiple spatial scales would be a necessary precondition for intrinsic spinal networks to maintain functionality during unconsciousness

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Summary

Introduction

Synchronous neural activity across functionally and spatially distinct brain structures, i.e., functional connectivity, is a hallmark of sensorimotor integration, cognition, and behavior during periods of attentive wakefulness. Recent elucidation of brain networks intrinsically active during unconsciousness and inattentive wakefulness has led to a substantially more nuanced view of brain function(Demertzi et al., 2019; Fox et al, 2005; Greicius et al, 2003; Mashour and Hudetz, 2018; Raichle et al, 2001; Steriade et al, 1993; Wenzel et al, 2019). The finding of spontaneous, non-random network activity during unconsciousness appears to be robust across different functional regions of the brain, it has yet to be unequivocally confirmed whether this phenomenon is a conserved feature of complex neural systems that generalizes to the spinal cord. The most reliable findings to-date have been correlations between spontaneous

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