Intrinsic functional architecture of the non-human primate spinal cord derived from fMRI and electrophysiology

Tung-Lin Wu,Ruiqi Wu,Li Min Chen,Arabinda Mishra,John C Gore,Pai-Feng Yang,Zhaoyue Shi,Feng Wang

doi:10.1038/s41467-019-09485-3

Tung-Lin Wu, Ruiqi Wu + Show 6 more

Open Access

https://doi.org/10.1038/s41467-019-09485-3

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Abstract

Resting-state functional MRI (rsfMRI) has recently revealed correlated signals in the spinal cord horns of monkeys and humans. However, the interpretation of these rsfMRI correlations as indicators of functional connectivity in the spinal cord remains unclear. Here, we recorded stimulus-evoked and spontaneous spiking activity and local field potentials (LFPs) from monkey spinal cord in order to validate fMRI measures. We found that both BOLD and electrophysiological signals elicited by tactile stimulation co-localized to the ipsilateral dorsal horn. Temporal profiles of stimulus-evoked BOLD signals covaried with LFP and multiunit spiking in a similar way to those observed in the brain. Functional connectivity of dorsal horns exhibited a U-shaped profile along the dorsal-intermediate-ventral axis. Overall, these results suggest that there is an intrinsic functional architecture within the gray matter of a single spinal segment, and that rsfMRI signals at high field directly reflect this underlying spontaneous neuronal activity.

Highlights

Resting-state functional MRI has recently revealed correlated signals in the spinal cord horns of monkeys and humans
Altered resting-state functional connectivity under different pathological conditions suggests that these correlations reflect intrinsic neural processes that are relevant for maintaining normal brain functions[6]
The current study aims to address three key questions: (1) what are the intrinsic functional organization features of the spinal gray matter, (2) what is the relationship between changes in stimulus-evoked fMRI signals and the underlying neural electrical activity (local field potentials (LFPs) and multiunit activity (MUA)), and (3) do correlations in rsfMRI signal fluctuations reflect the underlying synchronous variations in spontaneous neural electrophysiological activity within the spinal gray matter from the same regions

Summary

Introduction

Resting-state functional MRI (rsfMRI) has recently revealed correlated signals in the spinal cord horns of monkeys and humans. Recent technical advances have allowed robust detection of strong, rsFC between spinal horns in animal models as well as human subjects[7,8,10,13,15,16,18] These observations have led several research groups to hypothesize that, like the brain, spinal cord gray matter exhibits its own intrinsic functional architecture that serves as a fundamental framework for executing and maintaining sensory, motor, and autonomic functions. The current study aims to address three key questions: (1) what are the intrinsic functional organization features of the spinal gray matter, (2) what is the relationship between changes in stimulus-evoked fMRI signals and the underlying neural electrical activity (local field potentials (LFPs) and multiunit activity (MUA)), and (3) do correlations in rsfMRI signal fluctuations (indicators of resting state FC) reflect the underlying synchronous variations in spontaneous neural electrophysiological activity within the spinal gray matter from the same regions. We propose that this will provide a foundation for using fMRI for assessing and monitoring alterations in spinal cord circuits that occur with injury and other pathologies

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