Spatiotemporal Organization of Neuronal Activity in the Cervical Cord of Behaving Primates

Oren Cohen,Ran Harel,Boris Rubinsky,Nofya Zinger,Yifat Prut,Yoel Sher

doi:10.3389/fnins.2010.00195

Abstract

Spinal neurons operate as a processing link that integrates descending and peripheral information and in turn, generates a specific yet complex muscle command. The functional organization of spinal circuitry during normal motor behavior dictates the way in which this translation process is achieved. Nonetheless, little is known about this organization during normal motor behavior. We examined the spatial organization of neural activity in the cervical spinal cord of behaving primates performing an isometric wrist task by estimating the averaged intraspinal activity of neuronal populations. We measured population response profiles and frequency content around torque onset and tested the tendency of these profiles to exhibit a specific organization within the spinal volume. We found that the spatial distribution of characteristic response profiles was non-uniform; namely, sites with a specific response profile tended to have a preferred spatial localization. Physiologically, this finding suggests that specific spinal circuitry that controls a unique feature of motor actions (with a particular task-related response pattern) may have a segregated spinal organization. Second, attempts to restore motor function via intraspinal stimulation may be more successful when the spatial distribution of these task-related profiles is taken into account.

Highlights

Spinal neurons are a critical element in integrating descending motor commands and converging peripheral inputs to generate a motor action (Baldissera et al, 1981)
This integration process is achieved via an extensive spinal network which includes different types of neuronal elements (Jankowska, 1992). While this network was shown to have a clear anatomical organization composed of laminas and segments, the functional organization of its elements during normal motor action is still under debate (Fetz et al, 2000)
K-means clustering analysis of torque-related population activity We processed the raw unit signal to generate a measure that corresponded to the multiunit activity (MUA) from the local vicinity of the electrodes (∼100–200 μm) (Asher et al, 2009)

Summary

Introduction

Spinal neurons are a critical element in integrating descending motor commands and converging peripheral inputs to generate a motor action (Baldissera et al, 1981). This integration process is achieved via an extensive spinal network which includes different types of neuronal elements (Jankowska, 1992). While this network was shown to have a clear anatomical organization composed of laminas (in the dorso-ventral axis) and segments (in the rostro-caudal axis), the functional organization of its elements during normal motor action is still under debate (Fetz et al, 2000). Further support for the existence of such functional modules in the spinal cord comes from experiments on cats (Alstermark et al, 1990, 1991; Pettersson et al, 1997, 2007; Alstermark and Ohlson, 2000; Mushahwar et al, 2002) and monkeys (Sasaki et al, 2004; Isa et al, 2006; Alstermark et al, 2007) and reveal an upper cervical set of neurons which may exert spinal control over reaching movements

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