Sub-populations of Spinal V3 Interneurons Form Focal Modules of Layered Pre-motor Microcircuits

Jeremy W Chopek,Filipe Nascimento,Marco Beato,Robert M Brownstone,Ying Zhang

doi:10.1016/j.celrep.2018.08.095

Jeremy W Chopek, Filipe Nascimento + Show 3 more

Open Access

https://doi.org/10.1016/j.celrep.2018.08.095

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Journal: Cell Reports	Publication Date: Oct 1, 2018
Citations: 79	License type: cc-by

Affiliation: Dalhousie University, University College London

Abstract

SummaryLayering of neural circuits facilitates the separation of neurons with high spatial sensitivity from those that play integrative temporal roles. Although anatomical layers are readily identifiable in the brain, layering is not structurally obvious in the spinal cord. But computational studies of motor behaviors have led to the concept of layered processing in the spinal cord. It has been postulated that spinal V3 interneurons (INs) play multiple roles in locomotion, leading us to investigate whether they form layered microcircuits. Using patch-clamp recordings in combination with holographic glutamate uncaging, we demonstrate focal, layered modules, in which ventromedial V3 INs form synapses with one another and with ventrolateral V3 INs, which in turn form synapses with ipsilateral motoneurons. Motoneurons, in turn, provide recurrent excitatory, glutamatergic input to V3 INs. Thus, ventral V3 interneurons form layered microcircuits that could function to ensure well-timed, spatially specific movements.

Highlights

Over the course of evolution, nervous systems developed neuronal layers for information processing
Using whole-cell patch-clamp recordings in combination with holographic glutamate uncaging, we demonstrate focal layers of neuronal connectivity between two ventral V3 IN sub-populations and ipsilateral MNs in the lateral motor column
Consistent with previous findings (Lutz et al, 2008; Zahid et al, 2010), the amplitudes of the responses were related to both the size and duration of photostimulation

Summary

Introduction

Over the course of evolution, nervous systems developed neuronal layers for information processing. This is perhaps most evident in the primate cerebral and cerebellar cortices, in which structural layers can be beautifully visualized. These structural layers likely evolved for geometric reasons, in particular for economies of wiring (Shipp, 2007), functional layers appeared even in the absence of structure. In the pallium, layered processing, which likely confers staged processing capabilities, appeared hundreds of millions of years ago, much earlier than structural layers (Calabrese and Woolley, 2015). The spinal cord predates the pallium, and models of spinal circuits for locomotion routinely implicate a layered organization as being necessary for the flexibility of motor rhythms and patterns (e.g., Danner et al, 2017; Lafreniere-Roula and McCrea, 2005)

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