Mechanosensory neurons control the timing of spinal microcircuit selection during locomotion.

Steven Knafo,Claire Wyart,Andrew Prendergast,Urs Lucas Böhm,Charles Dickey,Po-En Brian Tseng,Olivier Thouvenin,Sophie Nunes Figueiredo,Hugues Pascal-Moussellard,Kevin Fidelin,Alexandre Parrin

doi:10.7554/elife.25260

Abstract

Despite numerous physiological studies about reflexes in the spinal cord, the contribution of mechanosensory feedback to active locomotion and the nature of underlying spinal circuits remains elusive. Here we investigate how mechanosensory feedback shapes active locomotion in a genetic model organism exhibiting simple locomotion-the zebrafish larva. We show that mechanosensory feedback enhances the recruitment of motor pools during active locomotion. Furthermore, we demonstrate that inputs from mechanosensory neurons increase locomotor speed by prolonging fast swimming at the expense of slow swimming during stereotyped acoustic escape responses. This effect could be mediated by distinct mechanosensory neurons. In the spinal cord, we show that connections compatible with monosynaptic inputs from mechanosensory Rohon-Beard neurons onto ipsilateral V2a interneurons selectively recruited at high speed can contribute to the observed enhancement of speed. Altogether, our study reveals the basic principles and a circuit diagram enabling speed modulation by mechanosensory feedback in the vertebrate spinal cord.

Highlights

The generation of complex motor behaviors at a given speed relies on the sequential selection and orderly activation of groups of muscles by the nervous system (Bellardita and Kiehn, 2015)
To understand the contribution of mechanosensory feedback to speed control, we investigated the role of spinal mechanosensory neurons during acoustic escape responses in the zebrafish larva, a genetic model system with tractable locomotor behaviors that can be analyzed using fine kinematic analysis
In order to investigate the contribution of sensorimotor circuits during locomotor activity in zebrafish larvae, we used the bioluminescent calcium sensor GFP-Aequorin to monitor calcium activity emitted by identified neuronal populations in freely moving animals (Baubet et al, 2000; Naumann et al, 2010; Shimomura et al, 1962)

Summary

Introduction

The generation of complex motor behaviors at a given speed relies on the sequential selection and orderly activation of groups of muscles by the nervous system (Bellardita and Kiehn, 2015). At the level of locomotor circuits in the spinal cord, premotor excitatory V2a interneurons and motor neurons are recruited in a frequency-dependent manner (Crone et al, 2008; Kimura et al, 2006; McLean et al, 2007), a feature thought to underlie speed control in zebrafish (McLean et al, 2008). Circuit-mapping experiments revealed preferential connectivity profiles between identified groups of V2a interneurons and motor neurons suggesting that distinct microcircuit modules could regulate the mobilization of individual muscles during locomotion (Ampatzis et al, 2014; Bagnall and McLean, 2014). The nature of spinal circuits involved in motor pattern generation and speed control has mainly been studied during fictive locomotion when sensory feedback is absent (Kiehn, 2016; McLean and Dougherty, 2015). Less is known about the cellular and circuit mechanisms regulating the timing of microcircuit selection in the spinal cord during movement, which incorporate proprioceptive feedback from muscle contraction

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Conclusion