Regulation of locomotor speed and selection of active sets of neurons by V1 neurons

Yukiko Kimura,Shin-Ichi Higashijima

doi:10.1038/s41467-019-09871-x

Abstract

During fast movements in vertebrates, slow motor units are thought to be deactivated due to the mechanical demands of muscle contraction, but the associated neuronal mechanisms for this are unknown. Here, we perform functional analyses of spinal V1 neurons by selectively killing them in larval zebrafish, revealing two functions of V1 neurons. The first is the long-proposed role of V1 neurons: they play an important role in shortening the cycle period during swimming by providing in-phase inhibition. The second is that V1 neurons play an important role in the selection of active sets of neurons. We show that strong inhibitory inputs coming from V1 neurons play a crucial role in suppressing the activities of slow-type V2a and motor neurons, and, consequently, of slow muscles during fast swimming. Our results thus highlight the critical role of spinal inhibitory neurons for silencing slow-component neurons during fast movements.

Highlights

During fast movements in vertebrates, slow motor units are thought to be deactivated due to the mechanical demands of muscle contraction, but the associated neuronal mechanisms for this are unknown
In larval zebrafish and frog tadpoles, these neurons generally fire in phase with MNs located nearby during swimming and are proposed to provide in-phase inhibition to central pattern generators (CPGs) and motor neurons to help terminate the firing of the target neurons in each cycle during swimming[27,28]
We have revealed two functions of V1 neurons during swimming: the regulation of cycle frequency and the suppressing activities of slow components during fast/strong movements

Summary

Introduction

During fast movements in vertebrates, slow motor units are thought to be deactivated due to the mechanical demands of muscle contraction, but the associated neuronal mechanisms for this are unknown. We show that strong inhibitory inputs coming from V1 neurons play a crucial role in suppressing the activities of slow-type V2a and motor neurons, and, of slow muscles during fast swimming. In larval zebrafish and frog tadpoles, these neurons generally fire in phase with MNs located nearby during swimming and are proposed to provide in-phase inhibition to CPG and motor neurons to help terminate the firing of the target neurons in each cycle during swimming[27,28]. In this scheme, inactivation of V1 neurons would be expected to prolong firings of the CPG and motor neurons in each cycle and, prolong the cycle period. This kind of genetic inactivation of V1 neurons was performed in mice[30], which showed that the cycle period was prolonged during locomotor-like activities in V1-deficient neonatal mice

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