Long descending commissural V0v neurons ensure coordinated swimming movements along the body axis in larval zebrafish

Kohei Kawano,Kagayaki Kato,Takumi Sugioka,Shin-Ichi Higashijima,Yukiko Kimura,Masashi Tanimoto

doi:10.1038/s41598-022-08283-0

Abstract

Developmental maturation occurs in slow swimming behavior in larval zebrafish; older larvae acquire the ability to perform slow swimming while keeping their head stable in the yaw dimension. A class of long-distance descending commissural excitatory V0v neurons, called MCoD neurons, are known to develop in a later phase of neurogenesis, and participate in slow swimming in older larvae. We hypothesized that these MCoD neurons play a role in coordinating the activities of trunk muscles in the diagonal dimension (e.g., the rostral left and the caudal right) to produce the S-shaped swimming form that contributes to the stability of the head. Here, we show that MCoD neurons do indeed play this role. In larvae in which MCoD neurons were laser-ablated, the swimming body form often adopted a one-sided (C-shaped) bend with reduced appearance of the normal S-shaped bend. With this change in swimming form, the MCoD-ablated larvae exhibited a greater degree of head yaw displacement during slow swimming. In mice, the long-distance descending commissural V0v neurons have been implicated in diagonal interlimb coordination during walking. Together with this, our study suggests that the long-distance descending commissural V0v neurons form an evolutionarily conserved pathway in the spinal locomotor circuits that coordinates the movements of the diagonal body/limb muscles.

Highlights

In the early developmental stage, most animals can only exhibit immature forms of behaviors
Previous electrophysiological studies showed that MCoD neurons are rhythmically active during fictive slow swimming, and that the firing timings were generally in phase with nearby motor a ctivity[17,19]
A careful phase analysis has not yet been performed. We addressed this issue by performing loose-patch recordings of MCoD neurons together with motor-nerve recordings

Summary

Introduction

In the early developmental stage, most animals can only exhibit immature forms of behaviors. To make the net yawing moment force minimal, the movements of the rostral and caudal parts of the trunk need to be highly coordinated with the diagonal dimension; when the rostral part receives leftward force, for example, the caudal part needs to receive rightward force For this to occur, the swimming body form cannot be C-shaped (unilateral body bend); rather, the shape needs to be sinusoidal (S-shaped). MCoD neurons are a good candidate for implementing this coordinated movement of the trunk in the diagonal dimension, because they are active during slow swimming, and because they are long-distance descending commissural excitatory neurons that make direct connections onto MNs in the caudal region of the contralateral spinal cord[16,17] (Fig. 1B). We tested whether MCoD neurons play a role in the coordinated movements of the trunk in the diagonal dimension, thereby ensuring minimal head yaw displacement during slow swimming. We suggest that the long-distance descending commissural V0v neurons for the coordinated movements of the body/limbs in the diagonal dimension are the evolutionarily conserved pathway in spinal locomotor circuits

Methods

Results

Conclusion