Regulation of coordinated muscular relaxation in Drosophila larvae by a pattern-regulating intersegmental circuit

Atsuki Hiramoto,Hiroshi Kohsaka,Julius Jonaitis,Albert Cardona,Akinao Nose,Richard D Fetter,Stefan R Pulver,Sawako Niki

doi:10.1038/s41467-021-23273-y

Abstract

Typical patterned movements in animals are achieved through combinations of contraction and delayed relaxation of groups of muscles. However, how intersegmentally coordinated patterns of muscular relaxation are regulated by the neural circuits remains poorly understood. Here, we identify Canon, a class of higher-order premotor interneurons, that regulates muscular relaxation during backward locomotion of Drosophila larvae. Canon neurons are cholinergic interneurons present in each abdominal neuromere and show wave-like activity during fictive backward locomotion. Optogenetic activation of Canon neurons induces relaxation of body wall muscles, whereas inhibition of these neurons disrupts timely muscle relaxation. Canon neurons provide excitatory outputs to inhibitory premotor interneurons. Canon neurons also connect with each other to form an intersegmental circuit and regulate their own wave-like activities. Thus, our results demonstrate how coordinated muscle relaxation can be realized by an intersegmental circuit that regulates its own patterned activity and sequentially terminates motor activities along the anterior-posterior axis.

Highlights

Typical patterned movements in animals are achieved through combinations of contraction and delayed relaxation of groups of muscles
Our study identified a class of premotor interneurons, the consisting of a second-order excitatory premotor interneuron (Canon) neurons, that regulate muscular relaxation, and revealed their cellular-level circuit structure, including the upstream backward command neurons and downstream inhibitory premotor circuits extending from the brain to the muscles
Our results suggest that the Canon–Canon network is important, as an actuator of muscular relaxation in each segment, and as the pattern regulator of its own propagating activity during backward locomotion

Summary

Introduction

Typical patterned movements in animals are achieved through combinations of contraction and delayed relaxation of groups of muscles. Recent studies identified several classes of premotor interneurons that regulate various aspects of larval peristaltic locomotion, including speed of peristaltic propagation, left–right coordination, and sequential contraction of antagonistic muscles[5,24,25,26]. One such class, the period-positive median segmental interneurons (PMSIs) are activated later than their target MNs and regulate the duration of MN activities, and could potentially play roles in the regulation of muscle relaxation. Our results demonstrate how coordinated muscle relaxation can be regulated by the action of a pattern-regulating intersegmental circuit

Methods

Results

Conclusion