Distributed control of motor circuits for backward walking in Drosophila

Kai Feng,Michael Dübbert,Rajyashree Sen,Till Bockemühl,Ansgar Büschges,Barry J Dickson,Ryo Minegishi

doi:10.1038/s41467-020-19936-x

Abstract

How do descending inputs from the brain control leg motor circuits to change how an animal walks? Conceptually, descending neurons are thought to function either as command-type neurons, in which a single type of descending neuron exerts a high-level control to elicit a coordinated change in motor output, or through a population coding mechanism, whereby a group of neurons, each with local effects, act in combination to elicit a global motor response. The Drosophila Moonwalker Descending Neurons (MDNs), which alter leg motor circuit dynamics so that the fly walks backwards, exemplify the command-type mechanism. Here, we identify several dozen MDN target neurons within the leg motor circuits, and show that two of them mediate distinct and highly-specific changes in leg muscle activity during backward walking: LBL40 neurons provide the hindleg power stroke during stance phase; LUL130 neurons lift the legs at the end of stance to initiate swing. Through these two effector neurons, MDN directly controls both the stance and swing phases of the backward stepping cycle. These findings suggest that command-type descending neurons can also operate through the distributed control of local motor circuits.

Highlights

How do descending inputs from the brain control leg motor circuits to change how an animal walks? Conceptually, descending neurons are thought to function either as command-type neurons, in which a single type of descending neuron exerts a high-level control to elicit a coordinated change in motor output, or through a population coding mechanism, whereby a group of neurons, each with local effects, act in combination to elicit a global motor response
Backward walking triggered by the Moonwalker Descending Neurons (MDNs) is an excellent model for exploring how descending command-like neurons produce abrupt but coordinated changes in motor circuit output
The data presented here indicate that MDN acts primarily on the T3 motor circuits, such that the hindlegs become the major driving force in backward walking

Summary

Introduction

How do descending inputs from the brain control leg motor circuits to change how an animal walks? Conceptually, descending neurons are thought to function either as command-type neurons, in which a single type of descending neuron exerts a high-level control to elicit a coordinated change in motor output, or through a population coding mechanism, whereby a group of neurons, each with local effects, act in combination to elicit a global motor response. We identify several dozen MDN target neurons within the leg motor circuits, and show that two of them mediate distinct and highly-specific changes in leg muscle activity during backward walking: LBL40 neurons provide the hindleg power stroke during stance phase; LUL130 neurons lift the legs at the end of stance to initiate swing Through these two effector neurons, MDN directly controls both the stance and swing phases of the backward stepping cycle. The descending inputs modulate the overall locomotor pattern, effecting changes in direction or pace in accordance with the animal’s behavioral goals[3,4] Sensory feedback, including both external and proprioceptive signals, coordinate progression through the stepping cycle and make the fine adjustments needed to adapt to a varying terrain[5]. While some progress has been made in identifying the larval motor circuits that the MDNs engage for backward crawling[14], the motor circuits they activate in the adult for backward walking remain unknown

Methods

Results

Conclusion