A size principle for recruitment of Drosophila leg motor neurons.

Abstract:

:To move the body, the brain must precisely coordinate patterns of activity among diverse populations of motor neurons. Here, we use in vivo calcium imaging, electrophysiology, and behavior to understand how genetically-identified motor neurons control flexion of the fruit fly tibia. We find that leg motor neurons exhibit a coordinated gradient of anatomical, physiological, and functional properties. Large, fast motor neurons control high force, ballistic movements while small, slow motor neurons control low force, postural movements. Intermediate neurons fall between these two extremes. This hierarchical organization resembles the size principle, first proposed as a mechanism for establishing recruitment order among vertebrate motor neurons. Recordings in behaving flies confirmed that motor neurons are typically recruited in order from slow to fast. However, we also find that fast, intermediate, and slow motor neurons receive distinct proprioceptive feedback signals, suggesting that the size principle is not the only mechanism that dictates motor neuron recruitment. Overall, this work reveals the functional organization of the fly leg motor system and establishes Drosophila as a tractable system for investigating neural mechanisms of limb motor control. :In the body, spindly nerve cells called motor neurons connect the brain to the muscles. Their role is to control movement, as they translate the electrical signals from the brain into instructions to the muscles. In humans, it takes over 150,000 motor neurons to control the movement of one leg; in contrast, fruit flies only need 50 neurons to operate a leg, despite also executing a variety of movements. Fruit flies are commonly used in laboratories to study an array of biological processes, yet little is known about how their motor neurons direct movements. In particular, it was unclear whether the same principles that control how muscles contract in mammals also applied in the tiny fruit fly. To begin investigating, Azevedo et al. mapped out the arrangement of motor neurons that control muscles in the fruit fly leg. As the leg moved, the activity of both the neurons and the muscles they controlled was recorded, as well as the force that had been generated. The experiments showed that each motor neuron controls a certain range of leg force and speed: some produced small, slow motion important for posture and dexterity, while others created large, fast movements essential to running or escape. In addition, the neurons activate in a particular order – cells that control slow movements fire first, and those that direct fast maneuvers later. These processes are also found in other organisms, but the difference is that flies have so few neurons, allowing scientists to reliably identify each motor neuron. Future experiments will therefore be able to test how flies recruit the right neurons to create specific movement sequences. Fruit flies are often used to research human illnesses that affect movement, such as motor neuron disease. A better understanding of the way their neural circuits coordinate the body could help reveal how these conditions emerge.

journal_name

Elife

journal_title

eLife

authors

Azevedo AW,Dickinson ES,Gurung P,Venkatasubramanian L,Mann RS,Tuthill JC

doi

10.7554/eLife.56754

subject

Has Abstract

pub_date

2020-06-03 00:00:00

issn

2050-084X

pii

56754

journal_volume

9

pub_type

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