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.
Highlights
Dexterous motor behaviors require precise neural control of muscle contraction to coordinate force production and timing across dozens to hundreds of muscles
Subsequent work identified mechanisms associated with the recruitment order and synthesized these findings as the size principle, which states that small motor neurons, with lower spike thresholds, are recruited prior to larger neurons, which have higher spike thresholds
We recorded from several other motor neurons controlling tibia flexion, none of which had more extreme properties than the fast and slow movement, the whole-cell current clamp recording from the soma, and the EMG record from the leg; 3) shows video of individual trials from an intermediate neuron in which one or four spikes are driven with optogenetic stimulation in the ventral nerve cord (VNC); 4) shows video of a trial from a slow motor neuron in which current injection at the soma depolarizes the neuron and drives ~ 100 spikes, and a trial in which the slow neuron is hyperpolarized, reducing the force on the probe
Summary
Dexterous motor behaviors require precise neural control of muscle contraction to coordinate force production and timing across dozens to hundreds of muscles. The femur-tibia joint of a walking fly flexes and extends 10–20 times per second, reaching swing speeds of several thousand degrees per second (DeAngelis et al, 2019; Gowda et al, 2018; Mendes et al, 2013; Strauss and Heisenberg, 1990; Wosnitza et al, 2013) Flies use their legs to target other body parts during grooming (Hampel et al, 2015; Seeds et al, 2014), for social behaviors like aggression and courtship (Clowney et al, 2015; Hoopfer et al, 2015), and to initiate flight take-off (Card and Dickinson, 2008; Zumstein et al, 2004) and landing (Ache et al, 2019). In addition to the size principle, heterogeneous input from premotor circuits is likely to play an important role in coordinating neural activity within a motor pool
Sign-in/Register to view highlights & summary Sign-in/Register to access full text options 
Talk to us
Join us for a 30 min session where you can share your feedback and ask us any queries you have
Schedule a callDisclaimer: All third-party content on this website/platform is and will remain the property of their respective owners and is provided on "as is" basis without any warranties, express or implied. Use of third-party content does not indicate any affiliation, sponsorship with or endorsement by them. Any references to third-party content is to identify the corresponding services and shall be considered fair use under The CopyrightLaw.
