A size principle for recruitment of Drosophila leg motor neurons

  1. Anthony W Azevedo
  2. Evyn S Dickinson
  3. Pralaksha Gurung
  4. Lalanti Venkatasubramanian
  5. Richard S Mann
  6. John C Tuthill  Is a corresponding author
  1. University of Washington, United States
  2. Columbia University, United States

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.

Data availability

All data is publicly available on Dryad doi:10.5061/dryad.76hdr7stb

The following data sets were generated

Article and author information

Author details

  1. Anthony W Azevedo

    Department of Physiology and Biophysics, University of Washington, Seattle, United States
    Competing interests
    The authors declare that no competing interests exist.
  2. Evyn S Dickinson

    Dept of Physiology and Biophysics, University of Washington, Seattle, United States
    Competing interests
    The authors declare that no competing interests exist.
  3. Pralaksha Gurung

    Dept of Physiology and Biophysics, University of Washington, Seattle, United States
    Competing interests
    The authors declare that no competing interests exist.
  4. Lalanti Venkatasubramanian

    Department of Biochemistry and Molecular Biophysics, Columbia University, New York, United States
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-9280-8335
  5. Richard S Mann

    Department of Biochemistry and Molecular Biophysics, Columbia University, New York, United States
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-4749-2765
  6. John C Tuthill

    Dept of Physiology and Biophysics, University of Washington, Seattle, United States
    For correspondence
    johnctuthill@gmail.com
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-5689-5806

Funding

NIH (U19NS104655)

  • Anthony W Azevedo
  • Evyn S Dickinson
  • Pralaksha Gurung
  • Lalanti Venkatasubramanian
  • Richard S Mann
  • John C Tuthill

Searle Foundation (Scholar Award)

  • Anthony W Azevedo
  • Evyn S Dickinson
  • Pralaksha Gurung
  • John C Tuthill

McKnight Foundation (Scholar Award)

  • Anthony W Azevedo
  • Evyn S Dickinson
  • Pralaksha Gurung
  • John C Tuthill

Pew Biomedical Trust (Scholar Award)

  • Anthony W Azevedo
  • Evyn S Dickinson
  • Pralaksha Gurung
  • John C Tuthill

Sloan Foundation (Research Fellowship)

  • Anthony W Azevedo
  • Evyn S Dickinson
  • Pralaksha Gurung
  • John C Tuthill

The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.

Copyright

© 2020, Azevedo et al.

This article is distributed under the terms of the Creative Commons Attribution License permitting unrestricted use and redistribution provided that the original author and source are credited.

Metrics

  • 5,674
    views
  • 618
    downloads
  • 59
    citations

Views, downloads and citations are aggregated across all versions of this paper published by eLife.

Download links

A two-part list of links to download the article, or parts of the article, in various formats.

Downloads (link to download the article as PDF)

Open citations (links to open the citations from this article in various online reference manager services)

Cite this article (links to download the citations from this article in formats compatible with various reference manager tools)

  1. Anthony W Azevedo
  2. Evyn S Dickinson
  3. Pralaksha Gurung
  4. Lalanti Venkatasubramanian
  5. Richard S Mann
  6. John C Tuthill
(2020)
A size principle for recruitment of Drosophila leg motor neurons
eLife 9:e56754.
https://doi.org/10.7554/eLife.56754

Share this article

https://doi.org/10.7554/eLife.56754

Further reading

    1. Neuroscience
    William Hockeimer, Ruo-Yah Lai ... James J Knierim
    Research Article

    The hippocampus is believed to encode episodic memory by binding information about the content of experience within a spatiotemporal framework encoding the location and temporal context of that experience. Previous work implies a distinction between positional inputs to the hippocampus from upstream brain regions that provide information about an animal’s location and nonpositional inputs which provide information about the content of experience, both sensory and navigational. Here, we leverage the phenomenon of ‘place field repetition’ to better understand the functional dissociation between positional and nonpositional information encoded in CA1. Rats navigated freely on a novel maze consisting of linear segments arranged in a rectilinear, city-block configuration, which combined elements of open-field foraging and linear-track tasks. Unlike typical results in open-field foraging, place fields were directionally tuned on the maze, even though the animal’s behavior was not constrained to extended, one-dimensional (1D) trajectories. Repeating fields from the same cell tended to have the same directional preference when the fields were aligned along a linear corridor of the maze, but they showed uncorrelated directional preferences when they were unaligned across different corridors. Lastly, individual fields displayed complex time dynamics which resulted in the population activity changing gradually over the course of minutes. These temporal dynamics were evident across repeating fields of the same cell. These results demonstrate that the positional inputs that drive a cell to fire in similar locations across the maze can be behaviorally and temporally dissociated from the nonpositional inputs that alter the firing rates of the cell within its place fields, offering a potential mechanism to increase the flexibility of the system to encode episodic variables within a spatiotemporal framework provided by place cells.

    1. Neuroscience
    Patricia E Phelps, Sung Min Ha ... Xia Yang
    Research Article

    Olfactory ensheathing cells (OECs) are unique glial cells found in both central and peripheral nervous systems where they support continuous axonal outgrowth of olfactory sensory neurons to their targets. Previously, we reported that following severe spinal cord injury, OECs transplanted near the injury site modify the inhibitory glial scar and facilitate axon regeneration past the scar border and into the lesion. To better understand the mechanisms underlying the reparative properties of OECs, we used single-cell RNA-sequencing of OECs from adult rats to study their gene expression programs. Our analyses revealed five diverse OEC subtypes, each expressing novel marker genes and pathways indicative of progenitor, axonal regeneration, secreted molecules, or microglia-like functions. We found substantial overlap of OEC genes with those of Schwann cells, but also with microglia, astrocytes, and oligodendrocytes. We confirmed established markers on cultured OECs, and localized select top genes of OEC subtypes in olfactory bulb tissue. We also show that OECs secrete Reelin and Connective tissue growth factor, extracellular matrix molecules which are important for neural repair and axonal outgrowth. Our results support that OECs are a unique hybrid glia, some with progenitor characteristics, and that their gene expression patterns indicate functions related to wound healing, injury repair, and axonal regeneration.