1. Neuroscience
Download icon

Central processing of leg proprioception in Drosophila

  1. Sweta Agrawal
  2. Evyn S Dickinson
  3. Anne Sustar
  4. Pralaksha Gurung
  5. David Shepherd
  6. James W Truman
  7. John C Tuthill  Is a corresponding author
  1. University of Washington, United States
  2. Bangor University, United Kingdom
  3. Janelia Research Campus, Howard Hughes Medical Institute, United States
Research Article
  • Cited 5
  • Views 1,605
  • Annotations
Cite this article as: eLife 2020;9:e60299 doi: 10.7554/eLife.60299

Abstract

Proprioception, the sense of self-movement and position, is mediated by mechanosensory neurons that detect diverse features of body kinematics. Although proprioceptive feedback is crucial for accurate motor control, little is known about how downstream circuits transform limb sensory information to guide motor output. Here, we investigate neural circuits in Drosophila that process proprioceptive information from the fly leg. We identify three cell-types from distinct developmental lineages that are positioned to receive input from proprioceptor subtypes encoding tibia position, movement, and vibration. 13Bα neurons encode femur-tibia joint angle and mediate postural changes in tibia position. 9Aα neurons also drive changes in leg posture, but encode a combination of directional movement, high frequency vibration, and joint angle. Activating 10Bα neurons, which encode tibia vibration at specific joint angles, elicits pausing in walking flies. Altogether, our results reveal that central circuits integrate information across proprioceptor subtypes to construct complex sensorimotor representations that mediate diverse behaviors, including reflexive control of limb posture and detection of leg vibration.

Data availability

Data made freely available on Dryad (doi:10.5061/dryad.k3j9kd55t).

The following data sets were generated

Article and author information

Author details

  1. Sweta Agrawal

    Dept 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.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-7518-9512
  3. Anne Sustar

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

    Dept of Physiology and Biophysics, University of Washington, Seattle, United States
    Competing interests
    The authors declare that no competing interests exist.
  5. David Shepherd

    School of Natural Sciences, Bangor University, Bangor, United Kingdom
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-6961-7880
  6. James W Truman

    Janelia Research Campus, Howard Hughes Medical Institute, Ashburn, United States
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-9209-5435
  7. 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

National Institutes of Health (R01NS102333)

  • Sweta Agrawal
  • Evyn S Dickinson
  • Anne Sustar
  • Pralaksha Gurung
  • John C Tuthill

Howard Hughes Medical Institute

  • David Shepherd
  • James W Truman

Pew Charitable Trusts (Scholar Award)

  • Sweta Agrawal
  • Evyn S Dickinson
  • Anne Sustar
  • Pralaksha Gurung
  • John C Tuthill

Searle Scholars Program (Scholar Award)

  • Sweta Agrawal
  • Evyn S Dickinson
  • Anne Sustar
  • Pralaksha Gurung
  • John C Tuthill

Alfred P. Sloan Foundation (Scholar Award)

  • Sweta Agrawal
  • Evyn S Dickinson
  • Anne Sustar
  • Pralaksha Gurung
  • John C Tuthill

McKnight Endowment Fund for Neuroscience (Scholar Award)

  • Sweta Agrawal
  • Evyn S Dickinson
  • Anne Sustar
  • 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.

Reviewing Editor

  1. Ronald L Calabrese, Emory University, United States

Publication history

  1. Received: June 22, 2020
  2. Accepted: December 1, 2020
  3. Accepted Manuscript published: December 2, 2020 (version 1)
  4. Version of Record published: December 21, 2020 (version 2)

Copyright

© 2020, Agrawal 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

  • 1,605
    Page views
  • 240
    Downloads
  • 5
    Citations

Article citation count generated by polling the highest count across the following sources: Crossref, PubMed Central, Scopus.

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)

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

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

Further reading

    1. Cell Biology
    2. Neuroscience
    Rene Solano Fonseca et al.
    Research Article Updated

    Concussion is associated with a myriad of deleterious immediate and long-term consequences. Yet the molecular mechanisms and genetic targets promoting the selective vulnerability of different neural subtypes to dysfunction and degeneration remain unclear. Translating experimental models of blunt force trauma in C. elegans to concussion in mice, we identify a conserved neuroprotective mechanism in which reduction of mitochondrial electron flux through complex IV suppresses trauma-induced degeneration of the highly vulnerable dopaminergic neurons. Reducing cytochrome C oxidase function elevates mitochondrial-derived reactive oxygen species, which signal through the cytosolic hypoxia inducing transcription factor, Hif1a, to promote hyperphosphorylation and inactivation of the pyruvate dehydrogenase, PDHE1α. This critical enzyme initiates the Warburg shunt, which drives energetic reallocation from mitochondrial respiration to astrocyte-mediated glycolysis in a neuroprotective manner. These studies demonstrate a conserved process in which glycolytic preconditioning suppresses Parkinson-like hypersensitivity of dopaminergic neurons to trauma-induced degeneration via redox signaling and the Warburg effect.

    1. Biochemistry and Chemical Biology
    2. Neuroscience
    Lloyd Davis et al.
    Tools and Resources Updated

    Synthetic strategies for optically controlling gene expression may enable the precise spatiotemporal control of genes in any combination of cells that cannot be targeted with specific promoters. We develop an improved genetic code expansion system in Caenorhabditis elegans and use it to create a photoactivatable Cre recombinase. We laser-activate Cre in single neurons within a bilaterally symmetric pair to selectively switch on expression of a loxP-controlled optogenetic channel in the targeted neuron. We use the system to dissect, in freely moving animals, the individual contributions of the mechanosensory neurons PLML/PLMR to the C. elegans touch response circuit, revealing distinct and synergistic roles for these neurons. We thus demonstrate how genetic code expansion and optical targeting can be combined to break the symmetry of neuron pairs and dissect behavioural outputs of individual neurons that cannot be genetically targeted.