1. Neuroscience

Distinct subpopulations of mechanosensory chordotonal organ neurons elicit grooming of the fruit fly antennae

  1. Stefanie Hampel  Is a corresponding author
  2. Katharina Eichler
  3. Daichi Yamada
  4. Davi Bock
  5. Azusa Kamikouchi
  6. Andrew M Seeds  Is a corresponding author
  1. University of Puerto Rico Medical Sciences Campus, Puerto Rico
  2. Nagoya University, Japan
  3. University of Vermont, United States
https://doi.org/10.7554/eLife.59976
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  1. Stefanie Hampel
  2. Katharina Eichler
  3. Daichi Yamada
  4. Davi Bock
  5. Azusa Kamikouchi
  6. Andrew M Seeds
(2020)
Distinct subpopulations of mechanosensory chordotonal organ neurons elicit grooming of the fruit fly antennae
eLife 9:e59976.
https://doi.org/10.7554/eLife.59976
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Abstract

Diverse mechanosensory neurons detect different mechanical forces that can impact animal behavior. Yet our understanding of the anatomical and physiological diversity of these neurons and the behaviors that they influence is limited. We previously discovered that grooming of the Drosophila melanogaster antennae is elicited by an antennal mechanosensory chordotonal organ, the Johnston's organ (JO) (Hampel et al., 2015). Here, we describe anatomically and physiologically distinct JO mechanosensory neuron subpopulations that each elicit antennal grooming. We show that the subpopulations project to different, discrete zones in the brain and differ in their responses to mechanical stimulation of the antennae. Although activation of each subpopulation elicits antennal grooming, distinct subpopulations also elicit the additional behaviors of wing flapping or backward locomotion. Our results provide a comprehensive description of the diversity of mechanosensory neurons in the JO, and reveal that distinct JO subpopulations can elicit both common and distinct behavioral responses.

Data availability

Neuron reconstructions will be made available on https://v2.virtualflybrain.org/

The following previously published data sets were used

Article and author information

Author details

  1. Stefanie Hampel

    Institute of Neurobiology, University of Puerto Rico Medical Sciences Campus, San Juan, Puerto Rico
    For correspondence
    stef.hampel@gmail.com
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-8287-549X

  2. Katharina Eichler

    Institute of Neurobiology, University of Puerto Rico Medical Sciences Campus, San Juan, Puerto Rico
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-7833-8621

  3. Daichi Yamada

    Division of Biological Science, Nagoya University, Nagoya, Japan
    Competing interests
    The authors declare that no competing interests exist.

  4. Davi Bock

    Department of Neurological Sciences, Larner College of Medicine, University of Vermont, Burlington, United States
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-8218-7926

  5. Azusa Kamikouchi

    Graduate School of Science, Nagoya University, Nagoya, Japan
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-1552-6892

  6. Andrew M Seeds

    Institute of Neurobiology, University of Puerto Rico Medical Sciences Campus, San Juan, Puerto Rico
    For correspondence
    seeds.andrew@gmail.com
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-4932-6496

Funding

Whitehall Foundation (2017-12-69)

  • Andrew M Seeds

National Institute on Minority Health and Health Disparities (MD007600)

  • Andrew M Seeds

National Institute of General Medical Sciences (GM103642)

  • Stefanie Hampel
  • Andrew M Seeds

Puerto Rico Science, Technology and Research Trust (2020-00195)

  • Andrew M Seeds

National Science Foundation (HRD-1736019)

  • Andrew M Seeds

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

Copyright

© 2020, Hampel 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.

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  1. Stefanie Hampel
  2. Katharina Eichler
  3. Daichi Yamada
  4. Davi Bock
  5. Azusa Kamikouchi
  6. Andrew M Seeds
(2020)
Distinct subpopulations of mechanosensory chordotonal organ neurons elicit grooming of the fruit fly antennae
eLife 9:e59976.
https://doi.org/10.7554/eLife.59976

Share this article

https://doi.org/10.7554/eLife.59976

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Further reading

    1. Neuroscience

    A neural command circuit for grooming movement control

    Stefanie Hampel, Romain Franconville ... Andrew M Seeds
    Research Article Updated

    Animals perform many stereotyped movements, but how nervous systems are organized for controlling specific movements remains unclear. Here we use anatomical, optogenetic, behavioral, and physiological techniques to identify a circuit in Drosophila melanogaster that can elicit stereotyped leg movements that groom the antennae. Mechanosensory chordotonal neurons detect displacements of the antennae and excite three different classes of functionally connected interneurons, which include two classes of brain interneurons and different parallel descending neurons. This multilayered circuit is organized such that neurons within each layer are sufficient to specifically elicit antennal grooming. However, we find differences in the durations of antennal grooming elicited by neurons in the different layers, suggesting that the circuit is organized to both command antennal grooming and control its duration. As similar features underlie stimulus-induced movements in other animals, we infer the possibility of a common circuit organization for movement control that can be dissected in Drosophila.