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

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.

Metrics

  • 3,055
    views
  • 336
    downloads
  • 26
    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. 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

Further reading

    1. Medicine
    2. Neuroscience
    Chi Zhang, Qian Huang ... Yun Guan
    Research Article

    Pain after surgery causes significant suffering. Opioid analgesics cause severe side effects and accidental death. Therefore, there is an urgent need to develop non-opioid therapies for managing post-surgical pain. Local application of Clarix Flo (FLO), a human amniotic membrane (AM) product, attenuated established post-surgical pain hypersensitivity without exhibiting known side effects of opioid use in mice. This effect was achieved through direct inhibition of nociceptive dorsal root ganglion (DRG) neurons via CD44-dependent pathways. We further purified the major matrix component, the heavy chain-hyaluronic acid/pentraxin 3 (HC-HA/PTX3) from human AM that has greater purity and water solubility than FLO. HC-HA/PTX3 replicated FLO-induced neuronal and pain inhibition. Mechanistically, HC-HA/PTX3-induced cytoskeleton rearrangements to inhibit sodium current and high-voltage activated calcium current on nociceptive DRG neurons, suggesting it is a key bioactive component mediating pain relief. Collectively, our findings highlight the potential of naturally derived biologics from human birth tissues as an effective non-opioid treatment for post-surgical pain. Moreover, we unravel the underlying neuronal mechanisms of pain inhibition induced by FLO and HC-HA/PTX3.

    1. Computational and Systems Biology
    2. Neuroscience
    Jian Qiu, Margaritis Voliotis ... Martin J Kelly
    Research Article

    Hypothalamic kisspeptin (Kiss1) neurons are vital for pubertal development and reproduction. Arcuate nucleus Kiss1 (Kiss1ARH) neurons are responsible for the pulsatile release of gonadotropin-releasing hormone (GnRH). In females, the behavior of Kiss1ARH neurons, expressing Kiss1, neurokinin B (NKB), and dynorphin (Dyn), varies throughout the ovarian cycle. Studies indicate that 17β-estradiol (E2) reduces peptide expression but increases Slc17a6 (Vglut2) mRNA and glutamate neurotransmission in these neurons, suggesting a shift from peptidergic to glutamatergic signaling. To investigate this shift, we combined transcriptomics, electrophysiology, and mathematical modeling. Our results demonstrate that E2 treatment upregulates the mRNA expression of voltage-activated calcium channels, elevating the whole-cell calcium current that contributes to high-frequency burst firing. Additionally, E2 treatment decreased the mRNA levels of canonical transient receptor potential (TPRC) 5 and G protein-coupled K+ (GIRK) channels. When Trpc5 channels in Kiss1ARH neurons were deleted using CRISPR/SaCas9, the slow excitatory postsynaptic potential was eliminated. Our data enabled us to formulate a biophysically realistic mathematical model of Kiss1ARH neurons, suggesting that E2 modifies ionic conductances in these neurons, enabling the transition from high-frequency synchronous firing through NKB-driven activation of TRPC5 channels to a short bursting mode facilitating glutamate release. In a low E2 milieu, synchronous firing of Kiss1ARH neurons drives pulsatile release of GnRH, while the transition to burst firing with high, preovulatory levels of E2 would facilitate the GnRH surge through its glutamatergic synaptic connection to preoptic Kiss1 neurons.