1. Neuroscience
Download icon

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
Research Advance
  • Cited 1
  • Views 1,587
  • Annotations
Cite this article as: eLife 2020;9:e59976 doi: 10.7554/eLife.59976

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.

Reviewing Editor

  1. Ronald L Calabrese, Emory University, United States

Publication history

  1. Received: June 15, 2020
  2. Accepted: October 25, 2020
  3. Accepted Manuscript published: October 26, 2020 (version 1)
  4. Version of Record published: November 9, 2020 (version 2)

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

  • 1,587
    Page views
  • 210
    Downloads
  • 1
    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)

  1. Further reading

Further reading

    1. Developmental Biology
    2. Neuroscience
    Sonia Taïb et al.
    Research Article Updated

    Peripheral nerves are vascularized by a dense network of blood vessels to guarantee their complex function. Despite the crucial role of vascularization to ensure nerve homeostasis and regeneration, the mechanisms governing nerve invasion by blood vessels remain poorly understood. We found, in mice, that the sciatic nerve invasion by blood vessels begins around embryonic day 16 and continues until birth. Interestingly, intra-nervous blood vessel density significantly decreases during post-natal period, starting from P10. We show that, while the axon guidance molecule Netrin-1 promotes nerve invasion by blood vessels via the endothelial receptor UNC5B during embryogenesis, myelinated Schwann cells negatively control intra-nervous vascularization during post-natal period.

    1. Neuroscience
    Christian Brodbeck et al.
    Research Article

    Speech processing is highly incremental. It is widely accepted that human listeners continuously use the linguistic context to anticipate upcoming concepts, words, and phonemes. However, previous evidence supports two seemingly contradictory models of how a predictive context is integrated with the bottom-up sensory input: Classic psycholinguistic paradigms suggest a two-stage process, in which acoustic input initially leads to local, context-independent representations, which are then quickly integrated with contextual constraints. This contrasts with the view that the brain constructs a single coherent, unified interpretation of the input, which fully integrates available information across representational hierarchies, and thus uses contextual constraints to modulate even the earliest sensory representations. To distinguish these hypotheses, we tested magnetoencephalography responses to continuous narrative speech for signatures of local and unified predictive models. Results provide evidence that listeners employ both types of models in parallel. Two local context models uniquely predict some part of early neural responses, one based on sublexical phoneme sequences, and one based on the phonemes in the current word alone; at the same time, even early responses to phonemes also reflect a unified model that incorporates sentence level constraints to predict upcoming phonemes. Neural source localization places the anatomical origins of the different predictive models in non-identical parts of the superior temporal lobes bilaterally, with the right hemisphere showing a relative preference for more local models. These results suggest that speech processing recruits both local and unified predictive models in parallel, reconciling previous disparate findings. Parallel models might make the perceptual system more robust, facilitate processing of unexpected inputs, and serve a function in language acquisition.