A neural command circuit for grooming movement control

  1. Stefanie Hampel
  2. Romain Franconville
  3. Julie H Simpson
  4. Andrew M Seeds  Is a corresponding author
  1. Howard Hughes Medical Institute, United States

Abstract

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.

Article and author information

Author details

  1. Stefanie Hampel

    Janelia Research Campus, Howard Hughes Medical Institute, Ashburn, United States
    Competing interests
    The authors declare that no competing interests exist.
  2. Romain Franconville

    Janelia Research Campus, Howard Hughes Medical Institute, Ashburn, United States
    Competing interests
    The authors declare that no competing interests exist.
  3. Julie H Simpson

    Janelia Research Campus, Howard Hughes Medical Institute, Ashburn, United States
    Competing interests
    The authors declare that no competing interests exist.
  4. Andrew M Seeds

    Janelia Research Campus, Howard Hughes Medical Institute, Ashburn, United States
    For correspondence
    seeds.andrew@gmail.com
    Competing interests
    The authors declare that no competing interests exist.

Reviewing Editor

  1. Alexander Borst, Max Planck Institute of Neurobiology, Germany

Publication history

  1. Received: May 17, 2015
  2. Accepted: September 5, 2015
  3. Accepted Manuscript published: September 7, 2015 (version 1)
  4. Version of Record published: October 9, 2015 (version 2)

Copyright

© 2015, 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

  • 5,717
    Page views
  • 1,000
    Downloads
  • 66
    Citations

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

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. Romain Franconville
  3. Julie H Simpson
  4. Andrew M Seeds
(2015)
A neural command circuit for grooming movement control
eLife 4:e08758.
https://doi.org/10.7554/eLife.08758

Further reading

    1. Neuroscience
    Jingyi Guo Fuglstad, Pearl Saldanha ... Jonathan R Whitlock
    Tools and Resources Updated

    Recording technologies for rodents have seen huge advances in the last decade, allowing users to sample thousands of neurons simultaneously from multiple brain regions. This has prompted the need for digital tool kits to aid in curating anatomical data, however, existing tools either provide limited functionalities or require users to be proficient in coding to use them. To address this we created HERBS (Histological E-data Registration in rodent Brain Spaces), a comprehensive new tool for rodent users that offers a broad range of functionalities through a user-friendly graphical user interface. Prior to experiments, HERBS can be used to plan coordinates for implanting electrodes, targeting viral injections or tracers. After experiments, users can register recording electrode locations (e.g. Neuropixels and tetrodes), viral expression, or other anatomical features, and visualize the results in 2D or 3D. Additionally, HERBS can delineate labeling from multiple injections across tissue sections and obtain individual cell counts.Regional delineations in HERBS are based either on annotated 3D volumes from the Waxholm Space Atlas of the Sprague Dawley Rat Brain or the Allen Mouse Brain Atlas, though HERBS can work with compatible volume atlases from any species users wish to install. HERBS allows users to scroll through the digital brain atlases and provides custom-angle slice cuts through the volumes, and supports free-transformation of tissue sections to atlas slices. Furthermore, HERBS allows users to reconstruct a 3D brain mesh with tissue from individual animals. HERBS is a multi-platform open-source Python package that is available on PyPI and GitHub, and is compatible with Windows, macOS, and Linux operating systems.

    1. Neuroscience
    Nathaniel J Himmel, Akira Sakurai ... Daniel N Cox
    Research Article Updated

    Individual sensory neurons can be tuned to many stimuli, each driving unique, stimulus-relevant behaviors, and the ability of multimodal nociceptor neurons to discriminate between potentially harmful and innocuous stimuli is broadly important for organismal survival. Moreover, disruptions in the capacity to differentiate between noxious and innocuous stimuli can result in neuropathic pain. Drosophila larval class III (CIII) neurons are peripheral noxious cold nociceptors and innocuous touch mechanosensors; high levels of activation drive cold-evoked contraction (CT) behavior, while low levels of activation result in a suite of touch-associated behaviors. However, it is unknown what molecular factors underlie CIII multimodality. Here, we show that the TMEM16/anoctamins subdued and white walker (wwk; CG15270) are required for cold-evoked CT, but not for touch-associated behavior, indicating a conserved role for anoctamins in nociception. We also evidence that CIII neurons make use of atypical depolarizing chloride currents to encode cold, and that overexpression of ncc69—a fly homologue of NKCC1—results in phenotypes consistent with neuropathic sensitization, including behavioral sensitization and neuronal hyperexcitability, making Drosophila CIII neurons a candidate system for future studies of the basic mechanisms underlying neuropathic pain.