Simultaneous activation of parallel sensory pathways promotes a grooming sequence in Drosophila

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

Abstract

A central model that describes how behavioral sequences are produced features a neural architecture that readies different movements simultaneously, and a mechanism where prioritized suppression between the movements determines their sequential performance. We previously described a model whereby suppression drives a Drosophila grooming sequence that is induced by simultaneous activation of different sensory pathways that each elicit a distinct movement (Seeds et al. 2014). Here, we confirm this model using transgenic expression to identify and optogenetically activate sensory neurons that elicit specific grooming movements. Simultaneous activation of different sensory pathways elicits a grooming sequence that resembles the naturally induced sequence. Moreover, the sequence proceeds after the sensory excitation is terminated, indicating that a persistent trace of this excitation induces the next grooming movement once the previous one is performed. This reveals a mechanism whereby parallel sensory inputs can be integrated and stored to elicit a delayed and sequential grooming response.

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. Claire E McKellar

    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
    For correspondence
    julie.simpson@lifesci.ucsb.edu
    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.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-4932-6496

Funding

Howard Hughes Medical Institute

  • Julie H Simpson

National Institutes of Health (GM103642)

  • Andrew M Seeds

National Institutes of Health (MD007600)

  • 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

Version history

  1. Received: May 19, 2017
  2. Accepted: September 6, 2017
  3. Accepted Manuscript published: September 9, 2017 (version 1)
  4. Version of Record published: September 26, 2017 (version 2)

Copyright

© 2017, 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. Claire E McKellar
  3. Julie H Simpson
  4. Andrew M Seeds
(2017)
Simultaneous activation of parallel sensory pathways promotes a grooming sequence in Drosophila
eLife 6:e28804.
https://doi.org/10.7554/eLife.28804

Share this article

https://doi.org/10.7554/eLife.28804

Further reading

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    Motor sequences are formed through the serial execution of different movements, but how nervous systems implement this process remains largely unknown. We determined the organizational principles governing how dirty fruit flies groom their bodies with sequential movements. Using genetically targeted activation of neural subsets, we drove distinct motor programs that clean individual body parts. This enabled competition experiments revealing that the motor programs are organized into a suppression hierarchy; motor programs that occur first suppress those that occur later. Cleaning one body part reduces the sensory drive to its motor program, which relieves suppression of the next movement, allowing the grooming sequence to progress down the hierarchy. A model featuring independently evoked cleaning movements activated in parallel, but selected serially through hierarchical suppression, was successful in reproducing the grooming sequence. This provides the first example of an innate motor sequence implemented by the prevailing model for generating human action sequences.

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