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.

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.

Metrics

  • 3,960
    views
  • 535
    downloads
  • 51
    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. 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

    1. Neuroscience
    Andrew M Seeds, Primoz Ravbar ... Julie H Simpson
    Research Article

    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.

    1. Neuroscience
    Lisa Reisinger, Gianpaolo Demarchi ... Nathan Weisz
    Research Article

    Phantom perceptions like tinnitus occur without any identifiable environmental or bodily source. The mechanisms and key drivers behind tinnitus are poorly understood. The dominant framework, suggesting that tinnitus results from neural hyperactivity in the auditory pathway following hearing damage, has been difficult to investigate in humans and has reached explanatory limits. As a result, researchers have tried to explain perceptual and potential neural aberrations in tinnitus within a more parsimonious predictive-coding framework. In two independent magnetoencephalography studies, participants passively listened to sequences of pure tones with varying levels of regularity (i.e. predictability) ranging from random to ordered. Aside from being a replication of the first study, the pre-registered second study, including 80 participants, ensured rigorous matching of hearing status, as well as age, sex, and hearing loss, between individuals with and without tinnitus. Despite some changes in the details of the paradigm, both studies equivalently reveal a group difference in neural representation, based on multivariate pattern analysis, of upcoming stimuli before their onset. These data strongly suggest that individuals with tinnitus engage anticipatory auditory predictions differently to controls. While the observation of different predictive processes is robust and replicable, the precise neurocognitive mechanism underlying it calls for further, ideally longitudinal, studies to establish its role as a potential contributor to, and/or consequence of, tinnitus.