Feedback inhibition and its control in an insect olfactory circuit

  1. Subhasis Ray
  2. Zane N Aldworth
  3. Mark A Stopfer  Is a corresponding author
  1. NIH/NICHD, United States

Abstract

Inhibitory neurons play critical roles in regulating and shaping olfactory responses in vertebrates and invertebrates. In insects, these roles are performed by relatively few neurons, which can be interrogated efficiently, revealing fundamental principles of olfactory coding. Here, with electrophysiological recordings from the locust and a large-scale biophysical model, we analyzed the properties and functions of GGN, a unique giant GABAergic neuron that plays a central role in structuring olfactory codes in the locust mushroom body. Our simulations suggest that depolarization of GGN at its input branch can globally inhibit KCs several hundred microns away. Our in vivo recordings show that GGN responds to odors with complex temporal patterns of depolarization and hyperpolarization that can vary with odors and across animals, leading our model to predict the existence of a yet-undiscovered olfactory pathway. Our analysis reveals basic new features of GGN and the olfactory network surrounding it.

Data availability

Traced neuronal morphology have been deposited on neuromorpho.org and they are currently being processed by the repository. Identical morphology data along with the computational models and simulation scripts are available on GitHub (https://github.com/subhacom/mbnet). Model source code curated in Model DB is available under the accession number 262670.

The following data sets were generated

Article and author information

Author details

  1. Subhasis Ray

    Section on Sensory Coding and Neural Ensembles, NIH/NICHD, Bethesda, United States
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-2566-7146
  2. Zane N Aldworth

    Section on Sensory Coding and Neural Ensembles, NIH/NICHD, Bethesda, United States
    Competing interests
    The authors declare that no competing interests exist.
  3. Mark A Stopfer

    Section on Sensory Coding and Neural Ensembles, NIH/NICHD, Bethesda, United States
    For correspondence
    stopferm@mail.nih.gov
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-9200-1884

Funding

NIH-NICHD (Intramural grant)

  • Subhasis Ray
  • Zane N Aldworth
  • Mark A Stopfer

The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.

Reviewing Editor

  1. Kristin Scott, University of California, Berkeley, United States

Version history

  1. Received: November 3, 2019
  2. Accepted: March 9, 2020
  3. Accepted Manuscript published: March 12, 2020 (version 1)
  4. Version of Record published: April 9, 2020 (version 2)

Copyright

This is an open-access article, free of all copyright, and may be freely reproduced, distributed, transmitted, modified, built upon, or otherwise used by anyone for any lawful purpose. The work is made available under the Creative Commons CC0 public domain dedication.

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  1. Subhasis Ray
  2. Zane N Aldworth
  3. Mark A Stopfer
(2020)
Feedback inhibition and its control in an insect olfactory circuit
eLife 9:e53281.
https://doi.org/10.7554/eLife.53281

Share this article

https://doi.org/10.7554/eLife.53281

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