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.

Metrics

  • 1,977
    views
  • 245
    downloads
  • 6
    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. 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

Further reading

    1. Neuroscience
    Songyao Zhang, Tuo Zhang ... Tianming Liu
    Research Article

    Cortical folding is an important feature of primate brains that plays a crucial role in various cognitive and behavioral processes. Extensive research has revealed both similarities and differences in folding morphology and brain function among primates including macaque and human. The folding morphology is the basis of brain function, making cross-species studies on folding morphology important for understanding brain function and species evolution. However, prior studies on cross-species folding morphology mainly focused on partial regions of the cortex instead of the entire brain. Previously, our research defined a whole-brain landmark based on folding morphology: the gyral peak. It was found to exist stably across individuals and ages in both human and macaque brains. Shared and unique gyral peaks in human and macaque are identified in this study, and their similarities and differences in spatial distribution, anatomical morphology, and functional connectivity were also dicussed.

    1. Neuroscience
    Avani Koparkar, Timothy L Warren ... Lena Veit
    Research Article

    Complex skills like speech and dance are composed of ordered sequences of simpler elements, but the neuronal basis for the syntactic ordering of actions is poorly understood. Birdsong is a learned vocal behavior composed of syntactically ordered syllables, controlled in part by the songbird premotor nucleus HVC (proper name). Here, we test whether one of HVC’s recurrent inputs, mMAN (medial magnocellular nucleus of the anterior nidopallium), contributes to sequencing in adult male Bengalese finches (Lonchura striata domestica). Bengalese finch song includes several patterns: (1) chunks, comprising stereotyped syllable sequences; (2) branch points, where a given syllable can be followed probabilistically by multiple syllables; and (3) repeat phrases, where individual syllables are repeated variable numbers of times. We found that following bilateral lesions of mMAN, acoustic structure of syllables remained largely intact, but sequencing became more variable, as evidenced by ‘breaks’ in previously stereotyped chunks, increased uncertainty at branch points, and increased variability in repeat numbers. Our results show that mMAN contributes to the variable sequencing of vocal elements in Bengalese finch song and demonstrate the influence of recurrent projections to HVC. Furthermore, they highlight the utility of species with complex syntax in investigating neuronal control of ordered sequences.