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.

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

  • 2,076
    views
  • 252
    downloads
  • 16
    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
    Nishal Pradeepbhai Shah, AJ Phillips ... EJ Chichilnisky
    Tools and Resources

    Neural implants have the potential to restore lost sensory function by electrically evoking the complex naturalistic activity patterns of neural populations. However, it can be difficult to predict and control evoked neural responses to simultaneous multi-electrode stimulation due to nonlinearity of the responses. We present a solution to this problem and demonstrate its utility in the context of a bidirectional retinal implant for restoring vision. A dynamically optimized stimulation approach encodes incoming visual stimuli into a rapid, greedily chosen, temporally dithered and spatially multiplexed sequence of simple stimulation patterns. Stimuli are selected to optimize the reconstruction of the visual stimulus from the evoked responses. Temporal dithering exploits the slow time scales of downstream neural processing, and spatial multiplexing exploits the independence of responses generated by distant electrodes. The approach was evaluated using an experimental laboratory prototype of a retinal implant: large-scale, high-resolution multi-electrode stimulation and recording of macaque and rat retinal ganglion cells ex vivo. The dynamically optimized stimulation approach substantially enhanced performance compared to existing approaches based on static mapping between visual stimulus intensity and current amplitude. The modular framework enabled parallel extensions to naturalistic viewing conditions, incorporation of perceptual similarity measures, and efficient implementation for an implantable device. A direct closed-loop test of the approach supported its potential use in vision restoration.

    1. Neuroscience
    Cuong Pham, Yuji Komaki ... Dongdong Li
    Research Article

    Brain water homeostasis not only provides a physical protection, but also determines the diffusion of chemical molecules key for information processing and metabolic stability. As a major type of glia in brain parenchyma, astrocytes are the dominant cell type expressing aquaporin water channel. How astrocyte aquaporin contributes to brain water homeostasis in basal physiology remains to be understood. We report that astrocyte aquaporin 4 (AQP4) mediates a tonic water efflux in basal conditions. Acute inhibition of astrocyte AQP4 leads to intracellular water accumulation as optically resolved by fluorescence-translated imaging in acute brain slices, and in vivo by fiber photometry in mobile mice. We then show that aquaporin-mediated constant water efflux maintains astrocyte volume and osmotic equilibrium, astrocyte and neuron Ca2+ signaling, and extracellular space remodeling during optogenetically induced cortical spreading depression. Using diffusion-weighted magnetic resonance imaging (DW-MRI), we observed that in vivo inhibition of AQP4 water efflux heterogeneously disturbs brain water homeostasis in a region-dependent manner. Our data suggest that astrocyte aquaporin, though bidirectional in nature, mediates a tonic water outflow to sustain cellular and environmental equilibrium in brain parenchyma.