Olfactory receptor neurons generate multiple response motifs, increasing coding space dimensionality

  1. Brian Kim
  2. Seth Haney
  3. Ana P Milan
  4. Shruti Joshi
  5. Zane Aldworth
  6. Nikolai Rulkov
  7. Alexander T Kim
  8. Maxim Bazhenov  Is a corresponding author
  9. Mark A Stopfer  Is a corresponding author
  1. Eunice Kennedy Shriver National Institute of Child Health and Human Development, United States
  2. University of California, San Diego, United States
  3. Amsterdam University Medical Centers, Netherlands

Abstract

Odorants binding to olfactory receptor neurons (ORNs) trigger bursts of action potentials, providing the brain with its only experience of the olfactory environment. Our recordings made in vivo from locust ORNs showed odor-elicited firing patterns comprise four distinct response motifs, each defined by a reliable temporal profile. Different odorants could elicit different response motifs from a given ORN, a property we term motif switching. Further, each motif undergoes its own form of sensory adaptation when activated by repeated plume-like odor pulses. A computational model constrained by our recordings revealed that organizing responses into multiple motifs provides substantial benefits for classifying odors and processing complex odor plumes: each motif contributes uniquely to encode the plume's composition and structure. Multiple motifs and motif switching further improve odor classification by expanding coding dimensionality. Our model demonstrated these response features could provide benefits for olfactory navigation, including determining the distance to an odor source.

Data availability

All data generated or analyzed during this study have been deposited at Open Science Framework and can be accessed here: https://osf.io/8bs72/

Article and author information

Author details

  1. Brian Kim

    Eunice Kennedy Shriver National Institute of Child Health and Human Development, Bethesda, United States
    Competing interests
    The authors declare that no competing interests exist.
  2. Seth Haney

    Department of Medicine, University of California, San Diego, La Jolla, United States
    Competing interests
    The authors declare that no competing interests exist.
  3. Ana P Milan

    Department of Clinical Neurophysiology, Amsterdam University Medical Centers, Amsterdam, Netherlands
    Competing interests
    The authors declare that no competing interests exist.
  4. Shruti Joshi

    Department of Medicine, University of California, San Diego, La Jolla, United States
    Competing interests
    The authors declare that no competing interests exist.
  5. Zane Aldworth

    Eunice Kennedy Shriver National Institute of Child Health and Human Development, Bethesda, United States
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-0647-8465
  6. Nikolai Rulkov

    Biocircuits Institute, University of California, San Diego, La Jolla, United States
    Competing interests
    The authors declare that no competing interests exist.
  7. Alexander T Kim

    Eunice Kennedy Shriver National Institute of Child Health and Human Development, Bethesda, United States
    Competing interests
    The authors declare that no competing interests exist.
  8. Maxim Bazhenov

    Biocircuits Institute, University of California, San Diego, La Jolla, United States
    For correspondence
    mbazhenov@health.ucsd.edu
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-1936-0570
  9. Mark A Stopfer

    Eunice Kennedy Shriver National Institute of Child Health and Human Development, 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

Office of Naval Research (N00014-16-1-2829)

  • Maxim Bazhenov

National Institutes of Health (RF1MH117155)

  • Maxim Bazhenov

National Institutes of Health (R01NS109553)

  • Maxim Bazhenov

National Science Foundation (IIS-1724405)

  • Maxim Bazhenov

Obra Social La Caixa (ID 100010434 with code LCF/BQ/ES15/10360004)

  • Ana P Milan

Eunice Kennedy Shriver National Institute of Child Health and Human Development (Intramural)

  • 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. Piali Sengupta, Brandeis University, United States

Version history

  1. Received: April 1, 2022
  2. Preprint posted: April 12, 2022 (view preprint)
  3. Accepted: January 31, 2023
  4. Accepted Manuscript published: January 31, 2023 (version 1)
  5. Version of Record published: February 13, 2023 (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. Brian Kim
  2. Seth Haney
  3. Ana P Milan
  4. Shruti Joshi
  5. Zane Aldworth
  6. Nikolai Rulkov
  7. Alexander T Kim
  8. Maxim Bazhenov
  9. Mark A Stopfer
(2023)
Olfactory receptor neurons generate multiple response motifs, increasing coding space dimensionality
eLife 12:e79152.
https://doi.org/10.7554/eLife.79152

Share this article

https://doi.org/10.7554/eLife.79152

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