Olfactory receptor neurons use gain control and complementary kinetics to encode intermittent odorant stimuli

Abstract

Insects find food and mates by navigating odorant plumes that can be highly intermittent, with intensities and durations that vary rapidly over orders of magnitude. Much is known about olfactory responses to pulses and steps, but it remains unclear how olfactory receptor neurons (ORNs) detect the intensity and timing of natural stimuli, where the absence of scale in the signal makes detection a formidable olfactory task. By stimulating Drosophila ORNs in vivo with naturalistic and Gaussian stimuli, we show that ORNs adapt to stimulus mean and variance, and that adaptation and saturation contribute to naturalistic sensing. Mean-dependent gain control followed the Weber-Fechner relation and occurred primarily at odor transduction, while variance-dependent gain control occurred at both transduction and spiking. Transduction and spike generation possessed complementary kinetic properties, that together preserved the timing of odorant encounters in ORN spiking, regardless of intensity. Such scale-invariance could be critical during odor plume navigation.

Article and author information

Author details

  1. Srinivas Gorur-Shandilya

    Interdepartmental Neuroscience Program, Yale University, New Haven, United States
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-7429-457X
  2. Mahmut Demir

    Department of Molecular, Cellular, and Developmental Biology, Yale University, New Haven, United States
    Competing interests
    The authors declare that no competing interests exist.
  3. Junjiajia Long

    Department of Physics, Yale University, New Haven, United States
    Competing interests
    The authors declare that no competing interests exist.
  4. Damon A Clark

    Interdepartmental Neuroscience Program, Yale University, New Haven, United States
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-8487-700X
  5. Thierry Emonet

    Interdepartmental Neuroscience Program, Yale University, New Haven, United States
    For correspondence
    thierry.emonet@yale.edu
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-6746-6564

Funding

Whitehall Foundation

  • Srinivas Gorur-Shandilya
  • Mahmut Demir
  • Thierry Emonet

Sloan Research Fellowship

  • Damon A Clark

Searle Scholar Award

  • Damon A Clark

Smith Family Foundation

  • Damon A Clark

Natural Sciences and Engineering Research Council of Canada (PGSD2-471587-2015)

  • Junjiajia Long

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

Reviewing Editor

  1. Fred Rieke, Howard Hughes Medical Institute, University of Washington, United States

Publication history

  1. Received: April 10, 2017
  2. Accepted: June 26, 2017
  3. Accepted Manuscript published: June 27, 2017 (version 1)
  4. Accepted Manuscript updated: June 28, 2017 (version 2)
  5. Version of Record published: July 24, 2017 (version 3)

Copyright

© 2017, Gorur-Shandilya 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.

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  1. Srinivas Gorur-Shandilya
  2. Mahmut Demir
  3. Junjiajia Long
  4. Damon A Clark
  5. Thierry Emonet
(2017)
Olfactory receptor neurons use gain control and complementary kinetics to encode intermittent odorant stimuli
eLife 6:e27670.
https://doi.org/10.7554/eLife.27670

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