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Odor identity coding by distributed ensembles of neurons in the mouse olfactory cortex

  1. Benjamin Roland
  2. Thomas Deneux
  3. Kevin M Franks
  4. Brice Bathellier  Is a corresponding author
  5. Alexander Fleischmann  Is a corresponding author
  1. Collège de France, France
  2. Centre National de la Recherche Scientifique, UPR 3293, France
  3. Duke University, United States
  4. Centre National de la Recherche Scientifique, France
Research Article
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Cite this article as: eLife 2017;6:e26337 doi: 10.7554/eLife.26337

Abstract

Olfactory perception and behaviors critically depend on the ability to identify an odor across a wide range of concentrations. Here, we use calcium imaging to determine how odor identity is encoded in olfactory cortex. We find that, despite considerable trial-to-trial variability, odor identity can accurately be decoded from ensembles of co-active neurons that are distributed across piriform cortex without any apparent spatial organization. However, piriform response patterns change substantially over a 100-fold change in odor concentration, apparently degrading the population representation of odor identity. We show that this problem can be resolved by decoding odor identity from a subpopulation of concentration-invariant piriform neurons. These concentration-invariant neurons are overrepresented in piriform cortex but not in olfactory bulb mitral and tufted cells. We therefore propose that distinct perceptual features of odors are encoded in independent subnetworks of neurons in the olfactory cortex.

Article and author information

Author details

  1. Benjamin Roland

    Center for Interdisciplinary Research in Biology, Collège de France, Paris, France
    Competing interests
    The authors declare that no competing interests exist.
  2. Thomas Deneux

    Unité de Neuroscience, Information et Complexité, Centre National de la Recherche Scientifique, UPR 3293, Gif-sur-Yvette, France
    Competing interests
    The authors declare that no competing interests exist.
  3. Kevin M Franks

    Department of Neurobiology, Duke University, Durham, United States
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-6386-9518
  4. Brice Bathellier

    Unité de Neuroscience, Information et Complexité, Centre National de la Recherche Scientifique, Gif-sur-Yvette, France
    For correspondence
    bathellier@unic.cnrs-gif.fr
    Competing interests
    The authors declare that no competing interests exist.
  5. Alexander Fleischmann

    Center for Interdisciplinary Research in Biology, Collège de France, Paris, France
    For correspondence
    alexander.fleischmann@college-de-france.fr
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-7956-9096

Funding

Marie Curie International Reintegration Grant (IRG 276869)

  • Alexander Fleischmann

Fondation pour la Recherche Médicale (AJE201106)

  • Alexander Fleischmann

European Molecular Biology Organization (ASTF 395 - 2014)

  • Benjamin Roland

LabEx Memolife

  • Benjamin Roland

National Institute on Deafness and Other Communication Disorders (DC009839 and DC015525)

  • Kevin M Franks

Agence Nationale de la Recherche (SENSEMAKER)

  • Brice Bathellier

Human Frontier Science Program (CDA-0064-2015)

  • Brice Bathellier

Marie Curie Program (CIG 334581)

  • Brice Bathellier

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

Ethics

Animal experimentation: This study was performed in strict accordance with French National and INSERM animal care and use committee guidelines (#B750512/00615.02). All surgery was performed under ketamine/xylazine anesthesia.

Reviewing Editor

  1. Upinder Singh Bhalla, National Centre for Biological Sciences, Tata Institute of Fundamental Research, India

Publication history

  1. Received: February 24, 2017
  2. Accepted: April 29, 2017
  3. Accepted Manuscript published: May 10, 2017 (version 1)
  4. Version of Record published: May 19, 2017 (version 2)

Copyright

© 2017, Roland 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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