Neuronal integration in the adult mouse olfactory bulb is a non-selective addition process

  1. Jean-Claude Platel  Is a corresponding author
  2. Alexandra Angelova
  3. Stephane Bugeon
  4. Jenelle Wallace
  5. Thibault Ganay
  6. Ilona Chudotvorova
  7. Jean-Christophe Deloulme
  8. Christophe Beclin
  9. Marie-Catherine Tiveron
  10. Nathalie Coré
  11. Venkatesh N Murthy
  12. Harold Cremer
  1. Aix-Marseille University, CNRS, France
  2. Harvard University, United States
  3. Université Grenoble Alpes, France

Abstract

Adult neurogenesis in the olfactory bulb (OB) is considered as a competition in which neurons scramble during a critical selection period for integration and survival. Moreover, newborn neurons are thought to replace pre-existing ones that die. Despite indirect evidence supporting this model, systematic in vivo observations are still scarce. We used 2-photon in vivo imaging to study neuronal integration and survival. We show that loss of new neurons in the OB after arrival at terminal positions occurs only at low levels. Moreover, long-term observations showed that no substantial cell death occurred at later stages. Neuronal death was induced by standard doses of thymidine analogs, but disappeared when low doses were used. Finally, we demonstrate that the OB grows throughout life. This shows that neuronal selection during OB-neurogenesis does not occur after neurons reached stable positions. Moreover, this suggests that OB neurogenesis does not represent neuronal turnover but lifelong neuronal addition.

Data availability

The raw data that support the findings of this study are several TBs in size and are therefore available on request. A source data file for the main figures has been provided.

Article and author information

Author details

  1. Jean-Claude Platel

    IBDM, UMR 7288, Aix-Marseille University, CNRS, Marseille, France
    For correspondence
    jean-claude.platel@univ-amu.fr
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-5542-3076
  2. Alexandra Angelova

    IBDM, Developmental Biology Institute of Marseille, Aix-Marseille University, CNRS, Marseille, France
    Competing interests
    The authors declare that no competing interests exist.
  3. Stephane Bugeon

    IBDM, UMR 7288, Aix-Marseille University, CNRS, Marseille, France
    Competing interests
    The authors declare that no competing interests exist.
  4. Jenelle Wallace

    Department of Molecular and Cellular Biology, Harvard University, Cambridge, United States
    Competing interests
    The authors declare that no competing interests exist.
  5. Thibault Ganay

    IBDM, UMR 7288, Aix-Marseille University, CNRS, Marseille, France
    Competing interests
    The authors declare that no competing interests exist.
  6. Ilona Chudotvorova

    IBDM, UMR 7288, Aix-Marseille University, CNRS, Marseille, France
    Competing interests
    The authors declare that no competing interests exist.
  7. Jean-Christophe Deloulme

    Grenoble Institut des Neurosciences, Université Grenoble Alpes, Grenoble, France
    Competing interests
    The authors declare that no competing interests exist.
  8. Christophe Beclin

    IBDM, Developmental Biology Institute of Marseille, Aix-Marseille University, CNRS, Marseille, France
    Competing interests
    The authors declare that no competing interests exist.
  9. Marie-Catherine Tiveron

    IBDM, UMR 7288, Aix-Marseille University, CNRS, Marseille, France
    Competing interests
    The authors declare that no competing interests exist.
  10. Nathalie Coré

    IBDM, Developmental Biology Institute of Marseille, Aix-Marseille University, CNRS, Marseille, France
    Competing interests
    The authors declare that no competing interests exist.
  11. Venkatesh N Murthy

    Department of Molecular and Cellular Biology, Harvard University, Cambridge, United States
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-2443-4252
  12. Harold Cremer

    IBDM, Developmental Biology Institute of Marseille, Aix-Marseille University, CNRS, Marseille, France
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-8673-5176

Funding

Agence Nationale de la Recherche (ANR-13-BSV4-0013)

  • Harold Cremer

Fondation pour la Recherche Médicale (ING20150532361)

  • Harold Cremer

Fondation pour la Recherche Médicale (FDT20160435597)

  • Harold Cremer

Fondation pour la Recherche Médicale (FTD20170437248)

  • Alexandra Angelova

Fondation de France (FDF70959)

  • Harold Cremer

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

Ethics

Animal experimentation: All mice were treated according to protocols approved by the French Ethical Committee (#5223-2016042717181477v2).

Reviewing Editor

  1. Gary L Westbrook, Oregon Health and Science University, United States

Publication history

  1. Received: January 2, 2019
  2. Accepted: July 7, 2019
  3. Accepted Manuscript published: July 11, 2019 (version 1)
  4. Version of Record published: July 16, 2019 (version 2)

Copyright

© 2019, Platel 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. Jean-Claude Platel
  2. Alexandra Angelova
  3. Stephane Bugeon
  4. Jenelle Wallace
  5. Thibault Ganay
  6. Ilona Chudotvorova
  7. Jean-Christophe Deloulme
  8. Christophe Beclin
  9. Marie-Catherine Tiveron
  10. Nathalie Coré
  11. Venkatesh N Murthy
  12. Harold Cremer
(2019)
Neuronal integration in the adult mouse olfactory bulb is a non-selective addition process
eLife 8:e44830.
https://doi.org/10.7554/eLife.44830
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