CA1 pyramidal cell diversity is rootedin the time of neurogenesis

  1. Davide Cavalieri
  2. Alexandra Angelova
  3. Anas Islah
  4. Catherine Lopez
  5. Marco Bocchio
  6. Yannick Bollmann
  7. Agnès Baude
  8. Rosa Cossart  Is a corresponding author
  1. INSERM Aix-Marseille University, France
  2. Newcastle University, United Kingdom
  3. King's College London, United Kingdom
  4. French Institute of Health and Medical Research, France

Abstract

Cellular diversity supports the computational capacity and flexibility of cortical circuits. Accordingly, principal neurons at the CA1 output node of the murine hippocampus are increasingly recognized as a heterogeneous population. Their genes, molecular content, intrinsic morphophysiology, connectivity, and function seem to segregate along the main anatomical axes of the hippocampus. Since these axes reflect the temporal order of principal cell neurogenesis, we directly examined the relationship between birthdate and CA1 pyramidal neuron diversity, focusing on the ventral hippocampus. We used a genetic fate-mapping approach that allowed tagging three groups of age-matched principal neurons: pioneer, early- and late-born. Using a combination of neuroanatomy, slice physiology, connectivity tracing and cFos staining in mice, we show that birthdate is a strong predictor of CA1 principal cell diversity. We unravel a subpopulation of pioneer neurons recruited in familiar environments with remarkable positioning, morpho-physiological features, and connectivity. Therefore, despite the expected plasticity of hippocampal circuits, given their role in learning and memory, the diversity of their main components is also partly determined at the earliest steps of development.

Data availability

Data generated or analysed during this study are included in the manuscript or available on Dryad (doi:10.5061/dryad.76hdr7swh). A single source data file (multiple sheets) is included in the submission. Raw data and code from the following experiments are also included in the submission: ex vivo electrophysiology. All other data and codes will be made public as soon as possible and are available upon request.

The following data sets were generated
    1. Davide Cavalieri
    (2021) Whole-cell voltage clamp recordings in slice
    Dryad Digital Repository, doi:10.5061/dryad.r4xgxd2cf.

Article and author information

Author details

  1. Davide Cavalieri

    INMED, INSERM Aix-Marseille University, marseille, France
    Competing interests
    The authors declare that no competing interests exist.
  2. Alexandra Angelova

    INMED, INSERM Aix-Marseille University, marseille, France
    Competing interests
    The authors declare that no competing interests exist.
  3. Anas Islah

    INMED, INSERM Aix-Marseille University, marseille, France
    Competing interests
    The authors declare that no competing interests exist.
  4. Catherine Lopez

    INMED, INSERM Aix-Marseille University, marseille, France
    Competing interests
    The authors declare that no competing interests exist.
  5. Marco Bocchio

    Newcastle University, Newcastle, United Kingdom
    Competing interests
    The authors declare that no competing interests exist.
  6. Yannick Bollmann

    King's College London, London, United Kingdom
    Competing interests
    The authors declare that no competing interests exist.
  7. Agnès Baude

    INMED, French Institute of Health and Medical Research, Marseille, France
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-7025-364X
  8. Rosa Cossart

    INMED, French Institute of Health and Medical Research, Marseille, France
    For correspondence
    rosa.cossart@inserm.fr
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-2111-6638

Funding

H2020 European Research Council (646925)

  • Rosa Cossart

Agence Nationale de la Recherche (ANR-13-ISV40002-01)

  • Rosa Cossart

Agence Nationale de la Recherche (JTC-2017-021)

  • Rosa Cossart

Fondation Bettencourt Schueller (Prix des Sciences de la Vie)

  • Rosa Cossart

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

Reviewing Editor

  1. John R Huguenard, Stanford University School of Medicine, United States

Ethics

Animal experimentation: All protocols were performed under the guidelines of the French National Ethics Committee for Sciencesand Health report on "Ethical Principles for Animal Experimentation" in agreement with theEuropean Community Directive 86/609/EEC under agreement #01 413.03. All efforts were madeto minimize pain and suffering and to reduce the number of animals used.

Version history

  1. Preprint posted: March 7, 2021 (view preprint)
  2. Received: April 9, 2021
  3. Accepted: October 31, 2021
  4. Accepted Manuscript published: November 1, 2021 (version 1)
  5. Version of Record published: December 9, 2021 (version 2)

Copyright

© 2021, Cavalieri 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. Davide Cavalieri
  2. Alexandra Angelova
  3. Anas Islah
  4. Catherine Lopez
  5. Marco Bocchio
  6. Yannick Bollmann
  7. Agnès Baude
  8. Rosa Cossart
(2021)
CA1 pyramidal cell diversity is rootedin the time of neurogenesis
eLife 10:e69270.
https://doi.org/10.7554/eLife.69270

Share this article

https://doi.org/10.7554/eLife.69270

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