The rapid developmental rise of somatic inhibition disengages hippocampal dynamics from self-motion

  1. Robin F Dard
  2. Erwan Leprince
  3. Julien Denis
  4. Shrisha Rao Balappa
  5. Dmitrii Suchkov
  6. Richard Boyce
  7. Catherine Lopez
  8. Marie Giorgi-Kurz
  9. Tom Szwagier
  10. Théo Dumont
  11. Hervé Rouault
  12. Marat Minlebaev
  13. Agnès Baude
  14. Rosa Cossart  Is a corresponding author
  15. Michel A Picardo  Is a corresponding author
  1. Aix Marseille Univ, INSERM, INMED U1249, France
  2. Aix-Marseille Univ, Université de Toulon, CNRS, CPT (UMR 7332), France
  3. Mines ParisTech, France

Abstract

Early electrophysiological brain oscillations recorded in preterm babies and newborn rodents are initially mostly driven by bottom-up sensorimotor activity and only later can detach from external inputs. This is a hallmark of most developing brain areas including the hippocampus, which in the adult brain, functions in integrating external inputs onto internal dynamics. Such developmental disengagement from external inputs is likely a fundamental step for the proper development of cognitive internal models. Despite its importance, the developmental timeline and circuit basis for this disengagement remain unknown. To address this issue, we have investigated the daily evolution of CA1 dynamics and underlying circuits during the first two postnatal weeks of mouse development using two-photon calcium imaging in non-anesthetized pups. We show that the first postnatal week ends with an abrupt shift in the representation of self-motion in CA1. Indeed, most CA1 pyramidal cells switch from activated to inhibited by self-generated movements at the end of the first postnatal week whereas the majority of GABAergic neurons remain positively modulated throughout this period. This rapid switch occurs within two days and follows the rapid anatomical and functional surge of local somatic GABAergic innervation. The observed change in dynamics is consistent with a two-population model undergoing a strengthening of inhibition. We propose that this abrupt developmental transition inaugurates the emergence of internal hippocampal dynamics.

Data availability

NWB dataset is available at DANDI Archive (https://dandiarchive.org 000219).All codes are on GITLAB (Cossart Lab - GitLab).

The following data sets were generated

Article and author information

Author details

  1. Robin F Dard

    Turing Centre for Living systems, Aix Marseille Univ, INSERM, INMED U1249, Marseille, France
    Competing interests
    The authors declare that no competing interests exist.
  2. Erwan Leprince

    Turing Centre for Living systems, Aix Marseille Univ, INSERM, INMED U1249, Marseille, France
    Competing interests
    The authors declare that no competing interests exist.
  3. Julien Denis

    Turing Centre for Living systems, Aix Marseille Univ, INSERM, INMED U1249, Marseille, France
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-0537-6483
  4. Shrisha Rao Balappa

    Turing Centre for Living systems, Aix-Marseille Univ, Université de Toulon, CNRS, CPT (UMR 7332), Marseille, France
    Competing interests
    The authors declare that no competing interests exist.
  5. Dmitrii Suchkov

    Turing Centre for Living systems, Aix Marseille Univ, INSERM, INMED U1249, Marseille, France
    Competing interests
    The authors declare that no competing interests exist.
  6. Richard Boyce

    Turing Centre for Living systems, Aix Marseille Univ, INSERM, INMED U1249, Marseille, France
    Competing interests
    The authors declare that no competing interests exist.
  7. Catherine Lopez

    Turing Centre for Living systems, Aix Marseille Univ, INSERM, INMED U1249, Marseille, France
    Competing interests
    The authors declare that no competing interests exist.
  8. Marie Giorgi-Kurz

    Turing Centre for Living systems, Aix Marseille Univ, INSERM, INMED U1249, Marseille, France
    Competing interests
    The authors declare that no competing interests exist.
  9. Tom Szwagier

    Mines ParisTech, Paris, France
    Competing interests
    The authors declare that no competing interests exist.
  10. Théo Dumont

    Mines ParisTech, Paris, France
    Competing interests
    The authors declare that no competing interests exist.
  11. Hervé Rouault

    Turing Centre for Living systems, Aix-Marseille Univ, Université de Toulon, CNRS, CPT (UMR 7332), Marseille, France
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-4997-2711
  12. Marat Minlebaev

    Turing Centre for Living systems, Aix Marseille Univ, INSERM, INMED U1249, Marseille, France
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-0722-7027
  13. Agnès Baude

    Turing Centre for Living systems, Aix Marseille Univ, INSERM, INMED U1249, 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
  14. Rosa Cossart

    Turing Centre for Living systems, Aix Marseille Univ, INSERM, INMED U1249, 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
  15. Michel A Picardo

    Turing Centre for Living systems, Aix Marseille Univ, INSERM, INMED U1249, Marseille, France
    For correspondence
    michel.picardo@inserm.fr
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-1198-3930

Funding

European Resuscitation Council (646925)

  • Rosa Cossart

Fondation Bettencourt Schueller

  • Rosa Cossart

Neurodata Without Borders (R20046AA)

  • Michel A Picardo

Agence Nationale de la Recherche (ANR-16-CONV-0001)

  • Rosa Cossart

Ministère de l'Education Nationale, de l'Enseignement Superieur et de la Recherche (MESR)

  • Robin F Dard
  • Erwan Leprince

Fondation pour la Recherche Médicale (FDT202106012824)

  • Robin F Dard

Fondation pour la Recherche Médicale (FDM20170638339)

  • Julien Denis

Fondation pour la Recherche Médicale (ARF20160936186)

  • Michel A Picardo

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 experiments were performed under the guidelines of the French National Ethics Committee forSciences and Health report on "Ethical Principles for Animal Experimentation" in agreement with theEuropean Community Directive 86/609/EEC (Apafis#18-185 and #30-959).

Reviewing Editor

  1. Adrien Peyrache, McGill University, Canada

Version history

  1. Preprint posted: June 9, 2021 (view preprint)
  2. Received: February 23, 2022
  3. Accepted: July 19, 2022
  4. Accepted Manuscript published: July 20, 2022 (version 1)
  5. Version of Record published: August 8, 2022 (version 2)
  6. Version of Record updated: August 10, 2022 (version 3)

Copyright

© 2022, Dard 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. Robin F Dard
  2. Erwan Leprince
  3. Julien Denis
  4. Shrisha Rao Balappa
  5. Dmitrii Suchkov
  6. Richard Boyce
  7. Catherine Lopez
  8. Marie Giorgi-Kurz
  9. Tom Szwagier
  10. Théo Dumont
  11. Hervé Rouault
  12. Marat Minlebaev
  13. Agnès Baude
  14. Rosa Cossart
  15. Michel A Picardo
(2022)
The rapid developmental rise of somatic inhibition disengages hippocampal dynamics from self-motion
eLife 11:e78116.
https://doi.org/10.7554/eLife.78116

Share this article

https://doi.org/10.7554/eLife.78116

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