The rapid developmental rise of somatic inhibition disengages hippocampal dynamics from self-motion
- Aix Marseille Univ, INSERM, INMED U1249, France
- Aix-Marseille Univ, Université de Toulon, CNRS, CPT (UMR 7332), France
- 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).
Article and author information
Author details
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.
Reviewing Editor
- Adrien Peyrache, McGill University, Canada
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).
Version history
- Preprint posted: June 9, 2021 (view preprint)
- Received: February 23, 2022
- Accepted: July 19, 2022
- Accepted Manuscript published: July 20, 2022 (version 1)
- Version of Record published: August 8, 2022 (version 2)
- 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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The rapid developmental rise of somatic inhibition disengages hippocampal dynamics from self-motion
eLife 11:e78116.
https://doi.org/10.7554/eLife.78116
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