Interneurons and oligodendrocyte progenitors form a structured synaptic network in the developing neocortex

  1. David Orduz
  2. Paloma P Maldonado
  3. Maddalena Balia
  4. Mateo Vélez-Fort
  5. Vincent de Sars
  6. Yuchio Yanagawa
  7. Valentina Emiliani
  8. Maria Cecilia Angulo  Is a corresponding author
  1. Institut national de la santé et de la recherche médicale, France
  2. The Royal Academy of Arts and Sciences, Netherlands
  3. National Institute for Medical Research, United Kingdom
  4. Université Paris Descartes, Sorbonne Paris Cité, France
  5. Gunma University Graduate School of Medicine, Japan

Abstract

NG2 cells, oligodendrocyte progenitors, receive a major synaptic input from interneurons in the developing neocortex. It is presumed that these precursors integrate cortical networks where they act as sensors of neuronal activity. We show that NG2 cells of the developing somatosensory cortex form a transient and structured synaptic network with interneurons that follows its own rules of connectivity. Fast-spiking interneurons, highly connected to NG2 cells, target proximal subcellular domains containing GABAA receptors with γ2 subunits. Conversely, non-fast-spiking interneurons, poorly connected with these progenitors, target distal sites lacking this subunit. In the network, interneuron-NG2 cell connectivity maps exhibit a local spatial arrangement reflecting innervation only by nearest interneurons. This microcircuit architecture shows a connectivity peak at PN10, coinciding with a switch to massive oligodendrocyte differentiation. Hence, GABAergic innervation of NG2 cells is temporally and spatially regulated from the subcellular to the network level in coordination with the onset of oligodendrogenesis.

Article and author information

Author details

  1. David Orduz

    INSERM U1128, Neurophysiology and New Microscopies Laboratory, Institut national de la santé et de la recherche médicale, Paris, France
    Competing interests
    The authors declare that no competing interests exist.
  2. Paloma P Maldonado

    Netherlands Institute for Neuroscience, The Royal Academy of Arts and Sciences, Amsterdam, Netherlands
    Competing interests
    The authors declare that no competing interests exist.
  3. Maddalena Balia

    INSERM U1128, Neurophysiology and New Microscopies Laboratory, Institut national de la santé et de la recherche médicale, Paris, France
    Competing interests
    The authors declare that no competing interests exist.
  4. Mateo Vélez-Fort

    Division of Neurophysiology, National Institute for Medical Research, London, United Kingdom
    Competing interests
    The authors declare that no competing interests exist.
  5. Vincent de Sars

    Université Paris Descartes, Sorbonne Paris Cité, Paris, France
    Competing interests
    The authors declare that no competing interests exist.
  6. Yuchio Yanagawa

    Department of Genetic and Behavioral Neuroscience, Gunma University Graduate School of Medicine, Maebashi, Japan
    Competing interests
    The authors declare that no competing interests exist.
  7. Valentina Emiliani

    Université Paris Descartes, Sorbonne Paris Cité, Paris, France
    Competing interests
    The authors declare that no competing interests exist.
  8. Maria Cecilia Angulo

    INSERM U1128, Neurophysiology and New Microscopies Laboratory, Institut national de la santé et de la recherche médicale, Paris, France
    For correspondence
    maria-cecilia.angulo@parisdescartes.fr
    Competing interests
    The authors declare that no competing interests exist.

Ethics

Animal experimentation: All experiments followed European Union and institutional guidelines for the care and use of laboratory of the INSERM. All of the animals were handled according to approved institutional animal care and use protocols of the University Paris Descartes. The protocol was approved by the Committee on the Ethics of Animal Experiments of the University Paris Descartes (Permit Number: CEEA34.MCA.070.12). Every effort was made to minimize suffering.

Reviewing Editor

  1. Ben Barres, Stanford School of Medicine, United States

Publication history

  1. Received: February 10, 2015
  2. Accepted: April 21, 2015
  3. Accepted Manuscript published: April 22, 2015 (version 1)
  4. Version of Record published: May 15, 2015 (version 2)

Copyright

© 2015, Orduz 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. David Orduz
  2. Paloma P Maldonado
  3. Maddalena Balia
  4. Mateo Vélez-Fort
  5. Vincent de Sars
  6. Yuchio Yanagawa
  7. Valentina Emiliani
  8. Maria Cecilia Angulo
(2015)
Interneurons and oligodendrocyte progenitors form a structured synaptic network in the developing neocortex
eLife 4:e06953.
https://doi.org/10.7554/eLife.06953

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