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

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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 GABA_A 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.

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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.
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.
Maddalena Balia

INSERM U1128, Neurophysiology and New Microscopies Laboratory, Institut national de la santé et de la recherche médicale, Paris, France

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The authors declare that no competing interests exist.
Mateo Vélez-Fort

Division of Neurophysiology, National Institute for Medical Research, London, United Kingdom

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The authors declare that no competing interests exist.
Vincent de Sars

Université Paris Descartes, Sorbonne Paris Cité, Paris, France

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The authors declare that no competing interests exist.
Yuchio Yanagawa

Department of Genetic and Behavioral Neuroscience, Gunma University Graduate School of Medicine, Maebashi, Japan

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The authors declare that no competing interests exist.
Valentina Emiliani

Université Paris Descartes, Sorbonne Paris Cité, Paris, France

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The authors declare that no competing interests exist.
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.

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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.