Short-term plasticity at cerebellar granule cell to molecular layer interneuron synapses expands information processing

Abstract

Information processing by cerebellar molecular layer interneurons (MLIs) plays a crucial role in motor behavior. MLI recruitment is tightly controlled by the profile of short-term plasticity (STP) at granule cell (GC)-MLI synapses. While GCs are the most numerous neurons in the brain, STP diversity at GC-MLI synapses is poorly documented. Here, we studied how single MLIs are recruited by their distinct GC inputs during burst firing. Using slice recordings at individual GC-MLI synapses of mice, we revealed four classes of connections segregated by their STP profile. Each class differentially drives MLI recruitment. We show that GC synaptic diversity is underlain by heterogeneous expression of synapsin II, a key actor of STP and that GC terminals devoid of synapsin II are associated with slow MLI recruitment. Our study reveals that molecular, structural and functional diversity across GC terminals provides a mechanism to expand the coding range of MLIs.

Article and author information

Author details

  1. Kevin Dorgans

    Institut des Neurosciences Cellulaires et Intégratives, CNRS, Strasbourg, France
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-1724-6384
  2. Valérie Demais

    UPS 3256 Plateforme Imagerie in vitro, CNRS, Strasbourg, France
    Competing interests
    The authors declare that no competing interests exist.
  3. Yannick Bailly

    Institut des Neurosciences Cellulaires et Intégratives, CNRS, Strasbourg, France
    Competing interests
    The authors declare that no competing interests exist.
  4. Bernard Poulain

    Institut des Neurosciences Cellulaires et Intégratives, CNRS, Strasbourg, France
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-2601-5310
  5. Philippe Isope

    Institut des Neurosciences Cellulaires et Intégratives, CNRS, Strasbourg, France
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-0630-5935
  6. Frédéric Doussau

    Institut des Neurosciences Cellulaires et Intégratives, CNRS, Strasbourg, France
    For correspondence
    doussau@inci-cnrs.unistra.fr
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-3769-1402

Funding

Agence Nationale de la Recherche (ANR-2015CeMod)

  • Philippe Isope

Fondation pour la Recherche Médicale (DEQ20140329514)

  • Philippe Isope

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

  • Kevin Dorgans

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

Reviewing Editor

  1. Indira M Raman, Northwestern University, United States

Ethics

Animal experimentation: This study was carried out in strict accordance with the national and international laws for laboratory animal welfare and experimentation and was approved in advance by the Ethics Committee of Strasbourg (CREMEAS; CEEA35; agreement number/reference protocol: APAFIS#4354-20 16030212155187 v3).

Version history

  1. Received: September 11, 2018
  2. Accepted: May 11, 2019
  3. Accepted Manuscript published: May 13, 2019 (version 1)
  4. Version of Record published: May 23, 2019 (version 2)

Copyright

© 2019, Dorgans 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. Kevin Dorgans
  2. Valérie Demais
  3. Yannick Bailly
  4. Bernard Poulain
  5. Philippe Isope
  6. Frédéric Doussau
(2019)
Short-term plasticity at cerebellar granule cell to molecular layer interneuron synapses expands information processing
eLife 8:e41586.
https://doi.org/10.7554/eLife.41586

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https://doi.org/10.7554/eLife.41586

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