Frequency-dependent mobilization of heterogeneous pools of synaptic vesicles shapes presynaptic plasticity

  1. Frédéric Doussau  Is a corresponding author
  2. Hartmut Schmidt  Is a corresponding author
  3. Kevin Dorgans
  4. Antoine M Valera  Is a corresponding author
  5. Bernard Poulain
  6. Philippe Isope
  1. CNRS, France
  2. University of Leipzig, Germany

Abstract

The segregation of the readily releasable pool of synaptic vesicles (RRP) in sub-pools that are differentially poised for exocytosis shapes short-term plasticity. However, the frequency-dependent mobilization of these sub-pools is poorly understood. Using slice recordings and modeling of synaptic activity at cerebellar granule cell to Purkinje cell synapses of mice, we describe two sub-pools in the RRP that can be differentially recruited upon ultrafast changes in the stimulation frequency. We show that at low frequency stimulations, a first sub-pool is gradually silenced, leading to full blockage of synaptic transmission. Conversely, a second pool of synaptic vesicles that cannot be released by a single stimulus is recruited within milliseconds by high-frequency stimulation and support an ultrafast recovery of neurotransmitter release after low-frequency depression. This frequency-dependent mobilization or silencing of sub-pools in the RRP in terminals of granule cells may play a role in the filtering of sensorimotor information in the cerebellum.

Article and author information

Author details

  1. 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
  2. Hartmut Schmidt

    Carl-Ludwig Institute for Physiology, University of Leipzig, Leipzig, Germany
    For correspondence
    Hartmut.Schmidt@medizin.uni-leipzig.de
    Competing interests
    The authors declare that no competing interests exist.
  3. 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
  4. Antoine M Valera

    Institut des Neurosciences Cellulaires et Intégratives, CNRS, Strasbourg, France
    For correspondence
    a.valera@ucl.ac.uk
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-0230-9752
  5. Bernard Poulain

    Institut des Neurosciences Cellulaires et Intégratives, CNRS, Strasbourg, France
    Competing interests
    The authors declare that no competing interests exist.
  6. 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

Funding

Agence Nationale de la Recherche (ANR-2010-JCJC-1403-1 MicroCer)

  • Philippe Isope

Fondation pour la Recherche Médicale (DEQ20140329514)

  • Philippe Isope

Centre National de la Recherche Scientifique

  • Philippe Isope

Université de Strasbourg

  • Philippe Isope

INTERREG IV Rhin superieur (FEDER # A31)

  • Philippe Isope

Deutsche Forschungsgemeinschaft (SCHM1838)

  • Hartmut Schmidt

Agence Nationale de la Recherche (ANR15-37-CE37-0001-01 CeModR)

  • Philippe Isope

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 experimental protocols are in accordance with European and French guidelines for animal experimentation and have been approved by the Bas-Rhin veterinary office, Strasbourg, France (authorization number A 67-311 to FD)

Reviewing Editor

  1. Inna Slutsky, Tel Aviv University, Israel

Publication history

  1. Received: May 30, 2017
  2. Accepted: October 6, 2017
  3. Accepted Manuscript published: October 9, 2017 (version 1)
  4. Version of Record published: October 19, 2017 (version 2)

Copyright

© 2017, Doussau 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. Frédéric Doussau
  2. Hartmut Schmidt
  3. Kevin Dorgans
  4. Antoine M Valera
  5. Bernard Poulain
  6. Philippe Isope
(2017)
Frequency-dependent mobilization of heterogeneous pools of synaptic vesicles shapes presynaptic plasticity
eLife 6:e28935.
https://doi.org/10.7554/eLife.28935
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