1. Neuroscience

Mechanisms and functional roles of glutamatergic synapse diversity in a cerebellar circuit

  1. Valeria Zampini
  2. Jian K Liu
  3. Marco A. Diana
  4. Paloma P Maldonado
  5. Nicolas Brunel  Is a corresponding author
  6. Stéphane Dieudonné  Is a corresponding author
  1. Ecole Normale Supérieure, France
  2. University Medical Center Goettingen, Germany
  3. Inserm, U1024, CNRS, UMR 8197, France
  4. The Royal Academy of Arts and Sciences, Netherlands
  5. University of Chicago, United States
https://doi.org/10.7554/eLife.15872
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  1. Valeria Zampini
  2. Jian K Liu
  3. Marco A. Diana
  4. Paloma P Maldonado
  5. Nicolas Brunel
  6. Stéphane Dieudonné
(2016)
Mechanisms and functional roles of glutamatergic synapse diversity in a cerebellar circuit
eLife 5:e15872.
https://doi.org/10.7554/eLife.15872
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Abstract

Synaptic currents display a large degree of heterogeneity of their temporal characteristics, but the functional role of such heterogeneities remains unknown. We investigated in rat cerebellar slices synaptic currents in Unipolar Brush Cells (UBCs), which generate intrinsic mossy fibers relaying vestibular inputs to the cerebellar cortex. We show that UBCs respond to sinusoidal modulations of their sensory input with heterogeneous amplitudes and phase shifts. Experiments and modeling indicate that this variability results both from the kinetics of synaptic glutamate transients and from the diversity of postsynaptic receptors. While phase inversion is produced by an mGluR2-activated outward conductance in OFF-UBCs, the phase delay of ON UBCs is caused by a late rebound current resulting from AMPAR recovery from desensitization. Granular layer network modeling indicates that phase dispersion of UBC responses generates diverse phase coding in the granule cell population, allowing climbing-fiber-driven Purkinje cell learning at arbitrary phases of the vestibular input.

Article and author information

Author details

  1. Valeria Zampini

    Institut de Biologie de l'ENS, Ecole Normale Supérieure, Paris, France
    Competing interests
    The authors declare that no competing interests exist.

  2. Jian K Liu

    Department of Ophthalmology, University Medical Center Goettingen, Goettingen, Germany
    Competing interests
    The authors declare that no competing interests exist.

  3. Marco A. Diana

    Neurosciences Paris Seine, Institut de Biologie Paris Seine, Inserm, U1024, CNRS, UMR 8197, Paris, France
    Competing interests
    The authors declare that no competing interests exist.

  4. 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.

  5. Nicolas Brunel

    Department of Statistics and Neurobiology, University of Chicago, Chicago, United States
    For correspondence
    nbrunel@uchicago.edu
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-2272-3248

  6. Stéphane Dieudonné

    Institut de Biologie de l'École Normale Supérieure, Ecole Normale Supérieure, Paris, France
    For correspondence
    dieudon@biologie.ens.fr
    Competing interests
    The authors declare that no competing interests exist.

Funding

Centre National de la Recherche Scientifique

  • Marco A. Diana
  • Nicolas Brunel
  • Stéphane Dieudonné

Institut National de la Santé et de la Recherche Médicale

  • Stéphane Dieudonné

Agence Nationale de la Recherche (ANR-BBSRC grant VESTICODE)

  • Valeria Zampini
  • Jian K Liu
  • Marco A. Diana
  • Paloma P Maldonado
  • Nicolas Brunel
  • Stéphane Dieudonné

Agence Nationale de la Recherche (ANR-10-LABX-54 MEMO LIFE)

  • Stéphane Dieudonné

Agence Nationale de la Recherche (ANR-11- 4 IDEX-0001-02 PSL*)

  • Stéphane Dieudonné

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: All animal manipulations were made in accordance with guidelines of the Centre national de la recherche scientifique. Protocols were approved under number 02235.02 of the general agreement C750520

Version history

  1. Received: March 10, 2016
  2. Accepted: September 17, 2016
  3. Accepted Manuscript published: September 19, 2016 (version 1)
  4. Accepted Manuscript updated: October 7, 2016 (version 2)
  5. Version of Record published: October 21, 2016 (version 3)

Copyright

© 2016, Zampini 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. Valeria Zampini
  2. Jian K Liu
  3. Marco A. Diana
  4. Paloma P Maldonado
  5. Nicolas Brunel
  6. Stéphane Dieudonné
(2016)
Mechanisms and functional roles of glutamatergic synapse diversity in a cerebellar circuit
eLife 5:e15872.
https://doi.org/10.7554/eLife.15872

Share this article

https://doi.org/10.7554/eLife.15872

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