1. Cell Biology
  2. Neuroscience
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The synaptic ribbon is critical for sound encoding at high rates and with temporal precision

  1. Philippe Jean
  2. David Lopez de la Morena
  3. Susann Michanski
  4. Lina María Jaime Tobón
  5. Rituparna Chakrabarti
  6. Maria Magdalena Picher
  7. Jakob Neef
  8. SangYong Jung
  9. Mehmet Gültas
  10. Stephan Maxeiner
  11. Andreas Neef  Is a corresponding author
  12. Carolin Wichmann  Is a corresponding author
  13. Nicola Strenzke  Is a corresponding author
  14. Chad Grabner  Is a corresponding author
  15. Tobias Moser  Is a corresponding author
  1. University Medical Center Göttingen, Germany
  2. University of Göttingen, Germany
  3. Georg-August-University Göttingen, Germany
  4. University of the Saarland, Germany
  5. Max Planck Institute for Dynamics and Self-Organization, Germany
Research Article
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Cite as: eLife 2018;7:e29275 doi: 10.7554/eLife.29275

Abstract

We studied the role of the synaptic ribbon for sound encoding at the synapses between inner hair cells (IHCs) and spiral ganglion neurons (SGNs) in mice lacking RIBEYE (RBEKO/KO). Electron and immunofluorescence microscopy revealed a lack of synaptic ribbons and an assembly of several small active zones (AZs) at each synaptic contact. Spontaneous and sound-evoked firing rates of SGNs and their compound action potential were reduced, indicating impaired transmission at ribbonless IHC-SGN synapses. The temporal precision of sound encoding was impaired and the recovery of SGN-firing from adaptation indicated slowed synaptic vesicle (SV) replenishment. Activation of Ca2+-channels was shifted to more depolarized potentials and exocytosis was reduced for weak depolarizations. Presynaptic Ca2+-signals showed a broader spread, compatible with the altered Ca2+-channel clustering observed by super-resolution immunofluorescence microscopy. We postulate that RIBEYE disruption is partially compensated by multi-AZ organization. The remaining synaptic deficit indicates ribbon function in SV-replenishment and Ca2+-channel regulation.

Article and author information

Author details

  1. Philippe Jean

    Institute for Auditory Neuroscience, University Medical Center Göttingen, Göttingen, Germany
    Competing interests
    The authors declare that no competing interests exist.

  2. David Lopez de la Morena

    Institute for Auditory Neuroscience, University Medical Center Göttingen, Göttingen, Germany
    Competing interests
    The authors declare that no competing interests exist.

  3. Susann Michanski

    Collaborative Research Center 889, University of Göttingen, Göttingen, Germany
    Competing interests
    The authors declare that no competing interests exist.

  4. Lina María Jaime Tobón

    Institute for Auditory Neuroscience, University Medical Center Göttingen, Göttingen, Germany
    Competing interests
    The authors declare that no competing interests exist.

  5. Rituparna Chakrabarti

    Collaborative Research Center 889, University of Göttingen, Göttingen, Germany
    Competing interests
    The authors declare that no competing interests exist.

  6. Maria Magdalena Picher

    Institute for Auditory Neuroscience, University Medical Center Göttingen, Göttingen, Germany
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon 0000-0003-0722-3883

  7. Jakob Neef

    Institute for Auditory Neuroscience, University Medical Center Göttingen, Göttingen, Germany
    Competing interests
    The authors declare that no competing interests exist.

  8. SangYong Jung

    Institute for Auditory Neuroscience, University Medical Center Göttingen, Göttingen, Germany
    Competing interests
    The authors declare that no competing interests exist.

  9. Mehmet Gültas

    Department of Breeding Informatics, Georg-August-University Göttingen, Göttingen, Germany
    Competing interests
    The authors declare that no competing interests exist.

  10. Stephan Maxeiner

    Institute for Anatomy and Cell Biology, University of the Saarland, Homburg, Germany
    Competing interests
    The authors declare that no competing interests exist.

  11. Andreas Neef

    Bernstein Group Biophysics of Neural Computation, Max Planck Institute for Dynamics and Self-Organization, Göttingen, Germany
    For correspondence
    aneef@gwdg.de
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon 0000-0003-4445-7478

  12. Carolin Wichmann

    Collaborative Research Center 889, University of Göttingen, Göttingen, Germany
    For correspondence
    carolin.wichmann@med.uni-goettingen.de
    Competing interests
    The authors declare that no competing interests exist.

  13. Nicola Strenzke

    Collaborative Research Center 889, University of Göttingen, Göttingen, Germany
    For correspondence
    nicola.strenzke@med.uni-goettingen.de
    Competing interests
    The authors declare that no competing interests exist.

  14. Chad Grabner

    Institute for Auditory Neuroscience, University Medical Center Göttingen, Göttingen, Germany
    For correspondence
    chad.grabner@mpibpc.mpg.de
    Competing interests
    The authors declare that no competing interests exist.

  15. Tobias Moser

    Institute for Auditory Neuroscience, University Medical Center Göttingen, Göttingen, Germany
    For correspondence
    tmoser@gwdg.de
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon 0000-0001-7145-0533

Funding

Deutsche Forschungsgemeinschaft (Collaborative Research Center 889)

  • Carolin Wichmann
  • Nicola Strenzke
  • Tobias Moser

Deutsche Forschungsgemeinschaft (Leibniz program MO 896/51)

  • Tobias Moser

Max-Planck-Gesellschaft (Max-Planck-Fellowship)

  • Tobias Moser

Niedersächsisches Vorab

  • Tobias Moser

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 experiments complied with national animal care guidelines and were approved by the University of Göttingen Board for Animal Welfare and the Animal Welfare Office of the State of Lower Saxony (permit number: 14-1391).

Reviewing Editor

  1. Christine Petit, Reviewing Editor, Institut Pasteur, France

Publication history

  1. Received: July 7, 2017
  2. Accepted: December 19, 2017
  3. Accepted Manuscript published: January 12, 2018 (version 1)
  4. Version of Record published: February 1, 2018 (version 2)

Copyright

© 2018, Jean 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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    The ribbon is the structural hallmark of cochlear inner hair cell (IHC) afferent synapses, yet its role in information transfer to spiral ganglion neurons (SGNs) remains unclear. We investigated the ribbon’s contribution to IHC synapse formation and function using KO mice lacking RIBEYE. Despite loss of the entire ribbon structure, synapses retained their spatiotemporal development and KO mice had a mild hearing deficit. IHCs of KO had fewer synaptic vesicles and reduced exocytosis in response to brief depolarization; a high stimulus level rescued exocytosis in KO. SGNs exhibited a lack of sustained excitatory postsynaptic currents (EPSCs). We observed larger postsynaptic glutamate receptor plaques, potentially compensating for the reduced EPSC rate in KO. Surprisingly, large-amplitude EPSCs were maintained in KO, while a small population of low-amplitude slower EPSCs was increased in number. The ribbon facilitates signal transduction at physiological stimulus levels by retaining a larger residency pool of synaptic vesicles.

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