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The presynaptic ribbon maintains vesicle populations at the hair cell afferent fiber synapse

  1. Lars Becker
  2. Michael E Schnee
  3. Mamiko Niwa
  4. Willy Sun
  5. Stephan Maxeiner
  6. Sara Talaei
  7. Bechara Kachar
  8. Mark A Rutherford
  9. Anthony J Ricci Is a corresponding author
  1. Stanford University, United States
  2. National Institute of Deafness and Communicative Disorders, United States
  3. University of the Saarland, Germany
  4. Washington University at St. Louis, United States
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Cite as: eLife 2018;7:e30241 doi: 10.7554/eLife.30241

Abstract

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; 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 in compensation 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.

Article and author information

Author details

  1. Lars Becker

    Department of Otolaryngology, Stanford University, Stanford, United States
    Competing interests
    The authors declare that no competing interests exist.
  2. Michael E Schnee

    Department of Otolaryngology, Stanford University, Stanford, United States
    Competing interests
    The authors declare that no competing interests exist.
  3. Mamiko Niwa

    Department of Otolaryngology, Stanford University, Stanford, United States
    Competing interests
    The authors declare that no competing interests exist.
  4. Willy Sun

    National Institute of Deafness and Communicative Disorders, Bethesda, United States
    Competing interests
    The authors declare that no competing interests exist.
  5. Stephan Maxeiner

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

    Department of Otolaryngology, Stanford University, Stanford, United States
    Competing interests
    The authors declare that no competing interests exist.
  7. Bechara Kachar

    National Institute of Deafness and Communicative Disorders, Bethesda, United States
    Competing interests
    The authors declare that no competing interests exist.
  8. Mark A Rutherford

    Department of Otolaryngology, Washington University at St. Louis, St Louis, United States
    Competing interests
    The authors declare that no competing interests exist.
  9. Anthony J Ricci

    Department of Otolaryngology, Stanford University, Stanford, United States
    For correspondence
    aricci@stanford.edu
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon 0000-0002-1706-8904

Funding

National Institutes of Health (DC009913)

  • Anthony J Ricci

Action on Hearing Loss

  • Mark A Rutherford

National Institutes of Health (DC014712)

  • Mark A Rutherford

National Institutes of Health (DC013721)

  • Mamiko Niwa

National Institutes of Health (P30 44992)

  • Anthony J Ricci

National Institutes of Health (Z01-DC000002)

  • Willy Sun
  • Bechara Kachar

National Institutes of Health (ZIC DC000081)

  • Willy Sun
  • Bechara Kachar

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

Ethics

Animal experimentation: This study was performed in strict accordance with the recommendations in the Guide for the Care and Use of Laboratory Animals of the National Institutes of Health. All of the animals were handled according to approved institutional animal care and use committee (IACUC) protocol 14345 of Stanford University. The protocol was approved by the Committee on the Ethics of Animal Experiments of the University of Minnesota. All auditory measurements were performed under Ketamine (100mg/kg) and Xylazine,(10mg/kg) and every effort was made to minimize suffering.

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)

Copyright

This is an open-access article, free of all copyright, and may be freely reproduced, distributed, transmitted, modified, built upon, or otherwise used by anyone for any lawful purpose. The work is made available under the Creative Commons CC0 public domain dedication.

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