The presynaptic ribbon maintains vesicle populations at the hair cell afferent fiber synapse
- Stanford University, United States
- National Institute of Deafness and Communicative Disorders, United States
- University of the Saarland, Germany
- Washington University at St. Louis, United States
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
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.
Reviewing Editor
- Christine Petit, Institut Pasteur, France
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.
Version history
- Received: July 7, 2017
- Accepted: December 19, 2017
- Accepted Manuscript published: January 12, 2018 (version 1)
- Version of Record published: February 1, 2018 (version 2)
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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The presynaptic ribbon maintains vesicle populations at the hair cell afferent fiber synapse
eLife 7:e30241.
https://doi.org/10.7554/eLife.30241
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