The synaptic ribbon is critical for sound encoding at high rates and with temporal precision
- University Medical Center Göttingen, Germany
- University of Göttingen, Germany
- Georg-August-University Göttingen, Germany
- University of the Saarland, Germany
- Max Planck Institute for Dynamics and Self-Organization, Germany
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
Maria Magdalena Picher
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.
Reviewing Editor
- Christine Petit, Institut Pasteur, France
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).
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
© 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 synaptic ribbon is critical for sound encoding at high rates and with temporal precision
eLife 7:e29275.
https://doi.org/10.7554/eLife.29275
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