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

Research Article Jan 12, 2018

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Cite this article as: eLife 2018;7:e29275 doi: 10.7554/eLife.29275

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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 (RBE^KO^/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.

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Author details

Philippe Jean

Institute for Auditory Neuroscience, University Medical Center Göttingen, Göttingen, Germany

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The authors declare that no competing interests exist.
David Lopez de la Morena

Institute for Auditory Neuroscience, University Medical Center Göttingen, Göttingen, Germany

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Susann Michanski

Collaborative Research Center 889, University of Göttingen, Göttingen, Germany

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Lina María Jaime Tobón

Institute for Auditory Neuroscience, University Medical Center Göttingen, Göttingen, Germany

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Rituparna Chakrabarti

Collaborative Research Center 889, University of Göttingen, Göttingen, Germany

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Maria Magdalena Picher

Institute for Auditory Neuroscience, University Medical Center Göttingen, Göttingen, Germany

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"This ORCID iD identifies the author of this article:" 0000-0003-0722-3883
Jakob Neef

Institute for Auditory Neuroscience, University Medical Center Göttingen, Göttingen, Germany

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SangYong Jung

Institute for Auditory Neuroscience, University Medical Center Göttingen, Göttingen, Germany

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Mehmet Gültas

Department of Breeding Informatics, Georg-August-University Göttingen, Göttingen, Germany

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Stephan Maxeiner

Institute for Anatomy and Cell Biology, University of the Saarland, Homburg, Germany

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Andreas Neef

Bernstein Group Biophysics of Neural Computation, Max Planck Institute for Dynamics and Self-Organization, Göttingen, Germany

For correspondence
aneef@gwdg.de

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"This ORCID iD identifies the author of this article:" 0000-0003-4445-7478
Carolin Wichmann

Collaborative Research Center 889, University of Göttingen, Göttingen, Germany

For correspondence
carolin.wichmann@med.uni-goettingen.de

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Nicola Strenzke

Collaborative Research Center 889, University of Göttingen, Göttingen, Germany

For correspondence
nicola.strenzke@med.uni-goettingen.de

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Chad Grabner

Institute for Auditory Neuroscience, University Medical Center Göttingen, Göttingen, Germany

For correspondence
chad.grabner@mpibpc.mpg.de

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The authors declare that no competing interests exist.
Tobias Moser

Institute for Auditory Neuroscience, University Medical Center Göttingen, Göttingen, Germany

For correspondence
tmoser@gwdg.de

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The authors declare that no competing interests exist.

"This ORCID iD identifies the author of this article:" 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

Christine Petit, Institut Pasteur, France

Publication 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 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.