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

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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; 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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Most cited references 39

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Transmitter release at the hair cell ribbon synapse.

Robert P. Fuchs, Elisabeth Glowatzki (2002)

Neurotransmitters are released continuously at ribbon synapses in the retina and cochlea. Notably, a single ribbon synapse of inner hair cells provides the entire input to each cochlear afferent fiber. We investigated hair cell transmitter release in the postnatal rat cochlea by recording excitatory postsynaptic currents (EPSCs) from afferent boutons directly abutting the ribbon synapse. EPSCs were carried by rapidly gating AMPA receptors. EPSCs were clustered in time, indicating the possibility of coordinate release. Amplitude distributions of spontaneous EPSCs were highly skewed, peaking at 0.4 nS and ranging up to 20 times larger. Hair cell depolarization increased EPSC frequency up to 150 Hz without altering the amplitude distribution. We propose that the ribbon synapse operates by multivesicular release, possibly to achieve high-frequency transmission.

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Hair cell synaptic ribbons are essential for synchronous auditory signalling.

Rémy Pujol, Alexander Egner, Tobias Moser … (2005)

Hearing relies on faithful synaptic transmission at the ribbon synapse of cochlear inner hair cells (IHCs). At present, the function of presynaptic ribbons at these synapses is still largely unknown. Here we show that anchoring of IHC ribbons is impaired in mouse mutants for the presynaptic scaffolding protein Bassoon. The lack of active-zone-anchored synaptic ribbons reduced the presynaptic readily releasable vesicle pool, and impaired synchronous auditory signalling as revealed by recordings of exocytic IHC capacitance changes and sound-evoked activation of spiral ganglion neurons. Both exocytosis of the hair cell releasable vesicle pool and the number of synchronously activated spiral ganglion neurons co-varied with the number of anchored ribbons during development. Interestingly, ribbon-deficient IHCs were still capable of sustained exocytosis with normal Ca2+-dependence. Endocytic membrane retrieval was intact, but an accumulation of tubular and cisternal membrane profiles was observed in ribbon-deficient IHCs. We conclude that ribbon-dependent synchronous release of multiple vesicles at the hair cell afferent synapse is essential for normal hearing.

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Aging after noise exposure: acceleration of cochlear synaptopathy in "recovered" ears.

Katharine Fernandez, Penelope W C Jeffers, Kumud Lall … (2015)

Cochlear synaptic loss, rather than hair cell death, is the earliest sign of damage in both noise- and age-related hearing impairment (Kujawa and Liberman, 2009; Sergeyenko et al., 2013). Here, we compare cochlear aging after two types of noise exposure: one producing permanent synaptic damage without hair cell loss and another producing neither synaptopathy nor hair cell loss. Adult mice were exposed (8-16 kHz, 100 or 91 dB SPL for 2 h) and then evaluated from 1 h to ∼ 20 months after exposure. Cochlear function was assessed via distortion product otoacoustic emissions and auditory brainstem responses (ABRs). Cochlear whole mounts and plastic sections were studied to quantify hair cells, cochlear neurons, and the synapses connecting them. The synaptopathic noise (100 dB) caused 35-50 dB threshold shifts at 24 h. By 2 weeks, thresholds had recovered, but synaptic counts and ABR amplitudes at high frequencies were reduced by up to ∼ 45%. As exposed animals aged, synaptopathy was exacerbated compared with controls and spread to lower frequencies. Proportional ganglion cell losses followed. Threshold shifts first appeared >1 year after exposure and, by ∼ 20 months, were up to 18 dB greater in the synaptopathic noise group. Outer hair cell losses were exacerbated in the same time frame (∼ 10% at 32 kHz). In contrast, the 91 dB exposure, producing transient threshold shift without acute synaptopathy, showed no acceleration of synaptic loss or cochlear dysfunction as animals aged, at least to ∼ 1 year after exposure. Therefore, interactions between noise and aging may require an acute synaptopathy, but a single synaptopathic exposure can accelerate cochlear aging.

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Author and article information

Contributors

Michael E Schnee:

ORCID: http://orcid.org/0000-0001-7836-2632

Mamiko Niwa

Willy Sun

Sara Talaei

Bechara Kachar

Mark A Rutherford

Anthony J Ricci:

ORCID: http://orcid.org/0000-0002-1706-8904

Christine Petit: Role: Reviewing Editor

Journal

Journal ID (nlm-ta): eLife

Journal ID (iso-abbrev): Elife

Journal ID (publisher-id): eLife

Title: eLife

Publisher: eLife Sciences Publications, Ltd

ISSN (Electronic): 2050-084X

Publication date (Electronic, pub): 12 January 2018

Publication date Collection: 2018

Volume: 7

Electronic Location Identifier: e30241

Affiliations

[1 ]deptDepartment of Otolaryngology Stanford University StanfordUnited States

[2 ]National Institute of Deafness and Communicative Disorders United States

[3 ]deptMolecular and Cellular Physiology Stanford University StanfordUnited States

[4 ]deptDepartment of Otolaryngology Washington University St. LouisUnited States

[5]Institut Pasteur France

[6]Institut Pasteur France

Author notes

[†]

Department of Otolaryngology, Johns Hopkins University, Baltimore, United States.

[‡]

Department of Neuroanatomy, Institute for Anatomy and Cell Biology, Medical School Saarland University, Saarbrücken, Germany.

Author information

Lars Becker http://orcid.org/0000-0002-3041-3362

Michael E Schnee http://orcid.org/0000-0001-7836-2632

Anthony J Ricci http://orcid.org/0000-0002-1706-8904

Article

Publisher ID: 30241

DOI: 10.7554/eLife.30241

PMC ID: 5794257

PubMed ID: 29328021

SO-VID: b6d868bd-53e9-4ee9-97ed-4fc4e5b9d2ca

License:

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.