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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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        A new method was developed to acquire images automatically at a series of specimen tilts, as required for tomographic reconstruction. The method uses changes in specimen position at previous tilt angles to predict the position at the current tilt angle. Actual measurement of the position or focus is skipped if the statistical error of the prediction is low enough. This method allows a tilt series to be acquired rapidly when conditions are good but falls back toward the traditional approach of taking focusing and tracking images when necessary. The method has been implemented in a program, SerialEM, that provides an efficient environment for data acquisition. This program includes control of an energy filter as well as a low-dose imaging mode, in which tracking and focusing occur away from the area of interest. The program can automatically acquire a montage of overlapping frames, allowing tomography of areas larger than the field of the CCD camera. It also includes tools for navigating between specimen positions and finding regions of interest.
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          Otoferlin, defective in a human deafness form, is essential for exocytosis at the auditory ribbon synapse.

          The auditory inner hair cell (IHC) ribbon synapse operates with an exceptional temporal precision and maintains a high level of neurotransmitter release. However, the molecular mechanisms underlying IHC synaptic exocytosis are largely unknown. We studied otoferlin, a predicted C2-domain transmembrane protein, which is defective in a recessive form of human deafness. We show that otoferlin expression in the hair cells correlates with afferent synaptogenesis and find that otoferlin localizes to ribbon-associated synaptic vesicles. Otoferlin binds Ca(2+) and displays Ca(2+)-dependent interactions with the SNARE proteins syntaxin1 and SNAP25. Otoferlin deficient mice (Otof(-/-)) are profoundly deaf. Exocytosis in Otof(-/-) IHCs is almost completely abolished, despite normal ribbon synapse morphogenesis and Ca(2+) current. Thus, otoferlin is essential for a late step of synaptic vesicle exocytosis and may act as the major Ca(2+) sensor triggering membrane fusion at the IHC ribbon synapse.
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            Author and article information

            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
            Institut Pasteur France
            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.

            Contributors
            ORCID: http://orcid.org/0000-0001-7836-2632
            ORCID: http://orcid.org/0000-0002-1706-8904
            Role: Reviewing Editor,
            Institut Pasteur France
            Journal
            eLife
            Elife
            eLife
            eLife
            eLife Sciences Publications, Ltd
            2050-084X
            12 January 2018
            2018
            : 7
            29328021 5794257 30241 10.7554/eLife.30241

            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.

            Product
            Funding
            Funded by: FundRef http://dx.doi.org/10.13039/100000002, National Institutes of Health;
            Award ID: DC009913
            Award Recipient :
            Funded by: FundRef http://dx.doi.org/10.13039/501100000703, Action on Hearing Loss;
            Award Recipient :
            Funded by: FundRef http://dx.doi.org/10.13039/100000002, National Institutes of Health;
            Award ID: DC014712
            Award Recipient :
            Funded by: FundRef http://dx.doi.org/10.13039/100000002, National Institutes of Health;
            Award ID: DC013721
            Award Recipient :
            Funded by: FundRef http://dx.doi.org/10.13039/100000002, National Institutes of Health;
            Award ID: P30 44992
            Award Recipient :
            Funded by: FundRef http://dx.doi.org/10.13039/100000002, National Institutes of Health;
            Award ID: Z01-DC000002
            Award Recipient :
            Funded by: FundRef http://dx.doi.org/10.13039/100000002, National Institutes of Health;
            Award ID: ZIC DC000081
            Award Recipient :
            The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.
            Categories
            Research Article
            Neuroscience
            Custom metadata
            The auditory hair cell synaptic ribbon maintains vesicle pools near release sites in order to support sustained and timed vesicle release.

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