Onset Coding Is Degraded in Auditory Nerve Fibers from Mutant Mice Lacking Synaptic Ribbons

Synaptic ribbons, found at the presynaptic membrane of sensory cells in both ear and eye, have been implicated in the vesicle-pool dynamics of synaptic transmission. To elucidate ribbon function, we characterized the response properties of single auditory nerve fibers in mice lacking Bassoon, a scaf...

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Main Authors: Buran, Bradley N., Strenzke, Nicola, Neef, Andreas, Gundelfinger, Eckart D., Moser, Tobias, Liberman, M. Charles
Other Authors: Harvard University--MIT Division of Health Sciences and Technology
Format: Article
Language:en_US
Published: Society for Neuroscience 2011
Online Access:http://hdl.handle.net/1721.1/66676
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author Buran, Bradley N.
Strenzke, Nicola
Neef, Andreas
Gundelfinger, Eckart D.
Moser, Tobias
Liberman, M. Charles
author2 Harvard University--MIT Division of Health Sciences and Technology
author_facet Harvard University--MIT Division of Health Sciences and Technology
Buran, Bradley N.
Strenzke, Nicola
Neef, Andreas
Gundelfinger, Eckart D.
Moser, Tobias
Liberman, M. Charles
author_sort Buran, Bradley N.
collection MIT
description Synaptic ribbons, found at the presynaptic membrane of sensory cells in both ear and eye, have been implicated in the vesicle-pool dynamics of synaptic transmission. To elucidate ribbon function, we characterized the response properties of single auditory nerve fibers in mice lacking Bassoon, a scaffolding protein involved in anchoring ribbons to the membrane. In bassoon mutants, immunohistochemistry showed that fewer than 3% of the hair cells' afferent synapses retained anchored ribbons. Auditory nerve fibers from mutants had normal threshold, dynamic range, and postonset adaptation in response to tone bursts, and they were able to phase lock with normal precision to amplitude-modulated tones. However, spontaneous and sound-evoked discharge rates were reduced, and the reliability of spikes, particularly at stimulus onset, was significantly degraded as shown by an increased variance of first-spike latencies. Modeling based on in vitro studies of normal and mutant hair cells links these findings to reduced release rates at the synapse. The degradation of response reliability in these mutants suggests that the ribbon and/or Bassoon normally facilitate high rates of exocytosis and that its absence significantly compromises the temporal resolving power of the auditory system.
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spelling mit-1721.1/666762022-09-26T16:26:10Z Onset Coding Is Degraded in Auditory Nerve Fibers from Mutant Mice Lacking Synaptic Ribbons Buran, Bradley N. Strenzke, Nicola Neef, Andreas Gundelfinger, Eckart D. Moser, Tobias Liberman, M. Charles Harvard University--MIT Division of Health Sciences and Technology Buran, Bradley N. Buran, Bradley N. Liberman, M. Charles Synaptic ribbons, found at the presynaptic membrane of sensory cells in both ear and eye, have been implicated in the vesicle-pool dynamics of synaptic transmission. To elucidate ribbon function, we characterized the response properties of single auditory nerve fibers in mice lacking Bassoon, a scaffolding protein involved in anchoring ribbons to the membrane. In bassoon mutants, immunohistochemistry showed that fewer than 3% of the hair cells' afferent synapses retained anchored ribbons. Auditory nerve fibers from mutants had normal threshold, dynamic range, and postonset adaptation in response to tone bursts, and they were able to phase lock with normal precision to amplitude-modulated tones. However, spontaneous and sound-evoked discharge rates were reduced, and the reliability of spikes, particularly at stimulus onset, was significantly degraded as shown by an increased variance of first-spike latencies. Modeling based on in vitro studies of normal and mutant hair cells links these findings to reduced release rates at the synapse. The degradation of response reliability in these mutants suggests that the ribbon and/or Bassoon normally facilitate high rates of exocytosis and that its absence significantly compromises the temporal resolving power of the auditory system. National Institute on Deafness and Other Communication Disorders (U.S.) (Grant RO1 DC00188) National Institute on Deafness and Other Communication Disorders (U.S.) (Grant P30 DC05209) Jack Kent Cooke graduate fellowship Deutsche Forschungsgemeinschaft Deutsche Forschungsgemeinschaft (Center for Molecular Physiology of the Brain) Germany. Bundesministerium für Bildung und Forschung Bernstein Center for Computational Neuroscience Göttingen European Commission (Eurohear) Deutsche Forschungsgemeinschaft (SFB 779/B9) 2011-10-28T17:12:33Z 2011-10-28T17:12:33Z 2010-06 2010-03 Article http://purl.org/eprint/type/JournalArticle 0270-6474 1529-2401 http://hdl.handle.net/1721.1/66676 Buran, B. N. et al. “Onset Coding Is Degraded in Auditory Nerve Fibers from Mutant Mice Lacking Synaptic Ribbons.” Journal of Neuroscience 30 (2010): 7587-7597. Web. 28 Oct. 2011. en_US http://dx.doi.org/10.1523/jneurosci.0389-10.2010 Journal of Neuroscience Article is made available in accordance with the publisher's policy and may be subject to US copyright law. Please refer to the publisher's site for terms of use. application/pdf Society for Neuroscience MIT Amendment
spellingShingle Buran, Bradley N.
Strenzke, Nicola
Neef, Andreas
Gundelfinger, Eckart D.
Moser, Tobias
Liberman, M. Charles
Onset Coding Is Degraded in Auditory Nerve Fibers from Mutant Mice Lacking Synaptic Ribbons
title Onset Coding Is Degraded in Auditory Nerve Fibers from Mutant Mice Lacking Synaptic Ribbons
title_full Onset Coding Is Degraded in Auditory Nerve Fibers from Mutant Mice Lacking Synaptic Ribbons
title_fullStr Onset Coding Is Degraded in Auditory Nerve Fibers from Mutant Mice Lacking Synaptic Ribbons
title_full_unstemmed Onset Coding Is Degraded in Auditory Nerve Fibers from Mutant Mice Lacking Synaptic Ribbons
title_short Onset Coding Is Degraded in Auditory Nerve Fibers from Mutant Mice Lacking Synaptic Ribbons
title_sort onset coding is degraded in auditory nerve fibers from mutant mice lacking synaptic ribbons
url http://hdl.handle.net/1721.1/66676
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