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Tonotopic variation in the calcium dependence of neurotransmitter release and vesicle pool replenishment at mammalian auditory ribbon synapses

Johnson, S.L., Forge, A., Knipper, M., Münkner, S. and Marcotti, W. (2008) Tonotopic variation in the calcium dependence of neurotransmitter release and vesicle pool replenishment at mammalian auditory ribbon synapses. The Journal of Neuroscience, 28 (30). pp. 7670-7678. ISSN 1529-2401

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Abstract

The mammalian cochlea is specialized to recognize and process complex auditory signals with remarkable acuity and temporal precision over a wide frequency range. The quality of the information relayed to the auditory afferent fibers mainly depends on the transfer characteristics of inner hair cell (IHC) ribbon synapses. To investigate the biophysical properties of the synaptic machinery, we measured changes in membrane capacitance (ACm) in low-frequency (apical region, - 300 Hz) and high-frequency (basal, - 30 kHz) gerbil IHCs maintained in near physiological conditions (1.3mm extracellular Ca2+ and body temperature). With maturation, the Ca2+ efficiency of exocytosis improved in both apical and basal IHCs and was more pronounced in the latter. Prehearing IHCs showed a similar Ca2+ cooperativity of exocytosis despite the smaller ACm in apical cells. After maturation, ACm in high-frequency IHCs increased linearly with the Ca2+ current, whereas, somewhat surprisingly, the relationship was significantly more nonlinear in low-frequency cells. This tonotopic difference seemed to be correlated with ribbon synapse morphology (spherical in apical and ellipsoid in basal IHCs) but not with the expression level of the proposed Ca2+ sensor otoferlin or the spatial coupling between Ca2+ channels and active zones. Repetitive stimulation of adult IHCs showed that vesicle pool refilling could become rate limiting for vesicle release, with high-frequency IHCs able to sustain greater release rates. Together, our findings provide the first evidence for a tonotopic difference in the properties of the synaptic machinery in mammalian IHCs, which could be essential for fine-tuning their receptor characteristics during sound stimulation.

Item Type: Article
Copyright, Publisher and Additional Information: © 2008 The Society for Neuroscience. Reproduced in accordance with the publisher's self-archiving policy.
Keywords: hair cell, ribbon synapse, exocytosis, development, cochlea, calcium current
Academic Units: The University of Sheffield > Faculty of Science (Sheffield) > School of Biological Sciences (Sheffield) > Department of Biomedical Science (Sheffield)
Depositing User: Ms Suzannah Rockett
Date Deposited: 22 Aug 2008 08:36
Last Modified: 08 Feb 2013 16:56
Published Version: http://www.jneurosci.org/cgi/reprint/28/30/7670
Status: Published
Publisher: HighWire Press
Refereed: Yes
Identification Number: 10.1523/JNEUROSCI.0785-08.2008
URI: http://eprints.whiterose.ac.uk/id/eprint/4352

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