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The Journal of Neuroscience, July 23, 2008, 28(30):7670-7678; doi:10.1523/JNEUROSCI.0785-08.2008

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Cellular/Molecular
Tonotopic Variation in the Calcium Dependence of Neurotransmitter Release and Vesicle Pool Replenishment at Mammalian Auditory Ribbon Synapses

Stuart L. Johnson,¹ Andrew Forge,² Marlies Knipper,³ Stefan Münkner,⁴ and Walter Marcotti¹

¹Department of Biomedical Science, University of Sheffield, Sheffield S10 2TN, United Kingdom, ²Centre for Auditory Research, UCL Ear Institute, University College London, London WC1X 8EE, United Kingdom, ³Department of Otolaryngology, Molecular Neurobiology, Tübingen Hearing Research Center, and ⁴Institute of Physiology II, University of Tübingen, D-72076 Tübingen, Germany

Correspondence should be addressed to Dr. Walter Marcotti, Department of Biomedical Science, University of Sheffield, Sheffield S10 2TN, UK. Email: w.marcotti{at}sheffield.ac.uk

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 (C_m) in low-frequency (apical region, 300 Hz) and high-frequency (basal, 30 kHz) gerbil IHCs maintained in near physiological conditions (1.3 mM 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 C_m in apical cells. After maturation, C_m 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.

Key words: hair cell; ribbon synapse; exocytosis; development; cochlea; calcium current

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Received Feb. 21, 2008; revised May 28, 2008; accepted June 17, 2008.

Correspondence should be addressed to Dr. Walter Marcotti, Department of Biomedical Science, University of Sheffield, Sheffield S10 2TN, UK. Email: w.marcotti{at}sheffield.ac.uk

This article has been cited by other articles:

				D. Dulon, S. Safieddine, S. M. Jones, and C. Petit Otoferlin Is Critical for a Highly Sensitive and Linear Calcium-Dependent Exocytosis at Vestibular Hair Cell Ribbon Synapses J. Neurosci., August 26, 2009; 29(34): 10474 - 10487. [Abstract] [Full Text] [PDF]

				P. Heidrych, U. Zimmermann, S. Kuhn, C. Franz, J. Engel, S. V. Duncker, B. Hirt, C. M. Pusch, P. Ruth, M. Pfister, et al. Otoferlin interacts with myosin VI: implications for maintenance of the basolateral synaptic structure of the inner hair cell Hum. Mol. Genet., August 1, 2009; 18(15): 2779 - 2790. [Abstract] [Full Text] [PDF]

				S. L. Johnson, C. Franz, M. Knipper, and W. Marcotti Functional maturation of the exocytotic machinery at gerbil hair cell ribbon synapses J. Physiol., April 15, 2009; 587(8): 1715 - 1726. [Abstract] [Full Text] [PDF]

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