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The Journal of Neuroscience, November 21, 2007, 27(47):12933-12944; doi:10.1523/JNEUROSCI.1996-07.2007

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Cellular/Molecular
Probing the Mechanism of Exocytosis at the Hair Cell Ribbon Synapse

Andreas Neef,^1,2 * Darina Khimich,^2 * Primoz Pirih,^2,3 * Dietmar Riedel,⁴ Fred Wolf,^1,5 and Tobias Moser^1,2

¹Bernstein Center for Computational Neuroscience, Goettingen University, 37073 Goettingen, Germany, ²InnerEarLab, Department of Otolaryngology and Center for Molecular Physiology of the Brain, Goettingen University Medical School, 37075 Goettingen, Germany, ³Department of Neurobiophysics, University of Groningen, 9747 AG, Groningen, The Netherlands, ⁴Laboratory of Electron Microscopy, Max-Planck Institute for Biophysical Chemistry, 37077 Goettingen, Germany, and ⁵Research Group Theoretical Neurophysics, Department of Nonlinear Dynamics, Max Planck Institute for Dynamics and Self-Organization, 37073 Goettingen, Germany

Correspondence should be addressed to either of the following: Tobias Moser, InnerEarLab, Department of Otolaryngology, University of Goettingen, Center for Molecular Physiology of the Brain, Bernstein Center for Computational Neuroscience, 37099 Goettingen, Germany, Email: tmoser{at}gwdg.de; or Fred Wolf, Research Group Theoretical Neurophysics, Department of Nonlinear Dynamics, Max Planck Institute for Dynamics and Self-Organization, Bunsen-Strasse 10, 37073 Goettingen, Germany, E-mail: Email: fred-wl{at}nld.ds.mpg.de

Hearing relies on faithful synaptic transmission at the ribbon synapse of cochlear inner hair cells (IHCs). Postsynaptic recordings from this synapse in prehearing animals had delivered strong indications for synchronized release of several vesicles. The underlying mechanism, however, remains unclear. Here, we used presynaptic membrane capacitance measurements to test whether IHCs release vesicles in a statistically independent or dependent (coordinated) manner. Exocytic changes of membrane capacitance (C_m) were repeatedly stimulated in IHCs of prehearing and hearing mice by short depolarizations to preferentially recruit the readily releasable pool of synaptic vesicles. A compound Poisson model was devised to describe hair cell exocytosis and to test the analysis. From the trial-to-trial fluctuations of the C_m we were able to estimate the apparent size of the elementary fusion event (C_app) at the hair cell synapse to be 96–223 aF in immature and 55–149 aF in mature IHCs. We also approximated the single vesicle capacitance in IHCs by measurements of synaptic vesicle diameters in electron micrographs. The results (immature, 48 aF; mature, 45 aF) were lower than the respective C_app estimates. This indicates that coordinated exocytosis of synaptic vesicles occurs at both immature and mature hair cell synapses. Approximately 35% of the release events in mature IHCs and 50% in immature IHCs were predicted to involve coordinated fusion, when assuming a geometric distribution of elementary sizes. In summary, our presynaptic measurements indicate coordinated exocytosis but argue for a lesser degree of coordination than suggested by postsynaptic recordings.

Key words: exocytosis; synapse; hair cell; ribbon; sound encoding; fluctuation; capacitance; compound Poisson process

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Received May 2, 2007; revised Sept. 14, 2007; accepted Sept. 21, 2007.

Correspondence should be addressed to either of the following: Tobias Moser, InnerEarLab, Department of Otolaryngology, University of Goettingen, Center for Molecular Physiology of the Brain, Bernstein Center for Computational Neuroscience, 37099 Goettingen, Germany, Email: tmoser{at}gwdg.de; or Fred Wolf, Research Group Theoretical Neurophysics, Department of Nonlinear Dynamics, Max Planck Institute for Dynamics and Self-Organization, Bunsen-Strasse 10, 37073 Goettingen, Germany, E-mail: Email: fred-wl{at}nld.ds.mpg.de

This article has been cited by other articles:

				S. L. Johnson, A. Forge, M. Knipper, S. Munkner, and W. Marcotti Tonotopic Variation in the Calcium Dependence of Neurotransmitter Release and Vesicle Pool Replenishment at Mammalian Auditory Ribbon Synapses J. Neurosci., July 23, 2008; 28(30): 7670 - 7678. [Abstract] [Full Text] [PDF]

				G. Matthews and P. Sterling Evidence That Vesicles Undergo Compound Fusion on the Synaptic Ribbon J. Neurosci., May 21, 2008; 28(21): 5403 - 5411. [Abstract] [Full Text] [PDF]

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