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The Journal of Neuroscience, June 24, 2009, 29(25):7991-8004; doi:10.1523/JNEUROSCI.0632-09.2009

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Cellular/Molecular
Complexin-I Is Required for High-Fidelity Transmission at the Endbulb of Held Auditory Synapse

Nicola Strenzke,^1,2 Soham Chanda,³ Cornelia Kopp-Scheinpflug,⁴ Darina Khimich,¹ Kerstin Reim,⁵ Anna V. Bulankina,¹ Andreas Neef,⁶ Fred Wolf,^6,7 Nils Brose,⁵ Matthew A. Xu-Friedman,³ and Tobias Moser^1,6

¹InnerEarLab, Department of Otolaryngology, Göttingen University Medical School, D-37099 Göttingen, Germany, ²Eaton-Peabody Laboratory, Massachusetts Eye and Ear Infirmary, Harvard University, Boston, Massachusetts 02114, ³Department of Biological Sciences, University at Buffalo, State University of New York, Buffalo, New York 14260, ⁴Institute for Zoology, University of Leipzig, D-04103 Leipzig, Germany, ⁵Department of Molecular Neurobiology and Center for Molecular Physiology of the Brain, Max Planck Institute of Experimental Medicine, D-37075 Göttingen, Germany, and ⁶Bernstein Center for Computational Neuroscience, University of Göttingen, and ⁷Max Planck Institute of Dynamics and Self-Organization, D-37073 Göttingen, Germany

Correspondence should be addressed to either of the following: Tobias Moser, InnerEarLab, Department of Otolaryngology, Göttingen University Medical School, D-37099 Göttingen, Germany, Email: tmoser{at}gwdg.de; or Nils Brose, Department of Molecular Neurobiology, Max Planck Institute of Experimental Medicine, Hermann-Rein-Strasse 3, D-37075 Göttingen, Germany, Email: brose{at}em.mpg.de

Complexins (CPXs I–IV) presumably act as regulators of the SNARE (soluble N-ethylmaleimide-sensitive factor attachment protein receptor) complex, but their function in the intact mammalian nervous system is not well established. Here, we explored the role of CPXs in the mouse auditory system. Hearing was impaired in CPX I knock-out mice but normal in knock-out mice for CPXs II, III, IV, and III/IV as measured by auditory brainstem responses. Complexins were not detectable in cochlear hair cells but CPX I was expressed in spiral ganglion neurons (SGNs) that give rise to the auditory nerve. Ca²⁺-dependent exocytosis of inner hair cells and sound encoding by SGNs were unaffected in CPX I knock-out mice. In the absence of CPX I, the resting release probability in the endbulb of Held synapses of the auditory nerve fibers with bushy cells in the cochlear nucleus was reduced. As predicted by computational modeling, bushy cells had decreased spike rates at sound onset as well as longer and more variable first spike latencies explaining the abnormal auditory brainstem responses. In addition, we found synaptic transmission to outlast the stimulus at many endbulb of Held synapses in vitro and in vivo, suggesting impaired synchronization of release to stimulus offset. Although sound encoding in the cochlea proceeds in the absence of complexins, CPX I is required for faithful processing of sound onset and offset in the cochlear nucleus.

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Received Feb. 6, 2009; revised May 13, 2009; accepted May 19, 2009.

Correspondence should be addressed to either of the following: Tobias Moser, InnerEarLab, Department of Otolaryngology, Göttingen University Medical School, D-37099 Göttingen, Germany, Email: tmoser{at}gwdg.de; or Nils Brose, Department of Molecular Neurobiology, Max Planck Institute of Experimental Medicine, Hermann-Rein-Strasse 3, D-37075 Göttingen, Germany, Email: brose{at}em.mpg.de

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				J. Neef, A. Gehrt, A. V. Bulankina, A. C. Meyer, D. Riedel, R. G. Gregg, N. Strenzke, and T. Moser The Ca2+ Channel Subunit {beta}2 Regulates Ca2+ Channel Abundance and Function in Inner Hair Cells and Is Required for Hearing J. Neurosci., August 26, 2009; 29(34): 10730 - 10740. [Abstract] [Full Text] [PDF]

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