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The postsynaptic function of type II cochlear afferents

Abstract

The mammalian cochlea is innervated by two classes of sensory neurons. Type I neurons make up 90–95% of the cochlear nerve and contact single inner hair cells to provide acoustic analysis as we know it. In contrast, the far less numerous type II neurons arborize extensively among outer hair cells (OHCs)1,2 and supporting cells3,4. Their scarcity and smaller calibre axons have made them the subject of much speculation, but little experimental progress for the past 50 years. Here we record from type II fibres near their terminal arbors under OHCs to show that they receive excitatory glutamatergic synaptic input. The type II peripheral arbor conducts action potentials, but the small and infrequent glutamatergic excitation indicates a requirement for strong acoustic stimulation. Furthermore, we show that type II neurons are excited by ATP. Exogenous ATP depolarized type II neurons, both directly and by evoking glutamatergic synaptic input5. These results prove that type II neurons function as cochlear afferents, and can be modulated by ATP. The lesser magnitude of synaptic drive dictates a fundamentally different role in auditory signalling from that of type I afferents.

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Figure 1: Recording from type II terminal arbors.
Figure 2: EPSCs in type II fibres.
Figure 3: ATP stimulates type II fibres.

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Acknowledgements

Supported by NIDCD grants R01 DC000276 and R01 DC006476, T32 DC000023 and a grant from the Blaustein Pain Foundation of Johns Hopkins.

Author Contributions C.W. performed and analysed all experiments with further analysis from P.F. and E.G. C.W., E.G. and P.F. conceived the project, designed and discussed the experiments, and wrote the paper.

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Correspondence to Paul Fuchs.

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This file contains Supplementary Tables 1-3 and Supplementary Figure 1 with Legends and Supplementary References to Table 1. (PDF 165 kb)

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Weisz, C., Glowatzki, E. & Fuchs, P. The postsynaptic function of type II cochlear afferents. Nature 461, 1126–1129 (2009). https://doi.org/10.1038/nature08487

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