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Transmitter release at the hair cell ribbon synapse

Abstract

Neurotransmitters are released continuously at ribbon synapses in the retina and cochlea. Notably, a single ribbon synapse of inner hair cells provides the entire input to each cochlear afferent fiber. We investigated hair cell transmitter release in the postnatal rat cochlea by recording excitatory postsynaptic currents (EPSCs) from afferent boutons directly abutting the ribbon synapse. EPSCs were carried by rapidly gating AMPA receptors. EPSCs were clustered in time, indicating the possibility of coordinate release. Amplitude distributions of spontaneous EPSCs were highly skewed, peaking at 0.4 nS and ranging up to 20 times larger. Hair cell depolarization increased EPSC frequency up to 150 Hz without altering the amplitude distribution. We propose that the ribbon synapse operates by multivesicular release, possibly to achieve high-frequency transmission.

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Figure 1: IHCs contacted by afferent fibers.
Figure 2: EPSCs in afferent fibers of IHCs.
Figure 3: EPSCs at the IHC ribbon synapse are carried by AMPA receptors.
Figure 4: EPSC amplitude distributions and interevent interval histograms, in 40 mM K+ saline at −94 mV.
Figure 5: EPSC amplitude as a function of τdecay and 10–90% rise time, in 40 mM K+ saline at −94 mV.
Figure 6: EPSC analysis in 5.8 mM K+ saline. Vh −94 mV; mean amplitude ± s.d. indicated; n, number of EPSCs.
Figure 7: 'Bursting' activity in postnatal IHCs and afferent fibers, as assessed by whole-cell recordings.
Figure 8: Comparison of amplitude distributions from afferent fiber recordings with different EPSC frequencies.

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Acknowledgements

This work was supported by the US National Institute on Deafness and Other Communication Disorders (grant 00276) to P.A.F. We thank A.R. Martin for discussion and data analysis, T.D. Parsons for comments on the manuscript and H. Blum for the design of Figure 1.

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Correspondence to Elisabeth Glowatzki.

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Glowatzki, E., Fuchs, P. Transmitter release at the hair cell ribbon synapse. Nat Neurosci 5, 147–154 (2002). https://doi.org/10.1038/nn796

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