A sensory cell diversifies its output by varying Ca2+ influx-release coupling among presynaptic active zones for wide range intensity coding

Abstract

The cochlea encodes sound intensities ranging over six orders of magnitude which is collectively achieved by functionally diverse spiral ganglion neurons (SGNs). However, the mechanisms enabling the SGNs to cover specific fractions of the audible intensity range remain elusive. Here we tested the hypothesis that intensity information, fully contained in the receptor potential of the presynaptic inner hair cell (IHC), is fractionated via heterogeneous synapses. We studied the transfer function of individual active zones (AZs) using dual-color Rhod-FF and iGluSnFR imaging of Ca2+ and glutamate release. AZs differed in the voltage dependence of release: AZs residing at the IHCs pillar (abneural) side activate at more hyperpolarized potentials and typically showed tight control of release by few Ca2+-channels. We conclude that heterogeneity of voltage dependence and release-site coupling of Ca2+-channels among the AZs varies synaptic transfer within individual IHCs and, thereby, likely contributes to the functional diversity of SGNs.