Bridging the gap between presynaptic hair cell function and neural sound encoding

Abstract

Neural diversity can expand the encoding capacity of a circuitry. A striking example of diverse structure and function is presented by the afferent synapses between inner hair cells (IHCs) and spiral ganglion neurons (SGNs) in the cochlea. Synapses at the pillar IHC-side activate at lower voltages than those of the modiolar side, which show larger active zones and Ca2+-channel clusters. At the postsynapse, SGNs differ in their spontaneous firing rates, sound thresholds and operating ranges. While it is tempting to speculate about a causal relationship between synaptic heterogeneity and neural response diversity, direct experimental evidence is lacking. Here, we bridged this gap by ex-vivo paired recordings of IHCs and postsynaptic boutons with stimuli and conditions aimed to mimic those of in-vivo SGN-characterization. Synapses with high spontaneous rate (SR) were found predominantly on the pillar side of the IHC. These high SR synapses had larger spontaneous EPSCs, lower voltage-thresholds, shorter response latencies and higher initial release rates. This study indicates that synaptic heterogeneity in IHCs can account for functional response diversity of spontaneous and sound-evoked SGN.

Diversity matters — extending sound intensity coding by inner hair cells via heterogeneous synapses

“…Yet, iGluSnFR imaging could not reliably detect release of individual SVs such that a distinction of high and low spontaneous rate of transmission synapses was not possible. However, recordings of excitatory postsynaptic currents (EPSCs) from modiolar and pillar synapses indicated higher rates of spontaneous release for pillar synapses which supports the above hypothesis (Siebald et al , 2023; preprint: Jaime Tobón & Moser, 2022).…”