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

Abstract

AbstractNeural 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 byex-vivopaired recordings of IHCs and postsynaptic boutons with stimuli and conditions aimed to mimic those ofin-vivoSGN-characterization. Synapses with high spontaneous rate (SR) were found predominantly on the pillar side of the IHC. These highSRsynapses 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.Significance StatementSound encoding relies on spiral ganglion neurons (SGNs) with diverse spontaneous activities, sound thresholds and sound intensity ranges over which firing rates change. Such functional SGN diversity might originate from different input provided by the presynaptic inner hair cells (IHCs) at their afferent synapses. The present study addresses this hypothesis by using recordings from individual IHC-SGN synapses. The results provide evidence that synaptic heterogeneity in IHCs underlies SGN firing diversity. Thus, IHCs seem to employ diverse active zones to decompose sound information into different neural pathways that collectively inform the brain.