Spike encoding of neurotransmitter release timing by spiral ganglion neurons of the cochlea

Mammalian cochlear spiral ganglion neurons (SGNs) encode sound with microsecond precision. Spike triggering relies upon input from a single ribbon-type active zone of a presynaptic inner hair cell (IHC). Using patch-clamp recordings of rat SGN postsynaptic boutons innervating the modiolar face of IHCs from the cochlear apex, at room temperature, we studied how spike generation contributes to spike timing relative to synaptic input. SGNs were phasic, firing a single short-latency spike for sustained currents of sufficient onset slope. Almost every EPSP elicited a spike, but latency (300-1500 μs) varied with EPSP size and kinetics. When current-clamp stimuli approximated the mean physiological EPSC (≈300 pA), several times larger than threshold current (rheobase, ≈50 pA), spikes were triggered rapidly (latency, ≈500 μs) and precisely (SD, <50 μs). This demonstrated the significance of strong synaptic input. However, increasing EPSC size beyond the physiological mean resulted in less-potent reduction of latency and jitter. Differences in EPSC charge and SGN baseline potential influenced spike timing less as EPSC onset slope and peak amplitude increased. Moreover, the effect of baseline potential on relative threshold was small due to compensatory shift of absolute threshold potential. Experimental first-spike latencies in response to a broad range of stimuli were predicted by a two-compartment exponential integrate-and-fire model, with latency prediction error of <100 μs. In conclusion, the close anatomical coupling between a strong synapse and spike generator along with the phasic firing property lock SGN spikes to IHC exocytosis timing to generate the auditory temporal code with high fidelity.