Phase-Locking Precision Is Enhanced by Multiquantal Release at an Auditory Hair Cell Ribbon Synapse

Sound-evoked spikes in the auditory nerve can phase-lock with submillisecond precision for prolonged periods of time. However, the synaptic mechanisms that enable this accurate spike firing remain poorly understood. Using paired recordings from adult frog hair cells and their afferent fibers, we show here that during sine-wave stimuli, synaptic failures occur even during strong stimuli. However, exclusion of these failures leads to mean excitatory postsynaptic current (EPSC) amplitudes that are independent of Ca2+ current. Given the intrinsic jitter in spike triggering, evoked synaptic potentials and spikes had surprisingly similar degrees of synchronization to a sine-wave stimulus. This similarity was explained by an unexpected finding: large-amplitude evoked EPSCs have a significantly larger synchronization index than smaller evoked EPSCs. Large EPSCs therefore enhance the precision of spike timing. The hair cells' unique capacity for continuous, large-amplitude, and highly synchronous multiquantal release thus underlies its ability to trigger phase-locked spikes in afferent fibers.