Encoding sound in the cochlea: from receptor potential to afferent discharge.

Ribbon-class synapses in the ear achieve analog to digital transformation of a continuously graded membrane potential to all-or-none spikes. In mammals, several auditory nerve fibers (ANFs) carry information from each inner hair cell (IHC) to the brain in parallel. Heterogeneity of transmission among synapses contributes to the diversity of ANF sound-response properties. In addition to the place code for sound frequency and the rate code for sound level, there is also a temporal code. In series with cochlear amplification and frequency tuning, neural representation of temporal cues over a broad range of sound levels enables auditory comprehension in noisy multi-speaker settings. The IHC membrane time constant introduces a low-pass filter that attenuates fluctuations of the receptor potential above 1 - 2 kHz. The ANF spike generator adds a high-pass filter via its depolarization-rate threshold that rejects slow changes in the postsynaptic potential and its phasic response property that ensures one spike per depolarization. Synaptic transmission is the slowest cellular process between IHC depolarization and ANF spike generation, introducing delay and jitter that limits the speed and precision of spike timing. ANFs spike at a preferred phase of periodic sounds in a process called phase-locking that is limited to frequencies below a few kHz by both the IHC receptor potential and the jitter in synaptic transmission. During phase-locking to periodic sounds of increasing intensity, faster and facilitated activation of synaptic transmission and spike generation may be offset by presynaptic depletion of synaptic vesicles, resulting in relatively small changes in response phase. Here we review encoding of spike-timing at cochlear ribbon synapses. Abstract figure legend: The Auditory Ribbon Synapse Controls the Timing of Afferent Spikes. The afferent synapses between sensory hair cells and primary auditory neurons are glutamatergic ribbon-class synapses. This schematic highlights a ribbon synapse between a cochlear inner hair cell (IHC) and one of its auditory nerve fibers (ANF). Sound results in mechanical stimulation of the IHC bundle, evoking a transduction current that generates a receptor potential Vm (t) that changes over time with sound level and frequency. Depolarization of Vm (t) evokes Ca2+ -dependent exocytosis of glutamate at the ribbon synapse. Glutamate binds to AMPA-type receptors to generate an excitatory postsynaptic current (EPSC) in the ANF dendrite. The ensuring depolarization triggers an action potential in the ANF, signaling sound information to the brain. This article is protected by copyright. All rights reserved.