Mechanisms of the phase locking of auditory-nerve fibers: a modeling approach

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A hallmark of the extraordinary temporal precision of the auditory system and its processing speed is phase locking of neuronal discharges (spikes) of auditory-nerve fibers (ANFs; the primary afferents), and some more central neurons, to the fine-structure of acoustic stimuli. In response to tones, for example, phase locking is reflected in a peaked distribution of spikes over a stimulus cycle, even those that are 200 µs or shorter (the limit depending on species), with a temporal dispersion as low as 30 µs. Phase locking by ANFs appears crucial for sound localization and the perception of pitch, a salient feature of music, speech, and other vocalizations, and has also been used as a tool to infer cochlear mechanics. To this end, we developed a parsimonious phenomenological model that accurately accounts for the instantaneous spike probability of cat ANFs in the course of a stimulus cycle, as functions of sound frequency and level. A key requirement of this model is a dynamic Boltzmann transfer function at the front end, which rapidly adapts to the prevailing sound level. We also developed a model of synaptic-vesicle-pool depletion and replenishment that accurately accounts for spiking statistics (interspike interval distributions, serial interval correlations, and spike-count distributions) of these ANFs during spontaneous activity. We now plan to combine the two models to also account for the spiking statistics of sound-driven phase-locked responses. We also plan to further characterize the dynamics of the Boltzmann transfer function by recording ANF responses to novel mixed-amplitude stimuli and examining phase locking on a cycle-by-cycle basis. Furthermore, we plan to test the more general validity of our models by applying them to data from birds and from Bassoon mutant mice with altered ribbon synapses. Our work will help identify the key mechanisms underlying the remarkable temporal precision of ANF responses.