Phase Locking of Auditory-Nerve Fibers Reveals Stereotyped Distortions and an Exponential Transfer Function with a...

Phase locking of auditory-nerve-fiber (ANF) responses to the fine structure of acoustic stimuli is a hallmark of the auditory system's temporal precision and is important for many aspects of hearing. Period histograms from phase-locked ANF responses to low-frequency tones exhibit spike-rate and temporal asymmetries, but otherwise retain an approximately sinusoidal shape as stimulus level increases, even beyond the level at which the mean spike rate saturates. This is intriguing because apical cochlear mechanical vibrations show little compression, and mechanoelectrical transduction in the receptor cells is thought to obey a static sigmoidal nonlinearity, which might be expected to produce peak clipping at moderate and high stimulus levels. Here we analyze phase-locked responses of ANFs from cats of both sexes. We show that the lack of peak clipping is due neither to ANF refractoriness nor to spike-rate adaptation on time scales longer than the stimulus period. We demonstrate that the relationship between instantaneous pressure and instantaneous rate is well described by an exponential function whose slope decreases with increasing stimulus level. Relatively stereotyped harmonic distortions in the input to the exponential can account for the temporal asymmetry of the period histograms, including peak splitting. We show that the model accounts for published membrane-potential waveforms when assuming a power-of-three, but not a power-of-one, relationship to exocytosis. Finally, we demonstrate the relationship between the exponential transfer functions and the sigmoidal pseudotransducer functions obtained in the literature by plotting the maxima and minima of the voltage responses against the maxima and minima of the stimuli.SIGNIFICANCE STATEMENT Phase locking of auditory-nerve-fiber responses to the temporal fine structure of acoustic stimuli is important for many aspects of hearing, but the mechanisms underlying phase locking are not fully understood. Intriguingly, period histograms retain an approximately sinusoidal shape across sound levels, even when the mean rate has saturated. We find that neither refractoriness nor spike-rate adaptation is responsible for this behavior. Instead, the peripheral auditory system operates as though it contains an exponential transfer function whose slope changes with stimulus level. The underlying mechanism is distinct from the comparatively weak cochlear mechanical compression in the cochlear apex, and likely resides in the receptor cells.