Theoretical Conditions for High-Frequency Hair Bundle Oscillations in Auditory Hair Cells

Substantial evidence exists for spontaneous oscillations of hair cell stereociliary bundles in the lower vertebrate inner ear. Since the oscillations are larger than expected from Brownian motion, they must result from an active process in the stereociliary bundle suggested to underlie amplification of the sensory input as well as spontaneous otoacoustic emissions. However, their low frequency (<100 Hz) makes them unsuitable for amplification in birds and mammals that hear up to 5 kHz or higher. To examine the possibility of high-frequency oscillations, we used a finite-element model of the outer hair cell bundle incorporating previously measured mechanical parameters. Bundle motion was assumed to activate mechanotransducer channels according to the gating spring hypothesis, and the channels were regulated adaptively by Ca2+ binding. The model generated oscillations of freestanding bundles at 4 kHz whose sharpness of tuning depended on the mechanotransducer channel number and location, and the Ca2+ concentration. Entrainment of the oscillations by external stimuli was used to demonstrate nonlinear amplification. The oscillation frequency depended on channel parameters and was increased to 23 kHz principally by accelerating Ca2+ binding kinetics. Spontaneous oscillations persisted, becoming very narrow-band, when the hair bundle was loaded with a tectorial membrane mass.