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Effects of Efference on Hair Cell Bundle Mechanics


Hair cells in both the auditory and vestibular systems receive efferent innervation. A number of prior studies have indicated that efferent regulation serves to diminish the overall sensitivity of the auditory system. The efferent pathway is believed to affect the sensitivity and frequency selectivity of the hair cell by modulating its membrane potential. However, its effect on the mechanical response of the hair cell has not been established. We explored how stimulation of the efferent neurons affects the mechanical responsiveness of an individual hair bundle. We tested this effect on in vitro preparations of hair cells in the sacculi of American bullfrogs (Rana catesbeiana) of both genders. Efferent stimulation routinely resulted in an immediate increase of the frequency of hair bundle spontaneous oscillations for the duration of the stimulus. Enlarging the stimulus amplitude and pulse length, or conversely, decreasing the inter-pulse interval led to oscillation suppression. Additionally, we tested the effects of efference on the hair bundle response to mechanical stimulation. The Arnold Tongues of hair cells undergoing efferent actuation demonstrated an overall desensitization with respect to those of unstimulated cells.

In addition to fine-tuning the response, the efferent pathway strengthens the auditory system for optimal performance by protecting the inner ear from noise-induced damage. Although it has been well-documented that efference helps defend against hair cell and synaptic extinction, the mechanisms of its otoprotective role have still not been established. Specifically, the effect of efference on an individual hair cell’s recovery from mechanical overstimulation has not been demonstrated. Prior research on hair bundle mechanics has shown that a high-amplitude mechanical deflection detunes a bundle from its innately oscillatory regime - rendering it quiescent for intervals dependent on the applied signal. We explored the impact of efferent stimulation on this recovery using the same in vitro American bullfrog saccular hair cell preparations. Efferent actuation concomitant with the hair bundle’s relaxation from a high-amplitude deflection vastly changed the recovery profile and often entirely eliminated the transition to quiescence. Furthermore, we did not find efferent modulation to influence the magnitude of the mechanically-induced offset in a statistically significant manner. Our findings indicate that the efferent system acts as a control mechanism that determines the dynamic regime in which the hair cell is poised.

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