Control of hearing sensitivity by tectorial membrane calcium

Significance

A new mechanism that contributes to control of hearing sensitivity is described here. We show that an accessory structure in the hearing organ, the tectorial membrane, affects the function of inner ear sensory cells by storing calcium ions. When the calcium store is depleted, by brief exposure to rock concert-level sounds or by the introduction of calcium chelators, the sound-evoked responses of the sensory cells decrease. Upon restoration of tectorial membrane calcium, sensory cell function returns. This previously unknown mechanism contributes to explaining the temporary numbness in the ear that follows from listening to sounds that are too loud, a phenomenon that most people experience at some point in their lives.

Abstract

When sound stimulates the stereocilia on the sensory cells in the hearing organ, Ca ²⁺ ions flow through mechanically gated ion channels. This Ca ²⁺ influx is thought to be important for ensuring that the mechanically gated channels operate within their most sensitive response region, setting the fraction of channels open at rest, and possibly for the continued maintenance of stereocilia. Since the extracellular Ca ²⁺ concentration will affect the amount of Ca ²⁺ entering during stimulation, it is important to determine the level of the ion close to the sensory cells. Using fluorescence imaging and fluorescence correlation spectroscopy, we measured the Ca ²⁺ concentration near guinea pig stereocilia in situ. Surprisingly, we found that an acellular accessory structure close to the stereocilia, the tectorial membrane, had much higher Ca ²⁺ than the surrounding fluid. Loud sounds depleted Ca ²⁺ from the tectorial membrane, and Ca ²⁺ manipulations had large effects on hair cell function. Hence, the tectorial membrane contributes to control of hearing sensitivity by influencing the ionic environment around the stereocilia.