Cochlear hair cells convert sound-induced mechanical vibration into electrical signal. In addition, hair cells can perform reverse transduction, in which hair cells act as a motor. This reverse transduction is essential for the sharp frequency discrimination and high sensitivity of the ear. The reason for reverse transduction is that the tuning mechanism of the ear is based on mechanical resonance, requiring to pump energy into mechanical vibration. Mammalian outer hair cells have a voltage-dependent motor in their cell body. Non-mammals, which do not have outer hair cells, reverse transduction must be carried out by hair bundles. It has been shown that hair bundles of frog saccular hair cells have negative stiffness with which extra energy is made available to mechanical vibration. We found that negative stiffness requires cooperative interactions between mechanotransducer channels in the hair bundles. To clarify the mechanism of voltage-dependent motor in outer hair cells, we tested our hypothesis called the ``area motor model.'' This model proposes that the membrane motor in hair cells has electric charge that is transferable across the membrane and that charge transfer is coupled with changes in the membrane area of the motor. We found theoretically that such a mechanism belongs to a class of piezoelectricity where energy conversion is direct and reciprocal. Namely, the motor converts mechanical energy back into electrical energy in a symmetric manner. We tested this prediction using outer hair cells from the guinea pig. Our experiment showed that the piezoelectric reciprocity is indeed satisfied, demonstrating the piezoelectric nature of the motor. Because force produced by outer hair cells depends on the voltage oscillations (receptor potential) in the cells due to transducer current in hair bundles, the magnitude of receptor potential must be significant. Studies on electric properties of these cells, however, indicate that the receptor potential must be highly attenuated by hair cell's intrinsic electric circuit (RC filter). As the result, receptor potential appeared too small to affect the vibration in the cochlea. This is known as the RC time constant problem. We found that the receptor potential at the resonance frequency is not heavily attenuated up to 10 kHz because piezoelectric resonance can overcome the cells' RC filter. The frequency limit arises from the condition that force produced by outer hair cells needs to match viscous drag, which increases with frequency. Thus, for the ear to be sensitive at frequencies higher than 10 kHz, an additional mechanism is required. We propose that fast potassium channels that we found in the basal turn of the cochlea are an essential element that enhances the receptor potential at those high frequencies.
Showing the most recent 10 out of 14 publications
