Sound Transduction in the Mammalian Outer Hair Cells: Prestin Activity is Required for Proper Deflection of the Stereocilia Bundle

Abstract

The outer hair cell (OHC) body is capable of prestin-driven electromotility leading to force generation that increases the vibration of the hearing organ critical for auditory sensitivity. At the cell's apex, the stereocilia bundle deflects as a unit during sound stimulation (Fridberger et al, 2006). Such a deflection converts nanometric displacements into electrical signals transmitted to the auditory nerve. Very little is however known about how sound stimuli cause the bundle to deflect, especially, the possible contribution of prestin-induced cell body vibrations to this deflection has never been investigated. Here we investigated the influence of the membrane protein prestin activity on the bundle deflection, in an intact ear preparation from the Guinea pig. Prestin was previously shown to be specifically inactivated by salicylate and tributyltin. Using an approach combining rapid confocal imaging and optical flow-based computation, the bundle deflection was studied under simultaneous sound stimulus administered at 50-350HZ, a frequency band typical of OHCs vibrations in the apex of the cochlea. To our surprise and irrespective of the prestin inhibitor used, sound-induced bundle deflection drastically increases, specifically, near the best frequency whose position was altered. Likewise, the vibration of the bundle tip intensified. Moreover, the shape of the bundle deflection's pattern was affected. Our data challenge the general assumption that prestin inactivation decreases the vibrations of the cochlear's structures. Because no consistent change was observed for vibrations of the reticular lamina, the increase in the bundle deflection may be caused by a robust vibration of the top. The data suggest that prestin motor's activity regulates the tuning of the bundle vibrations and may explain how the stereociliary and saumatic amplifiers interact during sound transduction in the mammalian ear.