Nanomechanics of the subtectorial space caused by electromechanics of cochlear outer hair cells

Abstract

The stereocilia of the cochlear inner hair cells (IHCs) transduce vibrations into the sensory receptor current. Until now, mechanisms for deflecting these stereocilia have not been identified experimentally. Here, we identify a mechanism by using the electromechanical properties of the soma of the outer hair cell to produce an intracochlear, mechanical force stimulus. It is known that the soma of this cell generates mechanical force in response to a change of its transmembrane potential. In the present experiments, the force was induced by intracochlear electrical stimulation at frequencies that covered the entire functionally relevant range of 50 kHz. Vibration responses were measured in the transverse direction with a laser Doppler vibrometer. For frequencies up to Ϸ3 kHz in the first three turns of the guinea-pig cochlea, the apical surface of the IHC and the opposing surface of the tectorial membrane were found to vibrate with similar amplitudes but opposite phases. At high frequencies, there was little relative motion between these surfaces in the transverse direction. The counterphasic motion up to Ϸ3 kHz results in a pulsatile motion of the fluid surrounding the stereocilia of the IHCs. Based on physical principles of fluid flow between narrowly spaced elastic plates, we show that radial fluid motion is amplified relative to transverse membrane motion and that the radial motion is capable of bending the stereocilia. In conclusion, for frequencies up to at least 3 kHz, there appears to be direct fluid coupling between outer hair cells and IHCs.inner hair cell ͉ stereocilia ͉ tectorial membrane A major focus of sensory science is the elucidation of mechanisms by which stimuli are transduced into neural responses. Hearing has proved to be the most enigmatic of the sensory modalities to understand. The sensory cells of the receptor organ, the cochlea, remain only partially accessible to our experimental tools. The main, and to date intractable, experimental problem is gaining access to the top or apical surface of the hair cells in the sensory epithelium, the organ of Corti (Fig. 1A), while maintaining the cochlea in its pristine physiological condition. The mechanoelectrical transducers are located at this surface, in a bundle of microvilli, popularly called stereocilia. The adequate stimulus for the transducers is bending of the stereocilia (1). Despite their crucial role in sound processing, mechanisms of stereociliary bending in situ remain unknown.Based on geometrical considerations (2-4), stereociliary bending has long been believed to result from shear motion between the overlying tectorial membrane (TM) and the apical surface of the hair cell. According to this model, the shear motion arises when transverse motion of the basilar membrane (BM) is transformed into differential radial motion of the TM and the reticular lamina (RL), the structure formed by the apical surfaces of the hair cells and supporting cells (Fig. 1 A). However, recent experiments emphasize the inadequacy of this static model for hi...

Dissection of the Mechanical Impedance Components of the Outer Hair Cell Using a Chloride-Channel Blocker

“…Previous publications have shown that 9AC reduces the electromechanical response of the organ of Corti [9,14] and the magnitude of the imaginary component of the axial mechanical impedance of the isolated OHC [1]. As a result of showing that 9AC also reduces the NLC of prestin-transfected HEK293 cells, we conclude that 9AC directly interacts with the motor protein prestin.…”

“…The impedance was manipulated pharmacologically with the voltage-dependent chloridechannel blocker 9AC, which is known to reduce the electrically induced motion of the organ of Corti [9,14].…”

Active Outer Hair Cells Affect the Sound-Evoked Vibration of the Reticular Lamina

“…However, the vibration decrease observed at OHC1 defies any obvious explanation, but a somewhat similar behavior was reported for alternating current stimulation at acoustic frequencies [17]. Nowotny et al showed that the RL at the inner hair cell vibrated in antiphase to OHC2 and suggested a pivot close to the pillar head.…”

Electromechanical role of fixed charge in the mammalian tectorial membrane

“…Electrically evoked displacements of the TM reported in this study have important implications for cochlear preparations in which electrical stimulation is applied [2,11,12]. Mechanical responses to electrical stimulation generally have been attributed to OHC somatic and hair bundle motility mechanisms.…”