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...

Place based frequency discrimination (tonotopy) is a fundamental property of the coiled mammalian cochlea. Sound vibrations mechanically conducted to the hearing organ manifest themselves into slow moving waves that travel along the length of the organ, also referred to as traveling waves. These traveling waves form the basis of the tonotopic frequency representation in the inner ear of mammals. However, so far, due to the secure housing of the inner ear, these waves only could be measured partially over small accessible regions of the inner ear in a living animal. Here, we demonstrate the existence of tonotopically ordered traveling waves covering most of the length of a miniature hearing organ in the leg of bushcrickets in vivo using laser Doppler vibrometery. The organ is only 1 mm long and its geometry allowed us to investigate almost the entire length with a wide range of stimuli (6 to 60 kHz). The tonotopic location of the traveling wave peak was exponentially related to stimulus frequency. The traveling wave propagated along the hearing organ from the distal (high frequency) to the proximal (low frequency) part of the leg, which is opposite to the propagation direction of incoming sound waves. In addition, we observed a non-linear compression of the velocity response to varying sound pressure levels. The waves are based on the delicate micromechanics of cellular structures different to those of mammals. Hence place based frequency discrimination by traveling waves is a physical phenomenon that presumably evolved in mammals and bushcrickets independently.

Coupling of somatic electromechanical force from the outer hair cells (OHCs) into the organ of Corti is investigated by measuring transverse vibration patterns of the organ of Cori and tectorial membrane (TM) in response to intracochlear electrical stimulation. Measurement places at the organ of Corti extend from the inner sulcus cells to Hensen's cells and at the lower (and upper) surface of the TM from the inner sulcus to the OHC region. These locations are in the neighborhood of where electromechanical force is coupled into (1) the mechanoelectrical transducers of the stereocilia and (2) fluids of the organ of Corti. Experiments are conducted in the first, second, and third cochlear turns of an in vitro preparation of the adult guinea pig cochlea. Vibration measurements are made at functionally relevant stimulus frequencies (0.48-68 kHz) and response amplitudes (<15 nm). The experiments provide phase relations between the different structures, which, dependent on frequency range and longitudinal cochlear position, include in-phase transverse motions of the TM, counterphasic transverse motions between the inner hair cell and OHCs, as well as traveling-wave motion of Hensen's cells in the radial direction. Mechanics of sound processing in the cochlea are discussed based on these phase relationships.

Mechanoelectrical transduction of acoustic signals is the fundamental process for hearing in all ears across the animal kingdom. Here, we performed in vivo laser-vibrometric and electrophysiological measurements at the transduction site in an insect ear (Mecopoda elongata) to relate the biomechanical tonotopy along the hearing organ to the frequency tuning of the corresponding sensory cells. Our mechanical and electrophysiological map revealed a biomechanical filter process that considerably sharpens the neuronal response. We demonstrate that the channel gating, which acts on chordotonal stretch receptor neurons, is based on a mechanical directionality of the sound-induced motion. Further, anatomical studies of the transduction site support our finding of a stimulus-relevant tilt. In conclusion, we were able to show, in an insect ear, that directionality of channel gating considerably sharpens the neuronal frequency selectivity at the peripheral level and have identified a mechanism that enhances frequency discrimination in tonotopically organized ears.

Tinnitus often develops following inner ear pathologies, like acoustic trauma. Therefore, an acoustic trauma model of tinnitus in gerbils was established using a modulated acoustic startle response. Cochlear trauma evoked by exposure to narrow-band noise at 10 kHz was assessed by auditory brainstem responses (ABR) and distortion product otoacoustic emissions (DPOAE). Threshold shift amounted to about 25 dB at frequencies > 10 kHz. Induction of a phantom-noise perception was documented by an acoustic startle response paradigm. A reduction of the gap-prepulse inhibition of acoustic startle (GPIAS) was taken as evidence for tinnitus at the behavioral level. Three to five weeks after trauma the ABR and DPOAE thresholds were back to normal. At that time, a reduction of GPIAS in the frequency range 16-20 kHz indicated a phantom noise perception. Seven weeks post trauma the tinnitus-affected frequency range became narrow and shifted to the center-trauma frequency at 10 kHz. Taken together, by investigating frequency-dependent effects in detail, this study in gerbils found trauma-evoked tinnitus developing in the frequency range bordering the low frequency slope of the induced noise trauma. This supports the theory of lateral inhibition as the physiological basis of tinnitus.