Amplification of sound by active movements of hair-cell stereocilia in the inner ear plays an important role in the exquisite sensitivity and frequency selectivity of hearing1. Several motile mechanisms and candidate motors have been identified but the biophysical origin(s) and the power source driving the movements remain unclear. We do know that, across species, there is a strong correlation between stereocilia height and the optimal frequency of sensation. Mechanical explanations alone have been inadequate to explain this tonotopic organization across organs and species, thus indicating the contribution of electrical or chemical factors. Recent data demonstrate that membrane tethers from cells with dimensions similar to hair cell stereocilia are electromotile and generate reduced tensile forces when depolarized2. This effect appears to have flexoelectric origins, where biological asymmetries and curvature-induced electrical polarization of the tether membrane interact with the transmembrane electric field to generate a piezoelectric-like force. Results support the hypothesis that this biophysical mechanism is at play in inner ear hair cells and underlies the ability of stereocilia to convert electrical transduction current into useful mechanical work. We formulated a model of the stereocilia from first principles of physics based on stereocilia dimensions, the flexoelectric coefficient of lipid membranes, and the mechanical compliance. Remarkably, flexoelectric model results predict the phylogenetic correlation between stereocilia height and the tonotopic organization of hearing organs observed in nature, both within and across species. Results suggest that this fast hair-bundle motor mechanism is a key determinant in the exquisite sensitivity and frequency selectivity of non-mammalian hearing organs, and may contribute to the so-called “cochlear amplifier†in mammals3,4.

1 Tinevez, J. Y., Julicher, F., and Martin, P., Unifying the various incarnations of active hair-bundle motility by the vertebrate hair cell. Biophys J 93 (11), 4053 (2007).

2 Zhang, R. et al., Prestin modulates mechanics and electromechanical force of the plasma membrane. Biophys J 93 (1), L07 (2007); Qian, F. et al., Combining optical tweezers and patch clamp for studies of cell membrane electromechanics. Scientific Instruments 75 (9), 2937 (2004); Anvari, B. et al., Effects of prestin on membrane mechanics and electromechanics. Conf Proc IEEE Eng Med Biol Soc 1, 5384 (2007).

3 Hudspeth, A., Mechanical amplification of stimuli by hair cells. Curr Opin Neurobiol 7 (4), 480 (1997).

4 Fettiplace, R., Active hair bundle movements in auditory hair cells. J Physiol 576 (Pt 1), 29 (2006).