Sound-evoked deflections of outer hair cell stereocilia arise from tectorial membrane anisotropy

The exceptional performance of mammalian hearing is due to the cochlea's amplification of sound-induced mechanical stimuli. During acoustic stimulation, the vertical motion of the outer hair cells relative to the tectorial membrane (TM) is converted into the lateral motion of their stereocilia. The actual mode of this conversion, which represents a fundamental step in hearing, remains enigmatic, as it is unclear why the stereocilia are deflected when pressed against the TM, rather than penetrating it. In this study we show that deflection of the stereocilia is a direct outcome of the anisotropic material properties of the TM. Using force spectroscopy, we find that the vertical stiffness of the TM is significantly larger than its lateral stiffness. As a result, the TM is more resistant to the vertical motion of stereocilia than to their lateral motion, and so they are deflected laterally when pushed against the TM. Our findings are confirmed by finite element simulations of the mechanical interaction between the TM and stereocilia, which show that the vertical outer hair cells motion is converted into lateral stereocilia motion when the experimentally determined stiffness values are incorporated into the model. Our results thus show that the material properties of the TM play a central and previously unknown role in mammalian hearing.