Forces between clustered stereocilia minimize friction in the ear

The detection of sound begins when energy derived from an acoustic stimulus deflects the hair bundles atop hair cells. As the bundles move, the viscous friction between stereocilia and the surrounding liquid poses a fundamental physical challenge to the ear's high sensitivity and sharp frequency selectivity. Part of the solution to this problem lies in the active process that uses energy for frequency-selective sound amplification. We demonstrated that a complementary aspect involves the fluid-structure interaction between stereocilia and the liquid within the hair bundle. Using force measurement on a dynamically scaled model, finite-element analysis, analytical estimation of hydrodynamic forces, stochastic simulation, and high-resolution interferometric measurement of hair bundles, we characterized the origin and magnitude of the forces between individual stereocilia during small hair-bundle deflections. We determined that the close apposition of stereocilia effectively immobilizes the liquid between them, which reduces the drag and suppresses the relative squeezing but not the sliding mode of stereociliary motion. The obliquely oriented tip links couple the mechanotransduction channels to this least dissipative, coherent mode; the elastic horizontal top connectors that stabilize the structure further reduce the drag. As measured from the distortion products associated with channel gating at physiological stimulation amplitudes of tens of nanometers, the balance of viscous and elastic forces in a hair bundle permits a relative mode of motion between adjacent stereocilia that encompasses only a fraction of a nanometer. A combination of high-resolution experiments and detailed numerical modelling of fluid-structure interactions reveals the physical principles behind the basic structural features of hair bundles and shows quantitatively how these organelles are adapted to the needs of sensitive mechanotransduction.

Three top views illustrate the calculated motion of the components of a hair bundle without elastic elements other than the kinociliary links and rootlets in response to sinusoidal deflections of the kinocilium, which lies at the right in each diagram. As the frequency increases, the stereocilia display a transition from weakly coupled to collective motion as a result of hydrodynamic interactions. The color scale identifies successive positions through one cycle of stimulation with phase progressing counterclockwise.