  The detection of sound begins when energy derived from acoustic stimuli
deflects the hair bundles atop hair cells. As hair bundles move, the viscous
friction between stereocilia and the surrounding liquid poses a fundamental
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. Here we demonstrate that a
complementary part involves the fluid-structure interaction between the liquid
within the hair bundle and the stereocilia. 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 characterize the origin and magnitude of the
forces between individual stereocilia during small hair-bundle deflections. We
find 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, whereas the elastic horizontal top connectors
stabilize the structure, further reducing the drag. As measured from the
distortion products associated with channel gating at physiological stimulation
amplitudes of tens of nanometres, the balance of forces in a hair bundle
permits a relative mode of motion between adjacent stereocilia that encompasses
only a fraction of a nanometre. 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.
