Transduction Channels’ Gating Produce Friction Forces that Dominate Viscous Drag on Vibrating Hair-Cell Bundles

Abstract

Hearing begins when sound-evoked vibrations of the hair-cell bundle change the open probability of mechanosensitive transduction channels. A dynamic interplay between channel gating and Ca2+-dependent adaptation can give rise to spontaneous hair-bundle oscillations and frequency-selective amplification of sinusoidal inputs. As for any micromechanical device, friction is critical to the performance of the hair bundle. Here we performed dynamic force measurements to decipher the different contributions to hair-bundle friction.We used flexible glass fibers as force sensors to deflect single oscillatory hair bundles from the bullfrog's sacculus. In response to a symmetric triangular waveform of motion, the force-displacement relation followed a hysteretic cycle; friction forces were deduced from the cycle width along the force axis. At low velocities of bundle motion, friction could be negative, a signature of the active process that drives spontaneous hair-bundle oscillations. When moving at velocities high enough to outrun adaptation, however, we found that friction became positive with a maximum within the narrow region of displacements where the channels gate. Strikingly, friction was significantly reduced in the presence of a channel blocker (gentamicin). From this reduction, we estimated that channel gating contributed frictional forces 3-5 fold larger than those of hydrodynamic origin. In accordance with these measurements, increasing endolymph viscosity by thirty-fold had only a mild effect on active hair-bundle movements. A physical description of active hair-bundle mechanics that accounts for the finite activation kinetics of the transduction channels (τ ≌1 ms in frog) could quantitatively reproduce the data from both experiments.We conclude that transduction channels provide a major contribution to hair-bundle friction. Channel properties, but not endolymph viscosity, control damping of hair-bundle movements. Channel friction in turn helps setting the sensitivity and the characteristic frequency of the hair-bundle amplifier.