Sliding Adhesion Confers Coherent Motion to Hair Cell Stereocilia and Parallel Gating to Transduction Channels

When the tip of a hair bundle is deflected by a sensory stimulus, the stereocilia pivot as a unit, producing a shearing displacement between adjacent tips. It is not clear how stereocilia can stick together laterally but still shear. We used dissociated hair cells from the bullfrog saccule and high-speed video imaging to characterize this sliding adhesion. Movement of individual stereocilia was proportional to height, indicating that stereocilia pivot at their basal insertion points. All stereocilia moved by approximately the same angular deflection, and the same motion was observed at 1, 20, and 700 Hz stimulus frequency. Motions were consistent with a geometric model that assumes the stiffness of lateral links holding stereocilia together is >1000 times the pivot stiffness of stereocilia and that these links can slide in the plane of the membrane-in essence, that stereocilia shear without separation. The same motion was observed when bundles were moved perpendicular to the tip links, or when tip links, ankle links, and shaft connectors were cut, ruling out these links as the basis for sliding adhesion. Stereocilia rootlets are angled toward the center of the bundle, tending to push stereocilia tips together for small deflections. However, stereocilia remained cohesive for deflections of up to +/- 35 degrees, ruling out rootlet prestressing as the basis for sliding adhesion. These observations suggest that horizontal top connectors mediate a sliding adhesion. They also indicate that all transduction channels of a hair cell are mechanically in parallel, an arrangement that may enhance amplification in the inner ear.