Adaptive Shift in the Domain of Negative Stiffness during Spontaneous Oscillation by Hair Bundles from the Internal Ear

When a hair cell of the bullfrog's sacculus is maintained in vitro under native ionic conditions, its mechanosensitive hair bundle may oscillate spontaneously. This movement has been hypothesized to result from the interaction of the bundle's negative stiffness, which creates a region of mechanical instability, with a myosin-based adaptation mechanism that continually repositions the bundle there. To test this proposition, we used a flexible stimulus fiber in an analog feedback loop to measure the displacement-force relation of an oscillating hair bundle. A digital signal processor was used to monitor spontaneous oscillations in real time and trigger measurements at particular phases of the movement cycle. By comparing the displacement-force curves obtained at the two extremes of a hair bundle's motion, we demonstrated a shift in the negative-stiffness region whose direction, orientation, magnitude, and kinetics agreed with the predictions of the gating-spring theory. The results are in accordance with the idea that adaptation underlies spontaneous hair-bundle oscillation, and therefore powers the active process that also amplifies and tunes the hair cell's mechanical responsiveness.