The diverse effects of mechanical loading on active hair bundles

Hair cells in the auditory, vestibular, and lateral-line systems of vertebrates receive inputs through a remarkable variety of accessory structures that impose complex mechanical loads on the mechanoreceptive hair bundles. Although the physiological and morphological properties of the hair bundles in each organ are specialized for detecting the relevant inputs, we propose that the mechanical load on the bundles also adjusts their responsiveness to external signals. We used a parsimonious description of active hair-bundle motility to show how the mechanical environment can regulate a bundle's innate behavior and response to input. We found that an unloaded hair bundle can behave very differently from one subjected to a mechanical load. Depending on how it is loaded, a hair bundle can function as a switch, active oscillator, quiescent resonator, or low-pass filter. Moreover, a bundle displays a sharply tuned, nonlinear, and sensitive response for some loading conditions and an untuned or weakly tuned, linear, and insensitive response under other circumstances. Our simple characterization of active hair-bundle motility explains qualitatively most of the observed features of bundle motion from different organs and organisms. The predictions stemming from this description provide insight into the operation of hair bundles in a variety of contexts.

The left panel shows the state diagram for a simple model of an active hair bundle, whose behavior is parameterized by the system's total stiffness k and the external load force Fc. Operation of a bundle with a parameter set within the loop of Hopf bifurcations (red) corresponds to spontaneous oscillation, whereas the lines of saddle-node bifurcations (blue) delineate a region of bistability. In the central panel, the normalized amplitudes of spontaneous oscillations, which are encoded by a color spectrum within the "head" of the fishlike state diagram, range from zero (red) to 1.77 (violet). The right panel shows that the normalized frequencies of spontaneous oscillations vary from 0.06 (red) to 0.41 (violet).