Dynamics of mechanically coupled hair-cell bundles of the inner ear

ABSTRACT The high sensitivity and effective frequency discrimination of sound detection performed by the auditory system rely on the dynamics of a system of hair cells. In the inner ear, these acoustic receptors are primarily attached to an overlying structure which provides mechanical coupling between the hair bundles. While the dynamics of individual hair bundles have been extensively investigated, the influence of mechanical coupling on the motility of the system of bundles remains underdetermined. We developed a technique of mechanically coupling two active hair bundles, enabling us to probe the dynamics of the coupled system experimentally. We demonstrated that the coupling could enhance the coherence of hair bundles’ spontaneous oscillation as well as their phase-locked response to sinusoidal stimuli, at the calcium concentration in the surrounding fluid near the physiological level. The empirical data were consistent with numerical results from a model of two coupled nonisochronous oscillators, each displaying a supercritical Hopf bifurcation. The model revealed that weak coupling can poise the system of unstable oscillators closer to the bifurcation by a shift in the critical point. In addition, the dynamics of strongly coupled oscillators far from criticality suggested that individual hair bundles may be regarded as nonisochronous oscillators. An optimal degree of nonisochronicity was required for the observed tuning behavior in the coherence of autonomous motion of the coupled system. STATEMENT OF SIGNIFICANCE Hair cells of the inner ear transduce acoustic energy into electrical signals via a deflection of hair bundles. Unlike a passive mechanical antenna, a free-standing hair bundle behaves as an active oscillator that can sustain autonomous oscillations, as well as amplify a low-level stimulus. Hair bundles under physiological conditions are elastically coupled to each other via an extracellular matrix. Therefore, the dynamics of coupled nonlinear oscillators underlie the performance of the peripheral auditory system. Despite extensive theoretical investigations, there are limited experimental evidence that support the significance of coupling on hair bundle motility. We develop a technique to mechanically couple hair bundles and demonstrate the benefits of coupling on hair bundle spontaneous motility.