Viscoelasticity in the ear's mechanoelectrical-transduction apparatus

The ear detects sounds so faint that they produce only atomic-scale displacements in the mechanoelectrical transducer, yet thermal noise causes fluctuations larger by an order of magnitude. Explaining how hearing can operate when the magnitude of the noise greatly exceeds that of the signal requires an understanding both of the transducer's micromechanics and of the associated noise. Using microrheology, we characterized the statistics of this noise; exploiting the fluctuation-dissipation theorem, we determined the associated micromechanics. The statistics revealed unusual Brownian motion in which the mean-square displacement increases as a fractional power of time, indicating that the mechanisms governing energy dissipation are related to those of energy storage. Although this anomalous scaling contradicts the canonical model of mechanoelectrical transduction, the results can be explained if the micromechanics incorporates the viscoelasticity characteristic of biopolymers. We amended the canonical model and demonstrate several consequences of viscoelasticity for sensory coding.

The left panel shows a scanning electron micrograph of a hair bundle from the bullfrog's sacculus. The axis of mechanosensitivity corresponds to the plane of the illustration; the direction of excitatory mechanical stimulation is to the right. The scale bar represents 2 µm. The transmission electron micrograph in the central panel portrays the tops of two stereocilia joined by an obliquely oriented tip link, which is thought to be attached at its lower insertion to two transduction channels. The scale bar represents 100 nm. In the right panel, the average power spectrum (red) for the thermal motion of 16 intact hair bundles displays a high-frequency slope near 1.75 (underlying black line) indicative of subdiffusive behavior. Cutting the tip links with BAPTA in 11 cells yields a spectrum (blue) with the limiting slope of 2 (underlying black line) characteristic of ordinary diffusion.