Enhancement of sensitivity gain and frequency tuning by coupling of active hair bundles

Abstract

The vertebrate inner ear possesses an active process that provides nonlinear amplification of mechanical stimuli. A candidate for this process is active hair bundle mechanics observed, for instance, for hair cells of the bullfrog's sacculus. Hair bundles in various inner ear organs are coupled by overlying membranes. Using a stochastic description of active hair bundle dynamics, we study the consequences of an elastic coupling on the properties of amplification. We report that collective effects in arrays of hair bundles can enhance the amplification gain and the sharpness of frequency tuning as compared with the performance of an isolated hair bundle. We also discuss the transient response elicited by the sudden onset of a periodic stimulus and its relation to temporal integration curves. Simulations of systems with a gradient of intrinsic frequencies show an enhanced amplification gain while preserving a frequency gradient, provided the coupling strength is similar to the hair bundle stiffness. We relate our findings to the situation in the bullfrog's sacculus and the mammalian cochlea.auditory amplifier ͉ hair cells ͉ nonlinear oscillators ͉ stochastic processes T he extraordinary ability of the vertebrate ear to detect sound stimuli over many orders of magnitude in sound amplitude relies on active processes. The key features of the auditory amplifier are (i) the amplification of weak stimuli, (ii) a compressive nonlinearity for stronger stimuli, (iii) frequency selectivity, and (iv) the generation of spontaneous emissions (1-3). All these properties could be understood as the consequence of nonlinear dynamic oscillators that operate in the ear (4-7).

Coupling a sensory hair-cell bundle to cyber clones enhances nonlinear amplification

“…Correlation between median values obtained from experiments and simulations was quantified by a Pearson test ( are tonotopically organized, neighboring hair bundles display slowly varying characteristics. As suggested previously (21) and demonstrated here, a regular organization favors a synergic enhancement of hair-cells performances through mechanical coupling. This inference may be especially relevant to some bats, which devote an extended region of the cochlea-called the acoustic fovea-to echolocation near the frequency of the bat's call.…”

“…Details of the simulation procedure have been previously published (21). Cyber clones are arranged on a square lattice of spacing L ¼ 50 μm and positioned according to their coordinates ði; jÞ in the xy plane, where i ¼ 1; …; M and j ¼ 1; …; M. Cyber clones are all oriented with their excitatory direction pointing toward positive X; we denote by X i;j the deflection of a cyber clone along this axis and ignore perpendicular deflections.…”

“…Thus, active oscillator modules might each recruit a group of coupled hair bundles. It was proposed on theoretical grounds that coupled hair bundles may cooperate to improve their performance (21).…”

Striated organelle, a cytoskeletal structure positioned to modulate hair-cell transduction

“…Much is known about their structure, their mechanical properties, and their geometric arrangement (1)(2)(3). These cells are embedded in the cuticular plate, a dense structure composed of an actin gel (4) located at the apical end of the hair cell, which is thought to act as a rigid platform, helping stereocilia return to their resting positions after stimulus-evoked displacements (5,6).…”

Horizontal Top Connectors Mediate a Sliding Adhesion to Hair Cell Stereocilia

“…Amplification by positive feedback can be degraded by mechanical noise such as Brownian motion, but parallel coupling between adjacent hair bundles through an otolithic or tectorial membrane can reduce noise to restore amplification and tuning [7]. The parallel coupling of transduction elements within a hair bundle by tight coupling between stereocilia has the same effect [16].…”