Unifying the Various Incarnations of Active Hair-Bundle Motility by the Vertebrate Hair Cell

Abstract

The dazzling sensitivity and frequency selectivity of the vertebrate ear rely on mechanical amplification of the hair cells' responsiveness to small stimuli. As revealed by spontaneous oscillations and forms of mechanical excitability in response to force steps, the hair bundle that adorns each hair cell is both a mechanosensory antenna and a force generator that might participate in the amplificatory process. To study the various incarnations of active hair-bundle motility, we combined Ca(2+) iontophoresis with mechanical stimulation of single hair bundles from the bullfrog's sacculus. We identified three classes of active hair-bundle movements: a hair bundle could be quiescent but display nonmonotonic twitches in response to either excitatory or inhibitory force steps, or oscillate spontaneously. Extracellular Ca(2+) changes could affect the kinetics of motion and, when large enough, evoke transitions between the three classes of motility. We found that the Ca(2+)-dependent location of a bundle's operating point within its force-displacement relation controlled the type of movement observed. In response to an iontophoretic pulse of Ca(2+) or of a Ca(2+) chelator, a hair bundle displayed a movement whose polarity could be reversed by applying a static bias to the bundle's position at rest. Moreover, such polarity reversal was accompanied by a 10-fold change in the kinetics of the Ca(2+)-evoked hair-bundle movement. A unified theoretical description, in which mechanical activity stems solely from myosin-based adaptation, could account for the fast and slow manifestations of active hair-bundle motility observed in frog, as well as in auditory organs of the turtle and the rat.

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

“…We discuss properties of spontaneous oscillations and of the nonlinear amplification in response to mechanical stimulation of coupled hair bundles as a function of the coupling strength. Individual hair bundles in the group are described by a simple stochastic model (23,26) that takes into account random fluctuations and can capture the noise-limited amplification gain of a single hair bundle. Because this example is best studied, we choose parameters that correspond to hair bundles observed in the sacculus of the bullfrog.…”

“…Because this example is best studied, we choose parameters that correspond to hair bundles observed in the sacculus of the bullfrog. The same model, however with different parameters, could also be used to describe hair bundles in the cochlea (26).…”

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

“…Hair cells, the sensory receptors in the inner ear, can power active mechanical movements of their mechano-sensitive hair bundle, including spontaneous oscillations (11)(12)(13)(14)(15)(16). Although active hair-bundle motility provides a plausible component of the active process in vivo, amplification at the scale of a single hair bundle (10) is much less effective than the active process in an intact organ (17).…”

Amplifying effect of a release mechanism for fast adaptation in the hair bundle

“…However, it is clear that this property is not specific to this particular release model but is generic to any relaxation mechanism. One such example is the model proposed by Tinevez et al ͑2007͒, which posits that fast adaptation is an epiphenomenon that arises from an interplay between gating of the MET channel and the myosin motor that is responsible for slow adaptation. It includes viscoelastic relaxation and relaxation involving the movement of the myosin motor.…”