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

Jean-Yves Tinevez ^*, Frank Jülicher  and Pascal Martin ^*

^* Laboratoire Physico-Chimie Curie, CNRS, Institut Curie, Paris, France; and Max-Planck-Institute for the Physics of Complex Systems, Dresden, Germany

Correspondence: Address reprint requests to Dr. P. Martin, Laboratoire Physico-Chimie Curie, Institut Curie recherche, 26 rue d'Ulm, 75248 Paris cedex 05, France. Tel.: 33-1-42-34-67-48; Fax: 33-1-40-51-06-36; E-mail: pascal.martin{at}curie.fr.

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 Ca²⁺ 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 Ca²⁺ changes could affect the kinetics of motion and, when large enough, evoke transitions between the three classes of motility. We found that the Ca²⁺-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 Ca²⁺ or of a Ca²⁺ 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 Ca²⁺-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.

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