Compressive nonlinearity in the hair bundle’s active response to mechanical stimulation

P. Martin*† and A. J. Hudspeth*

Proc Natl Acad Sci USA 2001 Dec 4;98(25):14386-91

*Howard Hughes Medical Institute and Laboratory of Sensory Neuroscience, The Rockefeller University, 1230 York Avenue, New York, NY 10021-6399; and
†Laboratoire Physico-Chimie Curie, Unité Mixte de Recherche 168, Institut Curie, 26 rue d’Ulm, F-75248 Paris Cedex 05, France
Contributed by A. J. Hudspeth, October 5, 2001

Abstract:

The auditory system's ability to interpret sounds over a wide range of amplitudes rests on the nonlinear responsiveness of the ear. Whether measured by basilar-membrane vibration, nerve-fiber activity, or perceived loudness, the ear is most sensitive to small signals and grows progressively less responsive as stimulation becomes stronger. Seeking a correlate of this behavior at the level of mechanoelectrical transduction, we examined the responses of hair bundles to direct mechanical stimulation. As reported by the motion of an attached glass fiber, an active hair bundle from the bullfrog's sacculus oscillates spontaneously. Sinusoidal movement of the fiber's base by as little as +/-1 nm, corresponding to the application at the bundle's top of a force of +/-0.3 pN, causes detectable phase-locking of the bundle's oscillations to the stimulus. Although entrainment increases as the stimulus grows, the amplitude of the hair-bundle movement does not rise until phase-locking is nearly complete. A bundle is most sensitive to stimulation at its frequency of spontaneous oscillation. Far from that frequency, the sensitivity of an active hair bundle resembles that of a passive bundle. Over most of its range, an active hair bundle's response grows as the one-third power of the stimulus amplitude; the bundle's sensitivity declines accordingly in proportion to the negative two-thirds power of the excitation. This scaling behavior, also found in the response of the mammalian basilar membrane to sound, signals the operation of an amplificatory process at the brink of an oscillatory instability, a Hopf bifurcation.
(Bold text emphasis by Martin Braun)

Comment:

Martin and Hudspeth observed that a hair bundle's response at threshold was not an increase in oscillation amplitude, but an increase in phase locking to the stimulus. It remains to be seen if the same behavior can be observed in mammalian cochlear hair cells. If yes, we would have a definite proof that spontaneous oscillations of tuned hair cells are functional for our low threshold of hearing. (Comment Martin Braun)

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