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Multiple-timescale dynamics underlying spontaneous oscillations of saccular hair bundles.

ABSTRACT: Spontaneous oscillations displayed by hair bundles of the bullfrog sacculus have complex temporal profiles, not fully captured by single limit-cycle descriptions. Quiescent intervals are typically interspersed with oscillations, leading to a bursting-type behavior. Temporal characteristics of the oscillation are strongly affected by imposing a mechanical load or by the application of a steady-state deflection to the resting position of the bundle. Separate spectral components of the spontaneous motility are differently affected by increases in the external calcium concentration. We use numerical modeling to explore the effects of internal parameters on the oscillatory profiles, and to reproduce the experimental modulation induced by mechanical or ionic manipulation.

SUBMITTER: Roongthumskul Y

PROVIDER: S-EPMC3145268 | biostudies-literature | 2011 Aug

REPOSITORIES: biostudies-literature

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Multiple-timescale dynamics underlying spontaneous oscillations of saccular hair bundles.

Roongthumskul Yuttana Y Fredrickson-Hemsing Lea L Kao Albert A Bozovic Dolores D

Biophysical journal 20110801 3

Spontaneous oscillations displayed by hair bundles of the bullfrog sacculus have complex temporal profiles, not fully captured by single limit-cycle descriptions. Quiescent intervals are typically interspersed with oscillations, leading to a bursting-type behavior. Temporal characteristics of the oscillation are strongly affected by imposing a mechanical load or by the application of a steady-state deflection to the resting position of the bundle. Separate spectral components of the spontaneous ...[more]

PMID: 21806928

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Project description:Hair cells of the inner ear can power spontaneous oscillations of their mechanosensory hair bundle, resulting in amplification of weak inputs near the characteristic frequency of oscillation. Recently, dynamic force measurements have revealed that delayed gating of the mechanosensitive ion channels responsible for mechanoelectrical transduction produces a friction force on the hair bundle. The significance of this intrinsic source of dissipation for the dynamical process underlying active hair-bundle motility has remained elusive. The aim of this work is to determine the role of friction in spontaneous hair-bundle oscillations. To this end, we characterized key oscillation properties over a large ensemble of individual hair cells and measured how viscosity of the endolymph that bathes the hair bundles affects these properties. We found that hair-bundle movements were too slow to be impeded by viscous drag only. Moreover, the oscillation frequency was only marginally affected by increasing endolymph viscosity by up to 30-fold. Stochastic simulations could capture the observed behaviors by adding a contribution to friction that was 3-8-fold larger than viscous drag. The extra friction could be attributed to delayed changes in tip-link tension as the result of the finite activation kinetics of the transduction channels. We exploited our analysis of hair-bundle dynamics to infer the channel activation time, which was ?1 ms. This timescale was two orders-of-magnitude shorter than the oscillation period. However, because the channel activation time was significantly longer than the timescale of mechanical relaxation of the hair bundle, channel kinetics affected hair-bundle dynamics. Our results suggest that friction from channel gating affects the waveform of oscillation and that the channel activation time can tune the characteristic frequency of the hair cell. We conclude that the kinetics of transduction channels' gating plays a fundamental role in the dynamic process that shapes spontaneous hair-bundle oscillations.

Dataset Information

Multiple-timescale dynamics underlying spontaneous oscillations of saccular hair bundles.

Publications

Multiple-timescale dynamics underlying spontaneous oscillations of saccular hair bundles.

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