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The Journal of Neuroscience, August 24, 2005, 25(34):7831-7839; doi:10.1523/JNEUROSCI.1127-05.2005

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Cellular/Molecular
The Transduction Channel Filter in Auditory Hair Cells

Anthony J. Ricci,¹ Helen J. Kennedy,² Andrew C. Crawford,³ and Robert Fettiplace²

¹Center for Neuroscience, Louisiana State University Medical Center, New Orleans, Louisiana 70112, ²Department of Physiology, University of Wisconsin Medical School, Madison, Wisconsin 53706, and ³Department of Physiology, Cambridge University, Cambridge CB2 3EG, United Kingdom

In the first step in auditory transduction, sound-induced vibrations of the stereociliary bundles on the sensory hair cells are converted into electrical signals by opening of mechanotransducer channels. Faithful transduction and hence auditory performance will be limited by the kinetic properties of these channels. We have measured the time course of mechanotransducer currents in turtle and rat auditory hair cells during rapid deflections of the hair bundle. Current activation in the turtle had a time constant that decreased 10-fold with stimulus amplitude to a limiting value of 50 µs. Lowering the external Ca²⁺ concentration slowed both activation and adaptation time constants. Similar effects were seen in hair cells tuned to low and high frequencies, but the overall kinetics was slower in low-frequency cells. In rat outer hair cells, the time courses of both activation and adaptation were at least 10-fold faster. Although activation kinetics was too fast to characterize accurately, the adaptation time constants in the rat, like the turtle, were Ca²⁺ dependent and faster in hair cells tuned to higher frequencies. The results imply that mechanotransducer channels operate similarly in turtle and rat but are faster in the mammal to accommodate its higher frequency range of hearing. We suggest that the kinetics of channel activation and adaptation imposes a bandpass filter on transduction, with a center frequency matched to the frequencies detected by the hair cell, which may improve the signal-to-noise ratio near threshold.

Key words: calcium; fast adaptation; electrical resonance; mechanosensitive channels; outer hair cells; rat; signal-to-noise ratio; stereociliary bundle

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Received March 22, 2005; revised June 27, 2005; accepted July 14, 2005.

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