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The Journal of Neuroscience, March 8, 2006, 26(10):2757-2766; doi:10.1523/JNEUROSCI.3808-05.2006

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Cellular/Molecular
Depolarization of Cochlear Outer Hair Cells Evokes Active Hair Bundle Motion by Two Mechanisms

Helen J. Kennedy,¹ Michael G. Evans,² Andrew C. Crawford,³ and Robert Fettiplace¹

¹Department of Physiology, University of Wisconsin Medical School, Madison, Wisconsin 53706, ²MacKay Institute of Communication and Neuroscience, School of Life Sciences, Keele University, Staffs ST5 5BG, United Kingdom, and ³Department of Physiology, Cambridge University, Cambridge CB2 3EG, United Kingdom

Correspondence should be addressed to Robert Fettiplace, 185 Medical Sciences Building, 1300 University Avenue, Madison, WI 53706. Email: fettiplace{at}physiology.wisc.edu

There is current debate about the origin of mechanical amplification whereby outer hair cells generate force to augment the sensitivity and frequency selectivity of the mammalian cochlea. To distinguish contributions to force production from the mechanotransducer (MET) channels and somatic motility, we have measured hair bundle motion during depolarization of individual outer hair cells in isolated rat cochleas. Depolarization evoked rapid positive bundle deflections that were reduced by perfusion with the MET channel blocker dihydrostreptomycin, with no effect on the nonlinear capacitance that is a manifestation of prestin-driven somatic motility. However, the movements were also diminished by Na salicylate and depended on the intracellular anion, properties implying involvement of the prestin motor. Furthermore, depolarization of one outer hair cell caused motion of neighboring hair bundles, indicating overall motion of the reticular lamina. Depolarization of solitary outer hair cells caused cell-length changes whose voltage-activation range depended on the intracellular anion but were insensitive to dihydrostreptomycin. These results imply that both the MET channels and the somatic motor participate in hair bundle motion evoked by depolarization. It is conceivable that the two processes can interact, a signal from the MET channels being capable of modulating the activity of the prestin motor.

Key words: anion; dihydrostreptomycin; cochlea; calcium; mechanosensory; hair cell

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Received Sept. 8, 2005; revised Jan. 15, 2006; accepted Jan. 16, 2006.

Correspondence should be addressed to Robert Fettiplace, 185 Medical Sciences Building, 1300 University Avenue, Madison, WI 53706. Email: fettiplace{at}physiology.wisc.edu

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