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Motility-associated hair-bundle motion in mammalian outer hair cells

Nature Neuroscience volume 8, pages 1028–1034 (2005)Cite this article

Abstract

Mammalian hearing owes its remarkable sensitivity and frequency selectivity to a local mechanical feedback process within the cochlea. Cochlear outer hair cells (OHCs) function as the key elements in the feedback loop in which the fast somatic motility of OHCs is thought to be the source of cochlear amplification. An alternative view is that amplification arises from active hair-bundle movement, similar to that seen in nonmammalian hair cells. We measured voltage-evoked hair-bundle motions in the gerbil cochlea to determine if such movements were also present in mammalian OHCs. The OHCs showed bundle movement with peak responses of up to 830 nm. The movement was insensitive to manipulations that would normally block mechanotransduction in the stereocilia, and it was absent in neonatal OHCs and prestin-knockout OHCs. These findings suggest that the bundle movement originated in somatic motility and that somatic motility has a central role in cochlear amplification in mammals.

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Figure 1: Mechanotransducer current and hair-bundle motion of gerbil OHCs.
Figure 2: Hair-bundle motion of neonatal gerbil OHCs and mouse OHCs.
Figure 3: Hair-bundle motion measured from a stimulated OHC and an adjacent unstimulated OHC.
Figure 4: Input-output function and frequency response of hair-bundle motion.
Figure 5: Relationship between OHC somatic motility and hair-bundle motion.

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Acknowledgements

This work was supported by grants R01 DC 006496 and R21 DC 006039 to D.Z.Z.H. from the National Institutes on Deafness and Other Communicative Disorders (NIDCD). We would like to thank P. Dallos, S. Neely, M.A. Cheatham and R. Hallworth for many helpful discussions and comments on an earlier draft of the manuscript. We thank J. Zuo for providing the prestin-knockout mice.

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  1. Department of Biomedical Sciences, Hair Cell Biophysics Laboratory, Creighton University School of Medicine, 2500 California Plaza, Omaha, 68175, Nebraska, USA

    Shuping Jia & David Z Z He

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Correspondence to David Z Z He.

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Supplementary information

Supplementary Video 1

The video clip shows large hair-bundle motion of an adult gerbil OHC in response to membrane potential change. The recording was made from an OHC in the apical-turn of the cochlea. The bundle behaved as light pipes and appeared as bright V-shaped lines when focused at their tips under the bright-field illumination (the image was magnified by 1,260x). The cell was held at -70 mV under the whole-cell voltage-clamp condition. Voltage steps (200 ms in duration) were applied to the cell to depolarize and hyperpolarize the cell membrane between -150 and 10 mV from the holding potential. Three important features are apparent in the videos. The first one is the magnitude of the bundle motion. One can roughly estimate the magnitude of bundle motion of OHCs by using the reference of the diameter of each stereocilium. The diameter of stereocilium is about 200-250 nm in OHCs. So the thickness of the white “V” line is about 750 nm (3 rows of stereocilia). Note that the magnitude of bundle motion during voltage stimulation is greater than the thickness of the white “V” line. That is to say, the bundle motion of OHCs is larger than 750 nm. The second feature is the motion pattern of the bundle. One can easily see that the entire hair bundle (both the base and the tip of the bundle) is moving, along with the cuticular plate (motion of the cuticular plate is evident by the movement of the background in the video). This is very different from the ciliary rotation seen in non-mammalian hair cells. The third feature is that the bundle motion is asymmetrical with depolarization evoking larger bundle motions in the direction toward the tallest stereocilia than hyperpolarization in the opposite direction. (AVI 1659 kb)

Supplementary Video 2

Another example of hair bundle motion of an adult gerbil OHC. The recording was made from an OHC in the basal-turn region of the cochlea. (AVI 1032 kb)

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Jia, S., He, D. Motility-associated hair-bundle motion in mammalian outer hair cells. Nat Neurosci 8, 1028–1034 (2005). https://doi.org/10.1038/nn1509

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