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Piezo- and Flexoelectric Membrane Materials Underlie Fast Biological Motors in the Inner Ear

Published online by Cambridge University Press:  31 January 2011

Kathryn D Breneman  and
Richard D Rabbitt
Kathryn D Breneman
Affiliation:
kathryn.d.breneman@utah.edu, Univerisity of Utah, Bioengineering, SALT LAKE CITY, Utah, United States
Richard D Rabbitt
Affiliation:
r.rabbitt@utah.edurrabbitt@eng.utah.edu, Univerisity of Utah, Bioengineering, SALT LAKE CITY, Utah, United States
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Abstract

The mammalian inner ear is remarkably sensitive to quiet sounds, exhibits over 100dB dynamic range, and has the exquisite ability to discriminate closely spaced tones even in the presence of noise. This performance is achieved, in part, through active mechanical amplification of vibrations by sensory hair cells within the inner ear. All hair cells are endowed with a bundle of motile microvilli, stereocilia, located at the apical end of the cell, and the more specialized outer hair cells (OHC's) are also endowed with somatic electromotility responsible for changes in cell length in response to perturbations in membrane potential. Both hair bundle and somatic motors are known to feed energy into the mechanical vibrations in the inner ear. The biophysical origin and relative significance of the motors remains a subject of intense research. Several biological motors have been identified in hair cells that might underlie the motor(s), including a cousin of the classical ATP driven actin-myosin motor found in skeletal muscle. Hydrolysis of ATP, however, is much too slow to be viable at audio frequencies on a cycle-by-cycle basis. Heuristically, the OHC somatic motor behaves as if the OHC lateral wall membrane were a piezoelectric material and the hair bundle motor behaves as if the plasma membrane were a flexoelectric material. We propose these observations from a continuum materials perspective are literally true. To examine this idea, we formulated mathematical models of the OHC lateral wall “piezoelectric” motor and the more ubiquitous “flexoelectric” hair bundle motor. Plausible biophysical mechanisms underlying piezo- and flexoelectircity were established. Model predictions were compared extensively to the available data. The models were then applied to study the power conversion efficiency of the motors. Results show that the material properties of the complex membranes in hair cells provide them with the ability to convert electrical power available in the inner ear cochlea into useful mechanical amplification of sound induced vibrations at auditory frequencies. We also examined how hair cell amplification might be controlled by the brain through efferent synaptic contacts on hair cells and found a simple mechanism to tune hearing to signals of interest to the listener by electrical control of these motors.

Keywords

biomaterialpiezoelectricelectrical properties
Type
Research Article
Information
MRS Online Proceedings Library (OPL) , Volume 1186: Symposium JJ – Nanoscale Electromechanics and Piezoresponse Force Microscopy of Inorganic, Macromolecular and Biological Systems , 2009 , 1186-JJ06-04
Copyright
Copyright © Materials Research Society 2009

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References

1. Rabbitt, R. D., Clifford, S., Breneman, K. D., Farrell, B. F. and Brownell, W., PLoS Comput Biol. 5 (7):e1000444 (2009).10.1371/journal.pcbi.1000444Google Scholar
2. Hudspeth, A. J. and Gillespie, P. G., Neuron 12 (1), 1–9 (1994).10.1016/0896-6273(94)90147-3Google Scholar
3. Holt, J. R., Gillespie, S. K., Provance, D. W., Shah, K., Shokat, K. M., Corey, D. P., Mercer, J. A. and Gillespie, P. G., Cell 108 (3), 371–381 (2002).10.1016/S0092-8674(02)00629-3Google Scholar
4. Gillespie, P. G. and Cyr, J. L., Annu Rev Physiol 66, 521–545 (2004).10.1146/annurev.physiol.66.032102.112842Google Scholar
5. Matsumoto, N. and Kalinec, F., Biophys J 89 (6), 4343–4351 (2005).10.1529/biophysj.105.064626Google Scholar
6. Frolenkov, G. I., Mammano, F. and Kachar, B., Cell Calcium 33 (3), 185–195 (2003).10.1016/S0143-4160(02)00228-2Google Scholar
7. Brownell, W. E., Bader, C. R. B., D., and Ribaupierre, Y. De, Science 227, 194–196 (1985).10.1126/science.3966153Google Scholar
8. Kachar, B., Brownell, W. E., Altschuler, R. and Fex, J., Nature 322 (6077), 365–368 (1986).10.1038/322365a0Google Scholar
9. Petrov, A. G., in Physical and Chemical Basis of Biological Information Transfer, edited by V. J., (Plenum Press, New York, 1975), pp. 111–125.10.1007/978-1-4684-2181-1_9Google Scholar
10. Petrov, A. G., Biochim Biophys Acta 1561 (1), 1–25 (2002).10.1016/S0304-4157(01)00007-7Google Scholar
11. Petrov, A. G., Anal Chim Acta 568 (1-2), 70–83 (2006).10.1016/j.aca.2006.01.108Google Scholar
12. Raphael, R. M., Popel, A. S. and Brownell, W. E., Biophysical journal 78 (6), 2844–2862 (2000).10.1016/S0006-3495(00)76827-5Google Scholar
13. Spector, A. A., Brownell, W. E. and Popel, A. S., J Acoust Soc Am 113 (1), 453–461 (2003).10.1121/1.1526493Google Scholar
14. Rabbitt, R. D., Clifford, S., Breneman, K. D., Farrell, B. F. and Brownell, W., PLoS Comput Biol. 5 (7):e1000444 (2009).10.1371/journal.pcbi.1000444Google Scholar
15. Weiss, T., Cellular Biophysics. Vol. 2: Electrical Properties. (MIT Press, Cambridge, 1996).Google Scholar
16. Breneman, K., Brownell, W. E. and Rabbitt, R. D., PLoS One 4 (4): e5201(2009).10.1371/journal.pone.0005201Google Scholar
17. Murugasu, E. and Russell, I. J., J Neurosci 16 (1), 325–332 (1996).10.1523/JNEUROSCI.16-01-00325.1996Google Scholar
18. Russell, I. J. and Murugasu, E., J Acoust Soc Am 102 (3), 1734–1738 (1997).10.1121/1.420083Google Scholar
19. Liberman, M. C., Hearing research 3 (3), 189–204 (1980).10.1016/0378-5955(80)90046-5Google Scholar
20. Flock, A. and Russell, I., J Physiol 257 (1), 45–62 (1976).10.1113/jphysiol.1976.sp011355Google Scholar
21. Boyle, R., Rabbitt, R. and Highstein, S., J. Neurophysiol. 102 (3): 1513–25 (2009).10.1152/jn.91367.2008Google Scholar
22. Martin, P. and Hudspeth, A. J., Proc Natl Acad Sci U S A 96 (25), 14306–14311 (1999).10.1073/pnas.96.25.14306Google Scholar