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. 1985 Jul;364:359–379. doi: 10.1113/jphysiol.1985.sp015750

The mechanical properties of ciliary bundles of turtle cochlear hair cells.

A C Crawford, R Fettiplace
PMCID: PMC1192975  PMID: 4032304

Abstract

The mechanical behaviour of the ciliary bundles of hair cells in the turtle cochlea was examined by deflecting them with flexible glass fibres of known compliance during simultaneous intracellular recording of the cell's membrane potential. Bundle motion was monitored through the attached fibre partially occluding a light beam incident on a photodiode array. The change in photocurrent was assumed to be proportional to bundle displacement. For deflexions of 1-100 nm towards the kinocilium, the stiffness of the ciliary bundles was estimated as about 6 X 10(-4) N/m, with the fibre attached to the top of the bundle. When the fibre was placed at different positions up the bundle, the stiffness decreased approximately as the inverse square of the distance from the ciliary base. This suggests that the bundles rotate about an axis close to the apical pole of the cell and have a rotational stiffness of about 2 X 10(-14) N. m/rad. Step displacements of the fixed end of the flexible fibre caused the hair cell's membrane potential to execute damped oscillations; the frequency of the oscillations in different cells ranged from 20 to 320 Hz. Displacements towards the kinocilium always produced membrane depolarization. The amplitude of the initial oscillation increased with displacements up to 100 nm and then saturated. For small displacements of a few nanometres, the hair cell's mechanoelectrical sensitivity was estimated as about 0.2 mV/nm. Force steps delivered by the flexible fibre caused the bundle position to undergo damped oscillations in synchrony with the receptor potential. The mechanical oscillations could be abolished with large depolarizing currents that attenuated the receptor potential. When placed against a bundle, a fibre's spontaneous motion increased and became quasi-sinusoidal with an amplitude several times that expected from the compliance of the system. It is suggested that the hair bundle drives the fibre. We conclude that turtle cochlear hair cells contain an active force generating mechanism.

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Selected References

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  1. Ashmore J. F. Frequency tuning in a frog vestibular organ. Nature. 1983 Aug 11;304(5926):536–538. doi: 10.1038/304536a0. [DOI] [PubMed] [Google Scholar]
  2. Brownell W. E. Microscopic observation of cochlear hair cell motility. Scan Electron Microsc. 1984;(Pt 3):1401–1406. [PubMed] [Google Scholar]
  3. Corey D. P., Hudspeth A. J. Analysis of the microphonic potential of the bullfrog's sacculus. J Neurosci. 1983 May;3(5):942–961. doi: 10.1523/JNEUROSCI.03-05-00942.1983. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Corey D. P., Hudspeth A. J. Ionic basis of the receptor potential in a vertebrate hair cell. Nature. 1979 Oct 25;281(5733):675–677. doi: 10.1038/281675a0. [DOI] [PubMed] [Google Scholar]
  5. Corey D. P., Hudspeth A. J. Mechanical stimulation and micromanipulation with piezoelectric bimorph elements. J Neurosci Methods. 1980 Dec;3(2):183–202. doi: 10.1016/0165-0270(80)90025-4. [DOI] [PubMed] [Google Scholar]
  6. Crawford A. C., Fettiplace R. An electrical tuning mechanism in turtle cochlear hair cells. J Physiol. 1981 Mar;312:377–412. doi: 10.1113/jphysiol.1981.sp013634. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Crawford A. C., Fettiplace R. Auditory nerve responses to imposed displacements of the turtle basilar membrane. Hear Res. 1983 Nov;12(2):199–208. doi: 10.1016/0378-5955(83)90106-5. [DOI] [PubMed] [Google Scholar]
  8. Crawford A. C., Fettiplace R. Non-linearities in the responses of turtle hair cells. J Physiol. 1981 Jun;315:317–338. doi: 10.1113/jphysiol.1981.sp013750. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Crawford A. C., Fettiplace R. The frequency selectivity of auditory nerve fibres and hair cells in the cochlea of the turtle. J Physiol. 1980 Sep;306:79–125. doi: 10.1113/jphysiol.1980.sp013387. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Drenckhahn D., Kellner J., Mannherz H. G., Gröschel-Stewart U., Kendrick-Jones J., Scholey J. Absence of myosin-like immunoreactivity in stereocilia of cochlear hair cells. Nature. 1982 Dec 9;300(5892):531–532. doi: 10.1038/300531a0. [DOI] [PubMed] [Google Scholar]
  11. Flock A., Flock B., Murray E. Studies on the sensory hairs of receptor cells in the inner ear. Acta Otolaryngol. 1977 Jan-Feb;83(1-2):85–91. doi: 10.3109/00016487709128817. [DOI] [PubMed] [Google Scholar]
  12. Hudspeth A. J., Corey D. P. Sensitivity, polarity, and conductance change in the response of vertebrate hair cells to controlled mechanical stimuli. Proc Natl Acad Sci U S A. 1977 Jun;74(6):2407–2411. doi: 10.1073/pnas.74.6.2407. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Itoh M. Preservation and visualization of actin-containing filaments in the apical zone of cochlear sensory cells. Hear Res. 1982 Apr;6(3):277–289. doi: 10.1016/0378-5955(82)90060-0. [DOI] [PubMed] [Google Scholar]
  14. Kemp D. T. Evidence of mechanical nonlinearity and frequency selective wave amplification in the cochlea. Arch Otorhinolaryngol. 1979;224(1-2):37–45. doi: 10.1007/BF00455222. [DOI] [PubMed] [Google Scholar]
  15. Khanna S. M., Leonard D. G. Basilar membrane tuning in the cat cochlea. Science. 1982 Jan 15;215(4530):305–306. doi: 10.1126/science.7053580. [DOI] [PubMed] [Google Scholar]
  16. Lewis R. S., Hudspeth A. J. Voltage- and ion-dependent conductances in solitary vertebrate hair cells. Nature. 1983 Aug 11;304(5926):538–541. doi: 10.1038/304538a0. [DOI] [PubMed] [Google Scholar]
  17. Macartney J. C., Comis S. D., Pickles J. O. Is myosin in the cochlea a basis for active motility? Nature. 1980 Dec 4;288(5790):491–492. doi: 10.1038/288491a0. [DOI] [PubMed] [Google Scholar]
  18. Miller M. R. Scanning electron microscope studies of the papilla basilaris of some turtles and snakes. Am J Anat. 1978 Mar;151(3):409–435. doi: 10.1002/aja.1001510306. [DOI] [PubMed] [Google Scholar]
  19. Oosawa F. The flexibility of F-actin. Biophys Chem. 1980 Jun;11(3-4):443–446. doi: 10.1016/0301-4622(80)87021-9. [DOI] [PubMed] [Google Scholar]
  20. Pickles J. O., Comis S. D., Osborne M. P. Cross-links between stereocilia in the guinea pig organ of Corti, and their possible relation to sensory transduction. Hear Res. 1984 Aug;15(2):103–112. doi: 10.1016/0378-5955(84)90041-8. [DOI] [PubMed] [Google Scholar]
  21. Rhode W. S. Some observations on cochlear mechanics. J Acoust Soc Am. 1978 Jul;64(1):158–176. doi: 10.1121/1.381981. [DOI] [PubMed] [Google Scholar]
  22. Sellick P. M., Patuzzi R., Johnstone B. M. Measurement of basilar membrane motion in the guinea pig using the Mössbauer technique. J Acoust Soc Am. 1982 Jul;72(1):131–141. doi: 10.1121/1.387996. [DOI] [PubMed] [Google Scholar]
  23. Shotwell S. L., Jacobs R., Hudspeth A. J. Directional sensitivity of individual vertebrate hair cells to controlled deflection of their hair bundles. Ann N Y Acad Sci. 1981;374:1–10. doi: 10.1111/j.1749-6632.1981.tb30854.x. [DOI] [PubMed] [Google Scholar]
  24. Strelioff D., Flock A. Stiffness of sensory-cell hair bundles in the isolated guinea pig cochlea. Hear Res. 1984 Jul;15(1):19–28. doi: 10.1016/0378-5955(84)90221-1. [DOI] [PubMed] [Google Scholar]
  25. Tilney L. G., Derosier D. J., Mulroy M. J. The organization of actin filaments in the stereocilia of cochlear hair cells. J Cell Biol. 1980 Jul;86(1):244–259. doi: 10.1083/jcb.86.1.244. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Tilney L. G., Saunders J. C., Egelman E., DeRosier D. J. Changes in the organization of actin filaments in the stereocilia of noise-damaged lizard cochleae. Hear Res. 1982 Jul;7(2):181–197. doi: 10.1016/0378-5955(82)90013-2. [DOI] [PubMed] [Google Scholar]
  27. Weiss T. F. Bidirectional transduction in vertebrate hair cells: a mechanism for coupling mechanical and electrical processes. Hear Res. 1982 Aug;7(3):353–360. doi: 10.1016/0378-5955(82)90045-4. [DOI] [PubMed] [Google Scholar]

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