Journal of Neurophysiology, Vol 70, Issue 1 299-323, Copyright © 1993 by APS

ARTICLES

Theory of electrically driven shape changes of cochlear outer hair cells

P. Dallos, R. Hallworth and B. N. Evans
Auditory Physiology Laboratory (The Hugh Knowles Center), Northwestern University, Evanston, Illinois 60208.

1. A theory of cochlear outer hair cell electromotility is developed and specifically applied to somatic shape changes elicited in a microchamber. The microchamber permits the arbitrary electrical and mechanical partitioning of the outer hair cell along its length. This means that the two partitioned segments are stimulated with different input voltages and undergo different shape changes. Consequently, by imposing more constraints than other methods, experiments in the microchamber are particularly suitable for testing different theories of outer hair cell motility. 2. The present model is based on simple hypotheses. They include a distributed motor associated with the cell membrane or cortex and the assumption that the displacement generated by the motor is related to the transmembrane voltage across the associated membrane element. It is expected that the force generated by the motor is counterbalanced by an elastic restoring force indigenous to the cell membrane and cortex, and a tensile force due to intracellular pressure. It is assumed that all changes take place while total cell volume is conserved. The above elements of the theory taken together permit the development of qualitative and quantitative predictions about the expected motile responses of both partitioned segments of the cell. Only a DC treatment is offered here. 3. Both a linear motor and an expanded treatment that incorporates a stochastic molecular motor model are considered. The latter is represented by a two-state Boltzmann process. We show that the linear motor treatment is an appropriate extrapolation of the stochastic motor theory for the case of small voltage driving signals. Comparison of experimental results with model responses permits the estimation of model parameters. Good match of data is obtained if it is assumed that the molecular motors undergo conformational length changes of 0.7-1.0 nm, that they have an effective displacement vector at approximately -20 degrees with the long axis of the cell, and that their linear density is approximately 80/microns. 4. An effort is made to parcel out motile response components that are a direct consequence of the motor action from those that are mediated by cytoplasmic pressure changes brought about by the concerted action of the motors. We show that pressure effects are of minor importance, and thus rule out models that rely on radial constriction/expansion-mediated internal pressure change as the primary cause of longitudinal motility. 5. As a consequence of the interaction between the Boltzmann process and the mechanical characteristics of the cell, the electromotile response is asymmetric.(ABSTRACT TRUNCATED AT 400 WORDS)

This article has been cited by other articles:

				J. Ashmore Cochlear Outer Hair Cell Motility Physiol Rev, January 1, 2008; 88(1): 173 - 210. [Abstract] [Full Text] [PDF]

				J. Fang and K. H. Iwasa Effects of Chlorpromazine and Trinitrophenol on the Membrane Motor of Outer Hair Cells Biophys. J., September 1, 2007; 93(5): 1809 - 1817. [Abstract] [Full Text] [PDF]

				J. Gao, X. Wang, X. Wu, S. Aguinaga, K. Huynh, S. Jia, K. Matsuda, M. Patel, J. Zheng, M. Cheatham, et al. Prestin-based outer hair cell electromotility in knockin mice does not appear to adjust the operating point of a cilia-based amplifier PNAS, July 24, 2007; 104(30): 12542 - 12547. [Abstract] [Full Text] [PDF]

				D. Muallem and J. Ashmore An Anion Antiporter Model of Prestin, the Outer Hair Cell Motor Protein Biophys. J., June 1, 2006; 90(11): 4035 - 4045. [Abstract] [Full Text] [PDF]

				E. G. Navarrete and J. Santos-Sacchi On the Effect of Prestin on the Electrical Breakdown of Cell Membranes Biophys. J., February 1, 2006; 90(3): 967 - 974. [Abstract] [Full Text] [PDF]

				N. Matsumoto and F. Kalinec Extraction of Prestin-Dependent and Prestin-Independent Components from Complex Motile Responses in Guinea Pig Outer Hair Cells Biophys. J., December 1, 2005; 89(6): 4343 - 4351. [Abstract] [Full Text] [PDF]

				M. P. Scherer and A. W. Gummer How Many States Can the Motor Molecule, Prestin, Assume in an Electric Field? Biophys. J., May 1, 2005; 88(5): L27 - L29. [Abstract] [Full Text] [PDF]

				M. P. Scherer and A. W. Gummer Impedance Analysis of the Organ of Corti with Magnetically Actuated Probes Biophys. J., August 1, 2004; 87(2): 1378 - 1391. [Abstract] [Full Text] [PDF]

				M. Ospeck, X.-x. Dong, and K. H. Iwasa Limiting Frequency of the Cochlear Amplifier Based on Electromotility of Outer Hair Cells Biophys. J., February 1, 2003; 84(2): 739 - 749. [Abstract] [Full Text] [PDF]

				G. A. Manley Evidence for an Active Process and a Cochlear Amplifier in Nonmammals J Neurophysiol, August 1, 2001; 86(2): 541 - 549. [Abstract] [Full Text] [PDF]

				J. Ludwig, D. Oliver, G. Frank, N. Klocker, A. W. Gummer, and B. Fakler Reciprocal electromechanical properties of rat prestin: The motor molecule from rat outer hair cells PNAS, March 27, 2001; 98(7): 4178 - 4183. [Abstract] [Full Text] [PDF]

				I. A. Belyantseva, G. I. Frolenkov, J. B. Wade, F. Mammano, and B. Kachar Water Permeability of Cochlear Outer Hair Cells: Characterization and Relationship to Electromotility J. Neurosci., December 15, 2000; 20(24): 8996 - 9003. [Abstract] [Full Text] [PDF]

				D. Z. Z. He and P. Dallos Somatic stiffness of cochlear outer hair cells is voltage-dependent PNAS, July 6, 1999; 96(14): 8223 - 8228. [Abstract] [Full Text] [PDF]

				G. Frank, W. Hemmert, and A. W. Gummer Limiting dynamics of high-frequency electromechanical transduction of outer hair cells PNAS, April 13, 1999; 96(8): 4420 - 4425. [Abstract] [Full Text] [PDF]

				G. I. Frolenkov, M. Atzori, F. Kalinec, F. Mammano, and B. Kachar The Membrane-based Mechanism of Cell Motility in Cochlear Outer Hair Cells Mol. Biol. Cell, August 1, 1998; 9(8): 1961 - 1968. [Full Text]

				R. A. Jerry and A. Dutta Molecular Motor and Electrokinetic Contributions to Outer Hair Cell Electromotility J Neurophysiol, January 1, 1998; 79(1): 471 - 473. [Abstract] [Full Text] [PDF]

				J. S. Oghalai, A. A. Patel, T. Nakagawa, and W. E. Brownell Fluorescence-Imaged Microdeformation of the Outer Hair Cell Lateral Wall J. Neurosci., January 1, 1998; 18(1): 48 - 58. [Abstract] [Full Text] [PDF]

				D. Z. Z. He Relationship between the Development of Outer Hair Cell Electromotility and Efferent Innervation: A Study in Cultured Organ of Corti of Neonatal Gerbils J. Neurosci., May 15, 1997; 17(10): 3634 - 3643. [Abstract] [Full Text] [PDF]

				P. Dallos, D. Z. Z. He, X. Lin, I. Sziklai, S. Mehta, and B. N. Evans Acetylcholine, Outer Hair Cell Electromotility, and the Cochlear Amplifier J. Neurosci., March 15, 1997; 17(6): 2212 - 2226. [Abstract] [Full Text] [PDF]

				P Dallos and B. Evans High-frequency motility of outer hair cells and the cochlear amplifier Science, March 31, 1995; 267(5206): 2006 - 2009. [Abstract] [PDF]