Deformations of the isolated mouse tectorial membrane produced by oscillatory forces

Mechanical properties of the isolated tectorial membrane (TM) of the mouse were measured by applying oscillatory shear forces to the TM with a magnetic bead (radius approximately 10 mcm). Sinusoidal forces at 10 Hz with amplitudes from 5 to 33 nN were applied tangentially to the surfaces of 11 TMs. The ratio of force to bead displacement ranged from 0.04 to 0.98 N/m (median: 0.18 N/m, interquartile range: 0.11-0.30 N/m, n=90). Increasing frequency from 10 to 100 Hz decreased the magnitude of the displacement of the magnetic bead by 6-7.3 dB/decade. The phase of the displacement lagged that of the stimulus current by approximately 27-44 degrees across frequencies. Displacement of the adjacent tissue decreased as the distance from the magnetic bead increased. Space constants were of the order of tens of micrometers. Forces with equal amplitude and frequency were applied radially and longitudinally. Longitudinal displacements in response to longitudinal forces were 1-10 times as large as radial displacements in response to radial forces in 85% of 560 paired measurements. These results suggest that the following mechanical properties of the TM are important. (1) Viscoelasticity: The frequency dependence of TM displacement lies between that of a purely viscous and a purely elastic material, suggesting that both are important. (2) Mechanical coupling: Space constants indicate that hair bundles could interact mechanically with adjacent hair bundles via the TM. (3) Anisotropy: The mechanical impedance is greater in the radial direction than it is in the longitudinal direction. This mechanical anisotropy correlates with anatomical anisotropies, such as the radially oriented fibrillar structure of the TM.

[1]  H. Davis,et al.  LIX A Mechano-Electrical Theory of Cochlear Action , 1958, Transactions of the American Otological Society.

[2]  Peter Dallos,et al.  Cochlear Inner and Outer Hair Cells: Functional Differences , 1972, Science.

[3]  D. M. Freeman,et al.  Statistics of subpixel registration algorithms based on spatiotemporal gradients or block matching , 1998 .

[4]  R. Tran-Son-Tay,et al.  Magnetically driven, acoustically tracked, translating‐ball rheometer for small, opaque samples , 1988 .

[5]  M. Litt,et al.  Rheology of biological systems , 1973 .

[6]  G. Békésy,et al.  Experiments in Hearing , 1963 .

[7]  Thomas F. Weiss,et al.  On the Role of Fluid Inertia and Viscosity in Stereociliary Tuft Motion: Analysis of Isolated Bodies of Regular Geometry , 1986 .

[8]  C. Daniel Geisler,et al.  A model of the effect of outer hair cell motility on cochlear vibrations , 1986, Hearing Research.

[9]  M. Tortonese,et al.  Cantilevers and tips for atomic force microscopy , 1997, IEEE Engineering in Medicine and Biology Magazine.

[10]  Aminoglycoside Antibiotics and Lectins Cause Irreversible Increases in the Stiffness of Cochlear Hair-Cell Stereocilia , 1989 .

[11]  A Ratcliffe,et al.  Determination of collagen-proteoglycan interactions in vitro. , 1996, Journal of biomechanics.

[12]  K. Jacobson,et al.  Local measurements of viscoelastic parameters of adherent cell surfaces by magnetic bead microrheometry. , 1998, Biophysical journal.

[13]  B. M. Johnstone,et al.  Measurement of basilar membrane motion in the guinea pig using the Mössbauer technique. , 1982, The Journal of the Acoustical Society of America.

[14]  W C Hayes,et al.  Flow-independent viscoelastic properties of articular cartilage matrix. , 1978, Journal of biomechanics.

[15]  P. Santi,et al.  Crystalline arrays of proteoglycan and collagen in the tectorial membrane. , 1996, Matrix biology : journal of the International Society for Matrix Biology.

[16]  I. Thalmann,et al.  Composition and supramolecular organization of the tectorial membrane , 1987, The Laryngoscope.

[17]  P. Macklem,et al.  Rheological properties of microliter quantities of normal mucus. , 1977, Journal of applied physiology: respiratory, environmental and exercise physiology.

[18]  A. Flock,et al.  Stiffness of sensory-cell hair bundles in the isolated guinea pig cochlea , 1984, Hearing Research.

[19]  D. Ingber,et al.  Mechanotransduction across the cell surface and through the cytoskeleton , 1993 .

[20]  K. Zaner,et al.  Viscoelasticity of F-actin measured with magnetic microparticles , 1989, The Journal of cell biology.

[21]  E. D. Boer,et al.  Mechanics of the Cochlea: Modeling Efforts , 1996 .

[22]  S. Neely,et al.  A model for active elements in cochlear biomechanics. , 1986, The Journal of the Acoustical Society of America.

[23]  D. M. Freeman,et al.  Equilibrium behavior of an isotropic polyelectrolyte gel model of the tectorial membrane: effect of pH 1 Preliminary versions of this work were presented earlier (Freeman et al., 1996b; Weiss and Freeman, 1996b). 1 , 1997, Hearing Research.

[24]  K. Steel Donnan equilibrium in the tectorial membrane , 1983, Hearing Research.

[25]  Stephen T. Neely,et al.  An active cochlear model showing sharp tuning and high sensitivity , 1983, Hearing Research.

[26]  Marco Tortonese,et al.  Characterization of application-specific probes for SPMs , 1997, Photonics West.

[27]  E. J. Kletsky,et al.  Micromechanics in the theory of cochlear mechanics , 1980, Hearing Research.

[28]  B. M. Johnstone,et al.  Origin of summating potential. , 1966, The Journal of the Acoustical Society of America.

[29]  C D Geisler,et al.  Model of the displacement between opposing points on the tectorial membrane and reticular lamina. , 1967, The Journal of the Acoustical Society of America.

[30]  D. Lim Fine morphology of the tectorial membrane. Its relationship to the organ of Corti. , 1972, Archives of otolaryngology.

[31]  A. Hudspeth,et al.  Controlled bending of high-resistance glass microelectrodes. , 1978, The American journal of physiology.

[32]  M. Billone,et al.  Transmission of radial shear forces to cochlear hair cells. , 1973, The Journal of the Acoustical Society of America.

[33]  G. Richardson,et al.  The ultrastructural organization and properties of the mouse tectorial membrane matrix , 1988, Hearing Research.

[34]  V. Hascall,et al.  Uronic acid-containing glycosaminoglycans and keratan sulfate are present in the tectorial membrane of the inner ear: functional implications. , 1993, Archives of biochemistry and biophysics.

[35]  D. T. Kemp,et al.  Cochlear Mechanisms: Structure, Function, and Models , 1989, NATO ASI Series.

[36]  J J Zwislocki,et al.  Tectorial membrane: a possible effect on frequency analysis in the cochlea. , 1979, Science.

[37]  F. Mammano,et al.  Biophysics of the cochlea: linear approximation. , 1993, The Journal of the Acoustical Society of America.

[38]  W. S. Rhode Observations of the vibration of the basilar membrane in squirrel monkeys using the Mössbauer technique. , 1971, The Journal of the Acoustical Society of America.

[39]  D. M. Freeman,et al.  The osmotic response of the isolated, unfixed mouse tectorial membrane to isosmotic solutions: effect of Na+, K+, and Ca2+ concentration , 1995, Hearing Research.

[40]  I. Thalmann,et al.  Collagen of accessory structures of organ of Corti. , 1993, Connective tissue research.

[41]  Robert Patuzzi,et al.  Cochlear Micromechanics and Macromechanics , 1996 .

[42]  D. Lim,et al.  Functional structure of the organ of Corti: a review , 1986, Hearing Research.

[43]  G E Kempson,et al.  The tensile properties of the cartilage of human femoral condyles related to the content of collagen and glycosaminoglycans. , 1973, Biochimica et biophysica acta.

[44]  D. Lim,et al.  Cochlear anatomy related to cochlear micromechanics. A review. , 1980, The Journal of the Acoustical Society of America.

[45]  Jozef J. Zwislocki,et al.  Tectorial membrane II: Stiffness measurements in vivo , 1989, Hearing Research.

[46]  D. M. Freeman,et al.  Using a light microscope to measure motions with nanometer accuracy , 1998 .

[47]  Sharp mechanical tuning in a cochlear model without negative damping. , 1988, The Journal of the Acoustical Society of America.

[48]  E. Sackmann,et al.  Local measurements of viscoelastic moduli of entangled actin networks using an oscillating magnetic bead micro-rheometer. , 1994, Biophysical journal.

[49]  W. Seifriz An Elastic Value of Protoplasm, with Further Observations on the Viscosity of Protoplasm , 1924 .

[50]  William S. Rhode,et al.  Nonlinear mechanics at the apex of the guinea-pig cochlea , 1995, Hearing Research.

[51]  J. Allen,et al.  Cochlear micromechanics--a physical model of transduction. , 1980, The Journal of the Acoustical Society of America.

[52]  L. Robles,et al.  Basilar-membrane responses to tones at the base of the chinchilla cochlea. , 1997, The Journal of the Acoustical Society of America.