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THE MECHANICS OF HEARING: A COMPARATIVE CASE STUDY IN BIO-MATHEMATICAL MODELLING

Published online by Cambridge University Press:  05 December 2011

A. R. CHAMPNEYS*
Affiliation:
Department of Engineering Mathematics, University of Bristol, Bristol, BS8 1TR, United Kingdom (email: a.r.champneys@bristol.ac.uk, martin-homer@bristol.ac.uk, r.szalai@bristol.ac.uk)
D. AVITABILE
Affiliation:
Department of Mathematics, University of Surrey, Guildford, GU2 7XH, United Kingdom (email: D.Avitabile@surrey.ac.uk)
M. HOMER
Affiliation:
Department of Engineering Mathematics, University of Bristol, Bristol, BS8 1TR, United Kingdom (email: a.r.champneys@bristol.ac.uk, martin-homer@bristol.ac.uk, r.szalai@bristol.ac.uk)
R. SZALAI
Affiliation:
Department of Engineering Mathematics, University of Bristol, Bristol, BS8 1TR, United Kingdom (email: a.r.champneys@bristol.ac.uk, martin-homer@bristol.ac.uk, r.szalai@bristol.ac.uk)
*
For correspondence; e-mail: a.r.champneys@bristol.ac.uk
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Abstract

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A synthesis is presented of two recent studies on modelling the nonlinear neuro-mechanical hearing processes in mosquitoes and in mammals. In each case, a hierarchy of models is considered in attempts to understand data that shows nonlinear amplification and compression of incoming sound signals. The insect’s hearing is tuned to the vicinity of a single input frequency. Nonlinear response occurs via an arrangement of many dual capacity neuro-mechanical units called scolopidia within the Johnston’s organ. It is shown how the observed data can be captured by a simple nonlinear oscillator model that is derived from homogenization of a more complex model involving a radial array of scolopidia. The physiology of the mammalian cochlea is much more complex, with hearing occurring via a travelling wave along a tapered, compartmentalized tube. Waves travel a frequency-dependent distance along the tube, at which point they are amplified and “heard”. Local models are reviewed for the pickup mechanism, within the outer hair cells of the organ of Corti. The current debate in the literature is elucidated, on the relative importance of two possible nonlinear mechanisms: active hair bundles and somatic motility. It is argued that the best experimental agreement can be found when the nonlinear terms include longitudinal coupling, the physiological basis of which is described. A discussion section summarizes the lessons learnt from both studies and attempts to shed light on the more general question of what constitutes a good mathematical model of a complex physiological process.

Type
Research Article
Copyright
Copyright © Australian Mathematical Society 2011

References

[1]Ashmore et al., J., “The remarkable cochlear amplifier”, Hear. Res. 266 (2010) 117; doi:10.1016/j.heares.2010.05.001.CrossRefGoogle Scholar
[2]Assad, J. A. and Corey, D. P., “An active motor model for adaptation by vertebrate hair cells”, J. Neurosci. 12 (1992) 32913309.CrossRefGoogle ScholarPubMed
[3]Avitabile, D., Homer, M., Champneys, A. R., Jackson, J. C. and Robert, D., “Mathematical modelling of the active hearing process in mosquitoes”, J. Roy. Soc. Interface 7 (2010) 105122; doi:10.1098/rsif.2009.0091.CrossRefGoogle ScholarPubMed
[4]Békésy, G., Experiments in hearing (McGraw-Hill, New York, 1960).Google Scholar
[5]de Boor, C. and Swartz, B., “Collocation at Gaussian points”, SIAM J. Numer. Anal. 10 (1973) 582606; doi:10.1137/0710052.CrossRefGoogle Scholar
[6]Brownell, W. E., Bader, C. R., Bertrand, D. and de Ribaupierre, Y., “Evoked mechanical responses of isolated cochlear outer hair cells”, Science 227 (1985) 194196; doi:10.1126/science.3966153.CrossRefGoogle ScholarPubMed
[7]Cooper, N. P. and Rhode, W. S., “Nonlinear mechanics at the apex of the guinea-pig cochlea”, Hearing Res. 82 (1995) 225243; doi:10.1016/0378-5955(94)00180-X.CrossRefGoogle ScholarPubMed
[8]Dallos, P., “Cochlear amplification, outer hair cells and prestin”, Current Opinion Neurobiol. 18 (2008) 370376; doi:10.1016/j.conb.2008.08.016.CrossRefGoogle ScholarPubMed
[9]Dallos, P., “Prestin-based outer hair cell motility is necessary for mammalian cochlear amplification”, Neuron 58 (2008) 333339; doi:10.1016/j.neuron.2008.02.028.CrossRefGoogle ScholarPubMed
[10]Doedel, E. J., Keller, H. B. and Kernévez, J. P., “Numerical analysis and control of bifurcation problems, part II: bifurcation in infinite dimensions”, Int. J. Bifur. Chaos Appl. Sci. Engrg. 1 (1991) 745772; doi:10.1142/S0218127491000555.CrossRefGoogle Scholar
[11]Eguíluz, V. M., Ospeck, M., Choe, Y., Hudspeth, A. J. and Magnasco, M. O., “Essential nonlinearities in hearing”, Phys. Rev. Lett. 84 (2000) 52325235; doi:10.1103/PhysRevLett.84.5232.CrossRefGoogle ScholarPubMed
[12]Elliott, S. J., Ku, E. M. and Lineton, B., “Time domain model of a nonlinear inhomogeneous cochlea’”, in: Concepts and challenges in the biophysics of hearing (eds Cooper, N. P. and Kemp, D. T.), (World Scientific, Singapore, 2009) 7481.CrossRefGoogle Scholar
[13]Frank, G., Hemmert, W. and Gummer, A. W., “Limiting dynamics of high-frequency electromechanical transduction of outer hair cells”, Proc. Natl. Acad. Sci. USA 96 (1999) 44204425; doi:10.1073/pnas.96.8.4420.CrossRefGoogle ScholarPubMed
[14]Geisler, C. D., “A realizable cochlear model using feedback from motile outer hair cells”, Hearing Res. 68 (1993) 253262; doi:10.1016/0378-5955(93)90129-O.CrossRefGoogle ScholarPubMed
[15]Ghaffari, R., Aranyosi, A. J. and Freeman, D. M., “Longitudinally propagating traveling waves of the mammalian tectorial membrane”, Proc. Natl. Acad. Sci. USA 104 (2007) 1651016515; doi:10.1073/pnas.0703665104.CrossRefGoogle ScholarPubMed
[16]Göpfert, M. C. and Robert, D., “Motion generation by Drosophila mechanosensory neurons”, Proc. Natl. Acad. Sci. USA 100 (2003) 55145519; doi:10.1073/pnas.0737564100.CrossRefGoogle ScholarPubMed
[17]Guckenheimer, J. and Holmes, P, Nonlinear oscillations, dynamical systems and bifurcations of vector fields, Volume 42 of Applied mathematical sciences (Springer, New York, 1986).Google Scholar
[18]Helmholtz, H., On the sensation of tone (Dover, New York, 1863).Google Scholar
[19]Hubbard, A., “A traveling-wave amplifier model of the cochlea”, Science 259 (1993) 6871; doi:10.1126/science.8418496.CrossRefGoogle ScholarPubMed
[20]Hudspeth, A. J., “Making an effort to listen: mechanical amplification in the ear”, Neuron 59 (2008) 530545; doi:10.1016/j.neuron.2008.07.012.CrossRefGoogle ScholarPubMed
[21]Hudspeth, A. J., Jülicher, F. and Martin, P., “A critique of the critical cochlea: Hopf – a bifurcation – is better than none”, J. Neurophysiology 104 (2010) 12191229; doi:10.1152/jn.00437.2010.CrossRefGoogle Scholar
[22]Jackson, J. C. and Robert, D., “Nonlinear auditory mechanism enhances female sounds for male mosquitoes”, Proc. Natl. Acad. Sci. USA 103 (2006) 1673416739; doi:10.1073/pnas.0606319103.CrossRefGoogle ScholarPubMed
[23]Jackson, J. C., Windmill, J. F. C., Pook, V. G. and Robert, D., “Synchrony through twice-frequency forcing for sensitive and selective auditory processing”, Proc. Natl. Acad. Sci. USA 106 (2009) 1017710182; doi:10.1073/pnas.0901727106.CrossRefGoogle ScholarPubMed
[24]Jülicher, F., Andor, D. and Duke, T., “Physical basis of two-tone interference in hearing”, Proc. Nat. Acad. Sci. USA 98 (2001) 90809085; doi:10.1073/pnas.151257898.CrossRefGoogle ScholarPubMed
[25]Karavitaki, K. D. and Mountain, D. C., “Evidence for outer hair cell driven oscillatory fluid flow in the tunnel of corti”, Biophysical J. 92 (2007) 32843293; doi:10.1529/biophysj.106.084087.CrossRefGoogle ScholarPubMed
[26]Kennedy, H. J., Crawford, A. C. and Fettiplace, R., “Force generation by mammalian hair bundles supports a role in cochlear amplification”, Nature 443 (2005) 880883; doi:10.1038/nature03367.CrossRefGoogle Scholar
[27]Kennedy, H. J., Evans, M. G., Crawford, A. C. and Fettiplace, R., “Fast adaptation of mechanoelectrical transducer channels in mammalian cochlear hair cells”, Nature Neuroscience 6 (2003) 832836; doi:10.1038/nn1089.CrossRefGoogle ScholarPubMed
[28]Lagarde, M. M. M., Drexl, M., Lukashkina, V. A., Lukashkin, A. N. and Russell, I. J., “Determining the identity of the cochlear amplifier: electrical stimulation of the tecta mouse cochlea”, in: Concepts and challenges in the biophysics of hearing (eds Cooper, N. P. and Kemp, D. T.), (World Scientific, Singapore, 2009) 106112.CrossRefGoogle Scholar
[29]Lesser, M. B. and Berkley, D. A., “Fluid mechanics of the cochlea. Part 1”, J. Fluid Mech. 51 (1972) 497512; doi:10.1017/S0022112072002320.CrossRefGoogle Scholar
[30]Lighthill, J., “Energy flow in the cochlea”, J. Fluid Mech. 106 (1981) 149213; doi:10.1017/S0022112081001560.CrossRefGoogle Scholar
[31]Meaud, J. and Grosh, K., “The effect of tectorial membrane and basilar membrane longitudinal coupling in cochlear mechanics”, J. Acoust. Soc. Am. 127 (2010) 14111421; doi:10.1121/1.3290995.CrossRefGoogle ScholarPubMed
[32]Ó Maoiléidigh, D. and Jülicher, F., “The interplay between active hair bundle motility and electromotility in the cochlea”, J. Acoust. Soc. Am. 128 (2010) 11751190; doi:10.1121/1.3463804.CrossRefGoogle ScholarPubMed
[33]Rhode, W. S., “Basilar membrane mechanics in the 6–9 kHz region of sensitive chinchilla cochleae”, J. Acoust. Soc. Am. 121 (2007) 27922804; doi:10.1121/1.2718397.CrossRefGoogle ScholarPubMed
[34]Ruggero, M. A., Rich, N. C., Recio, A., Narayan, S. S. and Robles, L., “Basilar-membrane responses to tones at the base of the chinchilla cochlea”, J. Acoust. Soc. Am. 101 (1997) 21512163; doi:10.1121/1.418265.CrossRefGoogle ScholarPubMed
[35]Steele, C. R. and Lim, K.-M., “Cochlear model with three-dimensional fluid, inner sulcus and feed-forward mechanism”, Audiol. Neurotol. 4 (1999) 197203; doi:10.1159/000013841.CrossRefGoogle ScholarPubMed
[36]Szalai, R., Champneys, A. R., Homer, M., Ó Maoiléidigh, D., Kennedy, H. J. and Cooper, N. P., “On the origins of the compressive cochlear nonlinearity”, J. Acoust. Soc. Am., to appear.Google Scholar
[37]Szalai, R., Epp, B., Champneys, A. R. and Homer, M., “On time-delayed and feed-forward transmission line models of the cochlea”, J. Mech. Mat. Struct. 6 (2011) 557568; doi:10.2140/jomms.2011.6.557.CrossRefGoogle Scholar
[38]Tinevez, J., Jülicher, F. and Martin, P., “Unifying the various incarnations of active hair-bundle motility by the vertebrate hair cell”, Biophysical J. 93 (2007) 40534067; doi:10.1529/biophysj.107.108498.CrossRefGoogle ScholarPubMed
[39]Zheng, J., Shen, W., He, D. Z. Z., Long, K. B., Madison, L. D. and Dallos, P., “Prestin is the motor protein of cochlear outer hair cells”, Nature 405 (2000) 149155; doi:10.1038/35012009.CrossRefGoogle ScholarPubMed
[40]Zweig, G., “Finding the impedance of the organ of corti”, J. Acoust. Soc. Am. 89 (1991) 12291254.CrossRefGoogle ScholarPubMed
[41]Zwislocki, J., “Theorie der schneckenmechanik: qualitative und quantitative analyse”, Acta Oto-Laryngologica 72 (1948) 176.Google Scholar