A Resonance Approach to Cochlear Mechanics

Background How does the cochlea analyse sound into its component frequencies? In the 1850s Helmholtz thought it occurred by resonance, whereas a century later Békésy's work indicated a travelling wave. The latter answer seemed to settle the question, but with the discovery in 1978 that the cochlea emits sound, the mechanics of the cochlea was back on the drawing board. Recent studies have raised questions about whether the travelling wave, as currently understood, is adequate to explain observations. Approach Applying basic resonance principles, this paper revisits the question. A graded bank of harmonic oscillators with cochlear-like frequencies and quality factors is simultaneously excited, and it is found that resonance gives rise to similar frequency responses, group delays, and travelling wave velocities as observed by experiment. The overall effect of the group delay gradient is to produce a decelerating wave of peak displacement moving from base to apex at characteristic travelling wave speeds. The extensive literature on chains of coupled oscillators is considered, and the occurrence of travelling waves, pseudowaves, phase plateaus, and forced resonance in such systems is noted. Conclusion and significance This alternative approach to cochlear mechanics shows that a travelling wave can simply arise as an apparently moving amplitude peak which passes along a bank of resonators without carrying energy. This highlights the possible role of the fast pressure wave and indicates how phase delays and group delays of a set of driven harmonic oscillators can generate an apparent travelling wave. It is possible to view the cochlea as a chain of globally forced coupled oscillators, and this model incorporates fundamental aspects of both the resonance and travelling wave theories.

[1]  Andrew J. Oxenham,et al.  Otoacoustic Estimation of Cochlear Tuning: Validation in the Chinchilla , 2010, Journal of the Association for Research in Otolaryngology.

[2]  Egbert de Boer,et al.  Cochlear models and minimum phase , 1997 .

[3]  Sir James Lighthill,et al.  Biomechanics of Hearing Sensitivity , 1991 .

[4]  R. Yamapi,et al.  Stability of the synchronization manifold in nearest neighbor nonidentical van der Pol-like oscillators , 2010, 1001.3240.

[5]  Y. Kuramoto,et al.  Phase transitions in active rotator systems , 1986 .

[6]  Daniel J. Lee,et al.  Physiology of the Auditory System , 2010 .

[7]  Interactions between Hair Cells Shape Spontaneous Otoacoustic Emissions in a Model of the Tokay Gecko's Cochlea , 2010, PloS one.

[8]  Georg v. Békésy Resonance in the Cochlea , 1969 .

[9]  J. A. Bell The cochlea as a graded bank of independent, simultaneously excited resonators: calculated properties of an apparent 'travelling wave' , 2010 .

[10]  Renato Nobili,et al.  Otoacoustic Emissions from Residual Oscillations of the Cochlear Basilar Membrane in a Human Ear Model , 2003, Journal of the Association for Research in Otolaryngology.

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

[12]  W S Rhode Cochlear mechanics. , 1984, Annual review of physiology.

[13]  Tianying Ren,et al.  Reverse propagation of sound in the gerbil cochlea , 2004, Nature Neuroscience.

[14]  Nigel P. Cooper,et al.  Concepts and Challenges in the Biophysics of Hearing , 2009 .

[15]  James Andrew Bell Are outer hair cells pressure sensors? Basis of a saw model of the cochlear amplifier , 2003 .

[16]  J. Eggermont,et al.  The effect of sound intensity on f1-sweep and f2-sweep distortion product otoacoustic emissions phase delay estimates in human adults. , 1997, The Journal of the Acoustical Society of America.

[17]  P. van Dijk,et al.  Are human spontaneous otoacoustic emissions generated by a chain of coupled nonlinear oscillators? , 2012, The Journal of the Acoustical Society of America.

[18]  Yoshiki Kuramoto,et al.  Chemical Oscillations, Waves, and Turbulence , 1984, Springer Series in Synergetics.

[19]  Hendrikus Duifhuis,et al.  Comprar Cochlear Mechanics. Introduction To A Time Domain Analysis Of The Nonlinear Cochlea | Hendrikus Duifhuis | 9781441961167 | Springer , 2012 .

[20]  M Lawrence,et al.  A NOTE ON RECENT DEVELOPMENTS IN AUDITORY THEORY. , 1954, Proceedings of the National Academy of Sciences of the United States of America.

[21]  Max A. Viergever,et al.  Mechanics of Hearing , 1983 .

[22]  Thomas Gold,et al.  Hearing. II. The Physical Basis of the Action of the Cochlea , 1948, Proceedings of the Royal Society of London. Series B - Biological Sciences.

[23]  M. Ruggero Systematic errors in indirect estimates of basilar membrane travel times. , 1980, The Journal of the Acoustical Society of America.

[24]  Christopher A Shera,et al.  Laser amplification with a twist: traveling-wave propagation and gain functions from throughout the cochlea. , 2007, The Journal of the Acoustical Society of America.

[25]  H. Duifhuis Comment on "An approximate transfer function for the dual-resonance nonlinear filter model of auditory frequency selectivity". , 2004, The Journal of the Acoustical Society of America.

[26]  Hidetsugu Sakaguchi,et al.  Cooperative Phenomena in Coupled Oscillator Systems under External Fields , 1988 .

[27]  David T. Kemp Otoacoustic emissions and evoked potentials , 2010 .

[28]  Renato Nobili,et al.  How Does the Inner Ear Generate Distortion Product Otoacoustic Emissions? , 2006, ORL.

[29]  A. Nuttall,et al.  Group delay of acoustic emissions in the ear. , 2006, Journal of neurophysiology.

[30]  Jan-Moritz P. Franosch,et al.  A two-dimensional cochlear fluid model based on conformal mapping. , 2010, The Journal of the Acoustical Society of America.

[31]  Alfred L. Nuttall,et al.  Cochlear mechanics, tuning, non-linearities , 2010 .

[32]  Michael Rosenblum,et al.  Synchronization and chaotization in interacting dynamical systems , 1995 .

[33]  M. Ruggero Responses to sound of the basilar membrane of the mammalian cochlea , 1992, Current Opinion in Neurobiology.

[34]  A. Winfree The geometry of biological time , 1991 .

[35]  P. Tass,et al.  Macroscopic entrainment of periodically forced oscillatory ensembles. , 2011, Progress in biophysics and molecular biology.

[36]  V S Anishchenko,et al.  Phase-frequency synchronization in a chain of periodic oscillators in the presence of noise and harmonic forcings. , 2001, Physical review. E, Statistical, nonlinear, and soft matter physics.

[37]  H. Helmholtz,et al.  On the Sensations of Tone as a Physiological Basis for the Theory of Music , 2005 .

[39]  G. Ermentrout,et al.  Frequency Plateaus in a Chain of Weakly Coupled Oscillators, I. , 1984 .

[40]  Stimulus frequency otoacoustic emissions in the Northern leopard frog, Rana pipiens pipiens: Implications for inner ear mechanics , 2006, Hearing Research.

[41]  C. Bergevin,et al.  Coherent reflection without traveling waves: on the origin of long-latency otoacoustic emissions in lizards. , 2010, The Journal of the Acoustical Society of America.

[42]  Peter Saunders The geometry of biological time (2nd edn), by Arthur T. Winfree. Pp. 777. £46.50. 2001 ISBN 0 387 98992 7 (Springer). , 2002, The Mathematical Gazette.

[43]  M. Ruggero,et al.  Wiener kernels of chinchilla auditory-nerve fibers: verification using responses to tones, clicks, and noise and comparison with basilar-membrane vibrations. , 2005, Journal of neurophysiology.

[44]  M. Ruggero SUR LES DELAIS COCHLEAIRES ET LES ONDES PROPAGEES: COMMENTAIRE SUR 'EXPERIMENTAL LOOK AT COCHLEAR MECHANICS' (APPROCHE EXPERIMENTALE DE LA MECANIQUE COCHLEAIRE) , 1994 .

[45]  Stacy R. Guild Symposium: Neural mechanism of hearing: I.— Anatomy and physiology (a)— Comments on the physiology of hearing and the anatomy of the inner ear , 1937 .

[46]  J J Zwislocki,et al.  Five decades of research on cochlear mechanics. , 1980, The Journal of the Acoustical Society of America.

[47]  Andrew Bell,et al.  The cochlear amplifier as a standing wave: "squirting" waves between rows of outer hair cells? , 2004, The Journal of the Acoustical Society of America.

[48]  Christopher A Shera,et al.  Mammalian spontaneous otoacoustic emissions are amplitude-stabilized cochlear standing waves. , 2003, The Journal of the Acoustical Society of America.

[49]  D. Kemp Stimulated acoustic emissions from within the human auditory system. , 1978, The Journal of the Acoustical Society of America.

[50]  Richard F. Lyon,et al.  An analog electronic cochlea , 1988, IEEE Trans. Acoust. Speech Signal Process..

[51]  Jozef J. Zwislocki,et al.  Auditory Sound Transmission: An Autobiographical Perspective , 2002 .

[52]  Geoffrey A. Manley,et al.  Active processes and otoacoustic emissions in hearing , 2007 .

[53]  R.N. Bracewell,et al.  Signal analysis , 1978, Proceedings of the IEEE.

[54]  S. Strogatz,et al.  Stability diagram for the forced Kuramoto model. , 2008, Chaos.

[55]  Arthur T. Winfree,et al.  Wavelike Activity in Biological and Chemical Media , 1974 .

[56]  E. Hiebert Sensations of Tone as the Physiological Basis for the Theory of Music , 2014 .

[58]  Enrique A Lopez-Poveda,et al.  An approximate transfer function for the dual-resonance nonlinear filter model of auditory frequency selectivity. , 2003, The Journal of the Acoustical Society of America.

[59]  Mario A Ruggero,et al.  Unexceptional sharpness of frequency tuning in the human cochlea. , 2005, Proceedings of the National Academy of Sciences of the United States of America.

[60]  W. S. Rhode,et al.  Two-Tone Suppression in Apical Cochlear Mechanics , 2012 .

[61]  Andrew Bell,et al.  Detection without deflection? A hypothesis for direct sensing of sound pressure by hair cells , 2007, Journal of Biosciences.

[62]  E. Lepage The mammalian cochlear map is optimally warped. , 2003, The Journal of the Acoustical Society of America.

[63]  Experimental Look at Cochlear Mechanics: Approche expérimental de la mécanique cochléaire , 1992 .

[64]  Jordi García-Ojalvo,et al.  Synchronization of coupled biological oscillators under spatially heterogeneous environmental forcing. , 2008, Journal of theoretical biology.

[65]  J. Guinan,et al.  Evoked otoacoustic emissions arise by two fundamentally different mechanisms: a taxonomy for mammalian OAEs. , 1999, The Journal of the Acoustical Society of America.

[66]  Arnold Tubis,et al.  Do Forward- and Backward-Traveling Waves Occur Within the Cochlea? Countering the Critique of Nobili et al. , 2004, Journal of the Association for Research in Otolaryngology.

[67]  G. Donaldson,et al.  Derived band auditory brain-stem response estimates of traveling wave velocity in humans. I: Normal-hearing subjects. , 1993, The Journal of the Acoustical Society of America.

[68]  Anthony W. Gummer,et al.  Biophysics of the Cochlea From Molecules to Models , 2003 .

[69]  James Lighthill,et al.  Energy flow in the cochlea , 1981, Journal of Fluid Mechanics.

[70]  E. Lepage Comment on "The cochlear amplifier as a standing wave: 'squirting' waves between rows of outer hair cells?" J. Acoust.Soc. Am. 116, 1016-1024. , 2006, The Journal of the Acoustical Society of America.

[71]  L. Robles,et al.  Basilar membrane mechanics at the base of the chinchilla cochlea. I. Input-output functions, tuning curves, and response phases. , 1986, The Journal of the Acoustical Society of America.

[72]  M. Ruggero,et al.  Frequency tuning of basilar membrane and auditory nerve fibers in the same cochleae. , 1998, Science.

[73]  Alberto Recio-Spinoso,et al.  Delays of stimulus-frequency otoacoustic emissions and cochlear vibrations contradict the theory of coherent reflection filtering. , 2005, The Journal of the Acoustical Society of America.

[74]  R. J. Field,et al.  The transition from phase waves to trigger waves in a model of the Zhabotinskii reaction , 1979 .

[75]  James D. Murray Mathematical Biology: I. An Introduction , 2007 .

[76]  T. Gold,et al.  Hearing. I. The Cochlea as a Frequency Analyzer , 1948, Proceedings of the Royal Society of London. Series B - Biological Sciences.

[77]  J. Lighthill Advantages from Describing Cochlear Mechanics in Terms of Energy Flow , 1983 .

[78]  M. Ruggero,et al.  Similarity of Traveling-Wave Delays in the Hearing Organs of Humans and Other Tetrapods , 2007, Journal for the Association for Research in Otolaryngology.

[79]  Cellular vibration and motility in the organ of Corti. , 1989, Acta oto-laryngologica. Supplementum.

[80]  Michael A. Arbib,et al.  The handbook of brain theory and neural networks , 1995, A Bradford book.

[81]  Jürgen Kurths,et al.  Synchronization: Phase locking and frequency entrainment , 2001 .

[82]  D. Mcqueen ‘Spatial oscillations’ in the Zhabotinskii reaction , 1974, Nature.

[83]  Michel F. Randrianandrasana,et al.  A preliminary study into emergent behaviours in a lattice of interacting nonlinear resonators and oscillators , 2011 .

[84]  Shigeru Shinomoto,et al.  Local and Grobal Self-Entrainments in Oscillator Lattices , 1987 .

[85]  David T. Kemp,et al.  Otoacoustic Emissions: Concepts and Origins , 2008 .

[86]  Richard F Lyon,et al.  Cascades of two-pole-two-zero asymmetric resonators are good models of peripheral auditory function. , 2011, The Journal of the Acoustical Society of America.

[87]  L. Robles,et al.  Mechanics of the mammalian cochlea. , 2001, Physiological reviews.

[88]  N. Kopell Chains of coupled oscillators , 1998 .

[89]  M. Ruggero,et al.  Cochlear delays and traveling waves: comments on 'Experimental look at cochlear mechanics'. , 1994, Audiology : official organ of the International Society of Audiology.

[90]  S. Rossignol,et al.  Neural Control of Rhythmic Movements in Vertebrates , 1988 .

[91]  M A Viergever,et al.  Cochlear power flux as an indicator of mechanical activity. , 1987, The Journal of the Acoustical Society of America.

[92]  E. D. Boer On the Nature of Cochlear Resonance , 1989 .

[93]  J. Kurthsb,et al.  Synchronization of two non-scalar-coupled limit-cycle oscillators , 2003 .

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

[95]  Y. Kuramoto Collective behavior of coupled oscillators , 1998 .

[96]  A. Oxenham,et al.  Frequency selectivity and masking , 2010 .

[97]  J. Murray,et al.  On travelling wave solutions in a model for the Belousov-Zhabotinskii reaction. , 1976, Journal of theoretical biology.

[98]  Christopher Bergevin,et al.  MoH 101: Basic Concepts in the Mechanics of Hearing , 2011 .

[99]  Christopher A Shera,et al.  Revised estimates of human cochlear tuning from otoacoustic and behavioral measurements , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[100]  Leonid I. Manevitch,et al.  The Mechanics Of Nonlinear Systems With Internal Resonances , 2005 .

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

[102]  James Andrew Bell,et al.  The Underwater Piano: A Resonance Theory of Cochlear Mechanics , 2005 .

[103]  U. F. Franck Kinetic feedback processes in physico-chemical oscillatory systems , 1974 .

[104]  Andrew Bell,et al.  Tuning the cochlea: wave-mediated positive feedback between cells , 2007, Biological Cybernetics.

[105]  P. Coleman,et al.  Experiments in hearing , 1961 .

[106]  J. Flanagan Models for Approximating Basilar Membrane Displacement , 1960 .

[107]  T. Gold Historical Background to the Proposal, 40 Years Ago, of an Active Model for Cochlear Frequency Analysis , 1989 .

[108]  G. B. Ermentrout,et al.  Phaselocking in a reaction-diffusion system with a linear frequency gradient , 1986 .

[109]  G. K. Yates,et al.  Basilar membrane measurements and the travelling wave , 1986, Hearing Research.

[110]  Peter Dallos,et al.  Overview: Cochlear Neurobiology , 1996 .

[111]  Andrew Bell,et al.  Hearing: Travelling Wave or Resonance? , 2004, PLoS biology.

[112]  E. Izhikevich,et al.  Weakly connected neural networks , 1997 .

[113]  Julius O. Smith,et al.  Introduction to Digital Filters: with Audio Applications , 2007 .

[114]  R. Batchelor,et al.  Chemical waves , 1984, Nature.

[115]  Reverse wave propagation in the cochlea , 2008, Proceedings of the National Academy of Sciences.

[116]  Alan R. Champneys,et al.  What Fire is in Mine Ears: Progress in Auditory Biomechanics , 2011 .

[117]  B L Lonsbury-Martin,et al.  Visualization of the onset of distortion-product otoacoustic emissions, and measurement of their latency. , 1996, The Journal of the Acoustical Society of America.

[118]  J. Claerbout Earth Soundings Analysis: Processing Versus Inversion , 1992 .

[119]  Dawn Konrad-Martin,et al.  Transient-evoked stimulus-frequency and distortion-product otoacoustic emissions in normal and impaired ears. , 2005, The Journal of the Acoustical Society of America.

[120]  Charles F. Babbs,et al.  Quantitative Reappraisal of the Helmholtz-Guyton Resonance Theory of Frequency Tuning in the Cochlea , 2011, Journal of biophysics.

[121]  J. Eggermont,et al.  Estimating cochlear filter response properties from distortion product otoacoustic emission (DPOAE) phase delay measurements in normal hearing human adults , 1998, Hearing Research.

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

[123]  Ben Lineton,et al.  Fluid coupling in a discrete model of cochlear mechanics. , 2011, The Journal of the Acoustical Society of America.

[124]  Tracing Distortion Product (DP) Waves in a Cochlear Model. , 2011, AIP conference proceedings.

[125]  E. Lopez-Poveda,et al.  A human nonlinear cochlear filterbank. , 2001, The Journal of the Acoustical Society of America.

[126]  R. Spigler,et al.  The Kuramoto model: A simple paradigm for synchronization phenomena , 2005 .

[127]  Enrique A Lopez-Poveda,et al.  Spectral processing by the peripheral auditory system: facts and models. , 2005, International review of neurobiology.

[128]  Thomas Duke,et al.  Frequency clustering in spontaneous otoacoustic emissions from a lizard's ear. , 2008, Biophysical journal.

[129]  G. Zweig,et al.  The origin of periodicity in the spectrum of evoked otoacoustic emissions. , 1995, The Journal of the Acoustical Society of America.

[130]  Comparison of Otoacoustic Emissions Within Gecko Subfamilies: Morphological Implications for Auditory Function in Lizards , 2011, Journal of the Association for Research in Otolaryngology.

[131]  D. D. Greenwood Critical Bandwidth and the Frequency Coordinates of the Basilar Membrane , 1961 .

[132]  P. Bressloff,et al.  Traveling Waves in a Chain of Pulse-Coupled Oscillators , 1998 .

[133]  Jürgen Kurths,et al.  Synchronization - A Universal Concept in Nonlinear Sciences , 2001, Cambridge Nonlinear Science Series.

[134]  Hiroaki Daido Order Function Theory of Macroscopic Phase-Locking in Globally and Weakly Coupled Limit-Cycle Oscillators , 1997 .

[135]  Andrew Bell The pipe and the pinwheel: Is pressure an effective stimulus for the 9 + 0 primary cilium? , 2008, Cell biology international.

[136]  E. de Boer,et al.  On ringing limits of the auditory periphery , 2004, Biological Cybernetics.

[137]  Frank Jülicher,et al.  Active traveling wave in the cochlea. , 2003, Physical review letters.

[138]  N. Fletcher,et al.  Acoustic systems in biology , 1992 .

[139]  A Dancer Experimental look at cochlear mechanics. , 1992, Audiology : official organ of the International Society of Audiology.

[140]  Dieter Thoenes ``Spatial Oscillations'' in the Zhabotinskii Reaction , 1973 .

[141]  István Z Kiss,et al.  Resonance clustering in globally coupled electrochemical oscillators with external forcing. , 2008, Physical review. E, Statistical, nonlinear, and soft matter physics.