Sensors, motors, and tuning in the cochlea: interacting cells could form a surface acoustic wave resonator

The outer hair cells of the cochlea occur in three distinct and geometrically precise rows and, unusually, display both sensing and motor properties. As well as sensing sound, outer hair cells (OHCs) undergo cycle-by-cycle length changes in response to stimulation. OHCs are central to the way in which the cochlea processes and amplifies sounds, but how they do so is presently unknown. In explanation, this paper proposes that outer hair cells act like a single-port surface acoustic wave (SAW) resonator in which the interdigital electrodes--the three distinctive rows--exhibit the required electromechanical and mechanoelectrical properties. Thus, frequency analysis in the cochlea might occur through sympathetic resonance of a bank of interacting cells whose microscopic separation largely determines the resonance frequency. In this way, the cochlea could be tuned from 20 Hz at the apex, where the spacing is largest, to 20 kHz at the base, where it is smallest. A suitable candidate for a wave that could mediate such a short-wavelength interaction--a 'squirting wave' known in ultrasonics--has recently been described. Such a SAW resonator could thereby underlie the 'cochlear amplifier'--the device whose action is evident to auditory science but whose identity has not yet been established.

[1]  Anthony W. Gummer,et al.  PULSATING FLUID MOTION AND DEFLECTION OF THE STEREOCILIA OF THE INNER HAIR CELLS DUE TO THE ELECTROMECHANICS OF THE OUTER HAIR CELLS , 2006 .

[2]  John J Guinan,et al.  Medial-olivocochlear-efferent inhibition of the first peak of auditory-nerve responses: evidence for a new motion within the cochlea. , 2005, The Journal of the Acoustical Society of America.

[3]  M. Ruggero,et al.  Basilar-membrane responses to clicks at the base of the chinchilla cochlea. , 1998, The Journal of the Acoustical Society of America.

[4]  A. Flock,et al.  Acoustic stimulation causes tonotopic alterations in the length of isolated outer hair cells from guinea pig hearing organ. , 1988, Proceedings of the National Academy of Sciences of the United States of America.

[5]  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.

[6]  H. Zenner,et al.  Active movements of the cuticular plate induce sensory hair motion in mammalian outer hair cells , 1988, Hearing Research.

[7]  Peter B. Nagy,et al.  On the low-frequency oscillation of a fluid layer between two elastic plates , 1997 .

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

[9]  Hendrikus Duifhuis,et al.  Biophysics of Hair Cell Sensory Systems , 1993 .

[10]  D. Bell,et al.  Surface-acoustic-wave resonators , 1976, Proceedings of the IEEE.

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

[12]  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.

[13]  Martin S. Robinette,et al.  Otoacoustic Emissions: Clinical Applications , 1997 .

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

[15]  N. P. Cooper RADIAL VARIATION IN THE VIBRATIONS OF THE COCHLEAR PARTITION , 2000 .

[16]  K. Yanagisawa,et al.  Potentials of outer hair cells and their membrane properties in cationic environments , 1980, Hearing Research.

[17]  Michael M. Paparella Ultrastructural Atlas of the Inner Ear , 1985 .

[18]  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.

[19]  P Dallos,et al.  Stereocilia displacement induced somatic motility of cochlear outer hair cells. , 1993, Proceedings of the National Academy of Sciences of the United States of America.

[20]  I. Russell,et al.  Tuned phasic and tonic motile responses of isolated outer hair cells to direct mechanical stimulation of the cell body , 1994, Hearing Research.

[21]  Thomas G Bifano,et al.  A hydromechanical biomimetic cochlea: experiments and models. , 2006, The Journal of the Acoustical Society of America.

[22]  W Hemmert,et al.  Limiting dynamics of high-frequency electromechanical transduction of outer hair cells. , 1999, Proceedings of the National Academy of Sciences of the United States of America.

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

[24]  GEORGE WILKINSON The Theory of Hearing , 1924, Nature.

[25]  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.

[26]  Barbara Canlon,et al.  Mechanically induced length changes of isolated outer hair cells are metabolically dependent , 1991, Hearing Research.

[27]  Werner Hemmert,et al.  Electromotility of outer hair cells from the cochlea of the echolocating bat, Carollia perspicillata , 1994, Journal of Comparative Physiology A.

[28]  Colin Campbell,et al.  Surface Acoustic Wave Devices for Mobile and Wireless Communications , 1998 .

[29]  The radial pattern of basilar membrane motion evoked by electric stimulation of the cochlea , 1999, Hearing Research.

[30]  I. Friedmann,et al.  Ultrastructural atlas of the inner ear , 1984 .

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

[32]  Norma B. Slepecky,et al.  Structure of the Mammalian Cochlea , 1996 .

[33]  Craig C. Bader,et al.  Evoked mechanical responses of isolated cochlear outer hair cells. , 1985, Science.

[34]  Barbara Canlon,et al.  Sound-induced motility of isolated cochlear outer hair cells is frequency-specific , 1989, Nature.