Modeling auditory-nerve responses for high sound pressure levels in the normal and impaired auditory periphery.

This paper presents a computational model to simulate normal and impaired auditory-nerve (AN) fiber responses in cats. The model responses match physiological data over a wider dynamic range than previous auditory models. This is achieved by providing two modes of basilar membrane excitation to the inner hair cell (IHC) rather than one. The two modes are generated by two parallel filters, component 1 (C1) and component 2 (C2), and the outputs are subsequently transduced by two separate functions. The responses are then added and passed through the IHC low-pass filter followed by the IHC-AN synapse model and discharge generator. The C1 filter is a narrow-band, chirp filter with the gain and bandwidth controlled by a nonlinear feed-forward control path. This filter is responsible for low and moderate level responses. A linear, static, and broadly tuned C2 filter followed by a nonlinear, inverted and nonrectifying C2 transduction function is critical for producing transition region and high-level effects. Consistent with Kiang's two-factor cancellation hypothesis, the interaction between the two paths produces effects such as the C1/C2 transition and peak splitting in the period histogram. The model responses are consistent with a wide range of physiological data from both normal and impaired ears for stimuli presented at levels spanning the dynamic range of hearing.

[1]  M. Charles Liberman,et al.  Single-neuron labeling and chronic cochlear pathology. I. Threshold shift and characteristic-frequency shift , 1984, Hearing Research.

[2]  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.

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

[4]  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.

[5]  M. Liberman,et al.  Single-neuron labeling and chronic cochlear pathology. III. Stereocilia damage and alterations of threshold tuning curves , 1984, Hearing Research.

[6]  Raimond L. Winslow,et al.  A computational model for rate-level functions from cat auditory-nerve fibers , 1989, Hearing Research.

[7]  Bertrand Delgutte,et al.  Two-tone rate suppression in auditory-nerve fibers: Dependence on suppressor frequency and level , 1990, Hearing Research.

[8]  M. Ruggero,et al.  Chinchilla auditory-nerve responses to low-frequency tones. , 1983, The Journal of the Acoustical Society of America.

[9]  P Dallos,et al.  The level dependence of response phase: observations from cochlear hair cells. , 1998, The Journal of the Acoustical Society of America.

[10]  John J. Rosowski,et al.  Middle-ear transmission: Acoustic versus ossicular coupling in cat and human , 1992, Hearing Research.

[11]  John J Guinan,et al.  Time-frequency analysis of auditory-nerve-fiber and basilar-membrane click responses reveal glide irregularities and non-characteristic-frequency skirts. , 2004, The Journal of the Acoustical Society of America.

[12]  L. A. Westerman,et al.  A diffusion model of the transient response of the cochlear inner hair cell synapse. , 1988, The Journal of the Acoustical Society of America.

[13]  N. Y. S. Kiang,et al.  Discharge Rates of Single Auditory‐Nerve Fibers as Functions of Tone Level , 1969 .

[14]  Mario A. Ruggero,et al.  Basilar membrane responses to clicks , 1992 .

[15]  A. Palmer,et al.  Phase-locking in the cochlear nerve of the guinea-pig and its relation to the receptor potential of inner hair-cells , 1986, Hearing Research.

[16]  E D Young,et al.  Effects of acoustic trauma on the representation of the vowel "eh" in cat auditory nerve fibers. , 1997, The Journal of the Acoustical Society of America.

[17]  E. de Boer,et al.  On cochlear encoding: Potentialities and limitations of the reverse‐correlation technique , 1978 .

[18]  D. H. Johnson,et al.  The relationship between spike rate and synchrony in responses of auditory-nerve fibers to single tones. , 1980, The Journal of the Acoustical Society of America.

[19]  Effects of acoustic trauma on stereocilia structure and spiral ganglion cell tuning properties in the guinea pig cochlea , 1982, Hearing Research.

[20]  L. Carney,et al.  Frequency glides in the impulse responses of auditory-nerve fibers. , 1999 .

[21]  D Robertson,et al.  Tuning in the mammalian cochlea. , 1988, Physiological reviews.

[22]  Oded Ghitza,et al.  Temporal non-place information in the auditory-nerve firing patterns as a front-end for speech recognition in a noisy environment , 1988 .

[23]  P Kuyper,et al.  Triggered correlation. , 1968, IEEE transactions on bio-medical engineering.

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

[25]  Eric D Young,et al.  Effects of high sound levels on responses to the vowel /ε/ in cat auditory nerve , 1998, Hearing Research.

[26]  T J Goblick,et al.  Time-domain measurements of cochlear nonlinearities using combination click stimuli. , 1969, The Journal of the Acoustical Society of America.

[27]  E. de Boer,et al.  Validity of the Liouville-Green (or WKB) method for cochlear mechanics , 1982, Hearing Research.

[28]  Mario A. Ruggero,et al.  “Peak-Splitting”: Intensity Effects in Cochlear Afferent Responses to Low Frequency Tones , 1989 .

[29]  H. Weiher,et al.  Ultrastructural and physiological defects in the cochlea of the Mpv17 mouse strain A comparison between young and old adult animals , 2001, Hearing Research.

[30]  Eric D Young,et al.  Response growth with sound level in auditory-nerve fibers after noise-induced hearing loss. , 2004, Journal of neurophysiology.

[31]  Blake S Wilson,et al.  Two New Directions in Speech Processor Design for Cochlear Implants , 2005, Ear and hearing.

[32]  E. de Boer,et al.  On cochlear encoding: potentialities and limitations of the reverse-correlation technique. , 1978, The Journal of the Acoustical Society of America.

[33]  Ian C Bruce Physiological assessment of contrast-enhancing frequency shaping and multiband compression in hearing aids. , 2004, Physiological measurement.

[34]  Response to ‘‘Comment on ‘Two‐tone suppression of inner hair cell and basilar membrane responses in the guinea pig’ ’’ [J. Acoust. Soc. Am. 94, 3509–3510 (1993)] , 1993 .

[35]  M. Liberman The cochlear frequency map for the cat: labeling auditory-nerve fibers of known characteristic frequency. , 1982, The Journal of the Acoustical Society of America.

[36]  A. Nuttall,et al.  Two-tone suppression of inner hair cell and basilar membrane responses in the guinea pig. , 1993, The Journal of the Acoustical Society of America.

[37]  M. Liberman,et al.  Auditory-nerve response from cats raised in a low-noise chamber. , 1978, The Journal of the Acoustical Society of America.

[38]  Laurel H Carney,et al.  A phenomenological model for the responses of auditory-nerve fibers. II. Nonlinear tuning with a frequency glide. , 2003, The Journal of the Acoustical Society of America.

[39]  M. Cheatham,et al.  Two-tone suppression in inner hair cell responses , 1989, Hearing Research.

[40]  M. Ruggero,et al.  Wiener-kernel analysis of basilar-membrane responses to white noise , 1997 .

[41]  Edwin C. Moxon,et al.  Physiological Considerations in Artificial Stimulation of the Inner Ear , 1972, The Annals of otology, rhinology, and laryngology.

[42]  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.

[43]  A. Møller,et al.  Frequency selectivity of single auditory-nerve fibers in response to broadband noise stimuli. , 1977, The Journal of the Acoustical Society of America.

[44]  P M Sellick,et al.  Intracellular studies of hair cells in the mammalian cochlea. , 1978, The Journal of physiology.

[45]  C. Daniel Geisler,et al.  Temporal patterns of the responses of auditory-nerve fibers to low-frequency tones , 1996, Hearing Research.

[46]  E. Lopez-Poveda,et al.  A computational algorithm for computing nonlinear auditory frequency selectivity. , 2001, The Journal of the Acoustical Society of America.

[47]  C D Geisler,et al.  Transient response of the basilar membrane measured in squirrel monkeys using the Mössbauer effect. , 1976, The Journal of the Acoustical Society of America.

[48]  M. Liberman,et al.  Single-neuron labeling and chronic cochlear pathology. IV. Stereocilia damage and alterations in rate- and phase-level functions , 1984, Hearing Research.

[49]  David J. Anderson,et al.  Temporal Position of Discharges in Single Auditory Nerve Fibers within the Cycle of a Sine‐Wave Stimulus: Frequency and Intensity Effects , 1971 .

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

[51]  I. Whitfield Discharge Patterns of Single Fibers in the Cat's Auditory Nerve , 1966 .

[52]  W. S. Rhode,et al.  Study of mechanical motions in the basal region of the chinchilla cochlea. , 2000, The Journal of the Acoustical Society of America.

[53]  Julius L. Goldstein,et al.  Quantifying 2-factor phase relations in non-linear responses from low characteristic-frequency auditory-nerve fibers , 1995, Hearing Research.

[54]  William F. Sewell,et al.  The effects of furosemide on the endocochlear potential and auditory-nerve fiber tuning curves in cats , 1984, Hearing Research.

[55]  Mario A. Ruggero,et al.  Auditory-nerve responses to low-frequency tones: Intensity dependence , 1996 .

[56]  J Tchorz,et al.  A model of auditory perception as front end for automatic speech recognition. , 1999, The Journal of the Acoustical Society of America.

[57]  Philip X Joris,et al.  Cochlear Phase and Amplitude Retrieved from the Auditory Nerve at Arbitrary Frequencies , 2003, The Journal of Neuroscience.

[58]  E. F. Evans,et al.  The Dynamic Range Problem: Place and Time Coding at the Level of Cochlear Nerve and Nucleus , 1981 .

[59]  C. Shera,et al.  Frequency glides in click responses of the basilar membrane and auditory nerve: their scaling behavior and origin in traveling-wave dispersion. , 2001, The Journal of the Acoustical Society of America.

[60]  Julius L. Goldstein,et al.  Relations among compression, suppression, and combination tones in mechanical responses of the basilar membrane: data and MBPNL model , 1995, Hearing Research.

[61]  J J Zwislocki,et al.  Effects of hair cell lesions on responses of cochlear nerve fibers. I. Lesions, tuning curves, two-tone inhibition, and responses to trapezoidal-wave patterns. , 1980, Journal of neurophysiology.

[62]  Eric D. Young,et al.  Contrast enhancement improves the representation of /ɛ/-like vowels in the hearing-impaired auditory nerve , 1999 .

[63]  Ray Meddis,et al.  A nonlinear filter-bank model of the guinea-pig cochlear nerve: rate responses. , 2003, The Journal of the Acoustical Society of America.

[64]  James M. Kates,et al.  A time-domain digital cochlear model , 1991, IEEE Trans. Signal Process..

[65]  J. Guinan,et al.  Auditory-nerve-fiber responses to high-level clicks: interference patterns indicate that excitation is due to the combination of multiple drives. , 2000, The Journal of the Acoustical Society of America.

[66]  L. Carney,et al.  A model for the responses of low-frequency auditory-nerve fibers in cat. , 1993, The Journal of the Acoustical Society of America.

[67]  Julius L. Goldstein,et al.  Modeling rapid waveform compression on the basilar membrane as multiple-bandpass-nonlinearity filtering , 1990, Hearing Research.

[68]  William F. Sewell,et al.  Furosemide selectively reduces one component in rate-level functions from auditory-nerve fibers , 1984, Hearing Research.

[69]  James M. Kates,et al.  Two-tone suppression in a cochlear model , 1995, IEEE Trans. Speech Audio Process..

[70]  M. Sachs,et al.  An auditory-periphery model of the effects of acoustic trauma on auditory nerve responses. , 2003, The Journal of the Acoustical Society of America.

[71]  Matthew C. Holley,et al.  Outer Hair Cell Motility , 1996 .

[72]  Simon Haykin,et al.  A novel signal-processing strategy for hearing-aid design: neurocompensation , 2004, Signal Process..

[73]  M. Charles Liberman,et al.  Single unit clues to cochlear mechanisms , 1986, Hearing Research.

[74]  R Meddis,et al.  Regularity of cochlear nucleus stellate cells: a computational modeling study. , 1993, The Journal of the Acoustical Society of America.

[75]  David C Mountain,et al.  Multiple modes of inner hair cell stimulation , 1999, Hearing Research.

[76]  Guy J. Brown,et al.  Computational auditory scene analysis , 1994, Comput. Speech Lang..

[77]  R A Levine,et al.  Auditory-Nerve Activity in Cats Exposed to Ototoxic Drugs and High-Intensity Sounds , 1976, The Annals of otology, rhinology, and laryngology.

[78]  P Dallos,et al.  Response characteristics of mammalian cochlear hair cells , 1985, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[79]  William S. Rhode,et al.  AN INVESTIGATION OF POST-MORTEM COCHLEAR MECHANICS USING THE MÖSSBAUER EFFECT , 1973 .

[80]  C D Geisler,et al.  The phases of basilar-membrane vibrations. , 1982, The Journal of the Acoustical Society of America.

[81]  J. Guinan,et al.  Effects of crossed-olivocochlear-bundle stimulation on cat auditory nerve fiber responses to tones. , 1983, The Journal of the Acoustical Society of America.

[82]  L. Carney,et al.  A phenomenological model for the responses of auditory-nerve fibers: I. Nonlinear tuning with compression and suppression. , 2001, The Journal of the Acoustical Society of America.

[83]  Laurel H. Carney,et al.  Spatiotemporal encoding of sound level: Models for normal encoding and recruitment of loudness , 1994, Hearing Research.

[84]  E de Boer,et al.  The mechanical waveform of the basilar membrane. I. Frequency modulations ("glides") in impulse responses and cross-correlation functions. , 1997, The Journal of the Acoustical Society of America.

[85]  W. S. Rhode,et al.  Mechanical responses to two-tone distortion products in the apical and basal turns of the mammalian cochlea. , 1997, Journal of neurophysiology.

[86]  W. S. Rhode,et al.  Basilar membrane mechanics in the hook region of cat and guinea-pig cochleae: Sharp tuning and nonlinearity in the absence of baseline position shifts , 1992, Hearing Research.

[87]  N. Kiang,et al.  Curious oddments of auditory-nerve studies , 1990, Hearing Research.

[88]  Peter Dallos,et al.  Neurobiology of cochlear inner and outer hair cells: intracellular recordings , 1986, Hearing Research.

[89]  C Giguère,et al.  A computational model of the auditory periphery for speech and hearing research. I. Ascending path. , 1994, The Journal of the Acoustical Society of America.

[90]  L. Carney,et al.  Temporal coding of resonances by low-frequency auditory nerve fibers: single-fiber responses and a population model. , 1988, Journal of neurophysiology.

[91]  H. Versnel,et al.  A dual filter model describing single-fiber responses to clicks in the normal and noise-damaged cochlea. , 1994, The Journal of the Acoustical Society of America.

[92]  C. D. Geisler,et al.  A composite auditory model for processing speech sounds. , 1987, The Journal of the Acoustical Society of America.

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

[94]  A Robert,et al.  A composite model of the auditory periphery for simulating responses to complex sounds. , 1999, The Journal of the Acoustical Society of America.

[95]  John W. Matthews,et al.  Modeling Reverse Middle Ear Transmission of Acoustic Distortion Signals , 1983 .