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.
REFERENCES
1.
Anderson
, D. J.
, Rose
, J. E.
, Hind
, J. E.
, and Brugge
, J. F.
(1971
). “Temporal position of discharges in single auditory nerve fibers within the cycle of a sine-wave stimulus: Frequency and intensity effects
,” J. Acoust. Soc. Am.
49
, 1131
–1139
.2.
Bondy
, J.
, Becker
, S.
, Bruce
, I.
, Trainor
, L.
, and Haykin
, S.
(2004
). “A novel signal-processing strategy for hearing-aid design: Neurocompensation
,” Signal Process.
84
, 1239
–1253
.3.
Brown
, G. J.
, and Cooke
, M.
(1994
). “Computational auditory scene analysis
,” Comput. Speech Lang.
8
, 297
–336
.4.
Bruce
, I. C.
(2004
). “Physiological assessment of contrast-enhancing frequency shaping and multi-band compression in hearing aids
,” Physiol. Meas
25
, 945
–956
.5.
Bruce
, I. C.
, Sachs
, M. B.
, and Young
, E. D.
(2003
). “An auditory-periphery model of the effects of acoustic trauma on auditory nerve responses
,” J. Acoust. Soc. Am.
113
, 369
–388
.6.
Cai
, Y.
(1995
). “Temporal responses of the auditory-nerve fibers to single-tone and two-tone stimuli: Experimental and modeling studies
,” Ph.D. thesis, University of Wisconsin-Madison
.7.
Cai
, Y.
, and Geisler
, C. D.
(1996
). “Temporal patterns of the responses of auditory-nerve fibers to low-frequency tones
,” Hear. Res.
96
, 83
–93
.8.
Carney
, L. H.
(1993
). “A model for the responses of low-frequency auditory-nerve fibers in cat
,” J. Acoust. Soc. Am.
93
, 401
–417
.9.
Carney
, L. H.
(1994
). “Spatiotemporal encoding of sound level: Models for normal encoding and recruitment of loudness
,” Hear. Res.
76
, 31
–44
.10.
Carney
, L. H.
, McDuffy
, M. J.
, and Shekhter
, I.
(1999
). “Frequency glides in the impulse responses of auditory-nerve fibers
,” J. Neurophysiol.
105
, 2384
–2391
.11.
Carney
, L. H.
, and Yin
, T. C. T.
(1988
). “Temporal coding of resonances by low-frequency auditory nerve fibers: Single-fiber responses and a population model
,” J. Neurophysiol.
60
, 1653
–1677
.12.
Cheatham
, M. A.
, and Dallos
, P.
(1989
). “Two-tone suppression in inner hair responses
,” Hear. Res.
40
, 187
–196
.13.
Cheatham
, M. A.
, and Dallos
, P.
(1998
). “The level dependence of response phase: Observations from cochlear hair cells
,” J. Acoust. Soc. Am.
104
, 356
–369
.14.
Cooper
, N. P.
, and Rhode
, W. S.
(1992
). “Basilar membrane mechanics in the hook region of cat and guinea-pig cochlae: Sharp tuning and nonlinarity in the absence of baseline position shifts
,” Hear. Res.
63
, 163
–190
.15.
Cooper
, N. P.
, and Rhode
, W. S.
(1997
). “Mechanical responses to two-tone distortion products in the apical and basal turns of the mammalian cochlea
,” J. Neurophysiol.
78
, 261
–270
.16.
Dallos
, P.
(1985
). “Response characteristics of mammalian cochlear hair cells
,” J. Neurosci.
5
, 1591
–1608
.17.
Dallos
, P.
(1986
). “Neurobiology of cochlear inner and outer hair cells: Intracellular recordings
,” Hear. Res.
22
, 185
–198
.18.
de Boer
, E.
, and de Jongh
, H. R.
(1978
). “On cochlear encoding: Potentialities and limitations of the reverse correlation technique
,” J. Acoust. Soc. Am.
63
, 115
–135
.19.
de Boer
, E.
, and Kuyper
, P.
(1968
). “Triggered correlation
,” IEEE Trans. Biomed. Eng.
15
, 169
–179
.20.
de Boer
, E.
, and Nuttall
, A. N.
(1997
). “The mechanical waveform of the basilar membrane. I. Frequency modulations (glides) in impulse responses and cross-correlation functions
,” J. Acoust. Soc. Am.
101
, 3583
–3592
.21.
de Boer
, E.
, and Viergever
, M. A.
(1982
). “Validity of the Liouville-Green (or WKB) method for cochlear mechanics
,” Hear. Res.
8
, 131
–155
.22.
Delgutte
, B.
(1990
). “Two-tone rate suppression in auditory-nerve fibers: Dependence on suppressor frequency and level
,” Hear. Res.
49
, 225
–246
.23.
Deng
, L.
, and Geisler
, C. D.
(1987
). “A composite auditory model for processing speech sounds
,” J. Acoust. Soc. Am.
82
, 2001
–2012
.24.
Evans
, E. F.
(1981
). “The dynamic range problem: Place and timing coding at the level of the cochlear nerve and nucleus
,” in Neuronal Mechanisms of Hearing
, edited by J.
Syka
and L.
Aitkin
(Plenum
, New York
), pp.69
–95
.25.
Geisler
, C. D.
, and Rhode
, W. S.
(1982
). “The phases of basilar-membrane vibrations
,” J. Acoust. Soc. Am.
71
, 1201
–1203
.26.
Ghitza
, O.
(1988
). “Temporal non-place information in the auditory-nerve firing patterns as a front-end for speech recognition in a noisy environment
,” J. Phonetics
16
, 109
–123
.27.
Gifford
, M. L.
, and Guinan
, J. J.
, Jr. (1983
). “Effects of crossed-olivocochlear bundle stimulation on cat auditory-nerve fiber response to tones
,” J. Acoust. Soc. Am.
74
, 115
–123
.28.
Giguère
, C.
, and Woodland
, P. C.
(1994
). “A computational model of the auditory periphery for speech and hearing research. I. Ascending path
,” J. Acoust. Soc. Am.
95
, 331
–342
.29.
Goblick
, T. J.
, and Pfeiffer
, R. R.
(1969
). “Time-domain measurements of cochlear nonlinearities using combination-click stimuli
,” J. Acoust. Soc. Am.
46
, 924
–938
.30.
Goldstein
, J. L.
(1990
). “Modeling rapid waveform compression on the basilar membrane as multiple-bandpass-nonlinearity filtering
,” Hear. Res.
49
, 39
–60
.31.
Goldstein
, J. L.
(1995
). “Relations among compression, suppression, and combination tones in mechanical responses of the basilar membrane: Data and MBPNL model
,” Hear. Res.
89
, 52
–68
.31.
Heinz
, M. G.
(private communication).32.
Heinz
, M. G.
, and Young
, E. D.
(2004
). “Response growth with sound level in auditory-nerve fibers after noise-induced hearing loss
,” J. Neurophysiol.
91
, 784
–795
.33.
Hewitt
, M. J.
, and Meddis
, R.
(1992
). “Regularity of cochlear neucleus stellate cells: A computational modeling study
,” J. Acoust. Soc. Am.
93
, 3390
–3399
.34.
Holley
, M. C.
(1996
). “Outer hair cell motility
,” in The Cochlea
, edited by P.
Dallos
, A. N.
Popper
, and R. R.
Fay
(Springer
, New York
), pp. 386
–434
.35.
Johnson
, D.
(1980
). “The relationship between spike rate and synchrony in responses to auditory-nerve fibers to single tones
,” J. Acoust. Soc. Am.
68
, 1115
–1122
.36.
Kates
, J. M.
(1991
). “A time-domain digital cochlear model
,” IEEE Trans. Signal Process.
39
, 2573
–2592
.37.
Kates
, J. M.
(1995
). “Two-tone suppression in a cochlear model
,” IEEE Trans. Speech Audio Process.
3
, 396
–406
.38.
Kiang
, N. Y.
, Liberman
, M. C.
, Sewell
, W. F.
, and Guinan
, J. J.
, Jr. (1986
). “Single unit clues to cochlear mechanisms
,” Hear. Res.
22
, 171
–182
.39.
Kiang
, N. Y.-S.
(1984
). “Peripheral neural processing of auditory information
,” in Handbook of Physiology, Section 1: The Nervous System
, edited by J. M.
Brookhart
and V. B.
Mountcastle
(American Physiological Society
, Bethesda, MD
), Vol. III
Pt. 2, pp. 639
–674
.40.
Kiang
, N. Y.-S.
(1990
). “Curious oddments of auditory-nerve studies
,” Hear. Res.
49
, 1
–16
.41.
Kiang
, N. Y.-S.
, Baer
, T.
, Marr
, E. M.
, and Demont
, D.
(1969
). “Discharge rates of single auditory-nerve fibers as a function of tone level
,” J. Acoust. Soc. Am.
46
, 106
.42.
Kiang
, N. Y.-S.
, Liberman
, M. C.
, and Levine
, R. A.
(1976
). “Auditory-nerve activity in cats exposed to ototoxic drugs and high-intensity sounds
,” Ann. Otol. Rhinol. Laryngol.
85
, 752
–768
.43.
Kiang
, N. Y.-S.
, and Moxon
, E. C.
(1972
). “Physiological considerations in artificial stimulation of the inner ear
,” Ann. Otol. Rhinol. Laryngol.
81
, 714
–731
.44.
Kiang
, N. Y.-S.
, Watanabe
, T.
, Thomas
, E. C.
, and Clark
, L. F.
(1965
). “Discharge patterns of single fibers in the cat’s auditory nerve
,” Res. Monogr. No. 35
(MIT
, Cambridge, MA).45.
Liberman
, M. C.
(1978
). “Auditory nerve response from cats raised in a low noise chamber
,” J. Acoust. Soc. Am.
63
, 442
–455
.46.
Liberman
, M. C.
(1982
). “The cochlear frequency map for the cat: Labeling auditory-nerve fibers of known characteristic frequency
,” J. Acoust. Soc. Am.
72
, 1441
–1449
.47.
Liberman
, M. C.
(1984
). “Single-neuron labeling and chronic cochlear pathology. I. Threshold shift and characteristic-frequency shift
,” Hear. Res.
16
, 33
–41
.48.
Liberman
, M. C.
, and Dodds
, L. W.
(1984
). “Single-neuron labeling and chronic cochlear pathology. III. Stereocilia damage and alterations of threshold tuning curves
,” Hear. Res.
16
, 55
–74
.49.
Liberman
, M. C.
, and Kiang
, N. Y.-S.
(1984
). “Single-neuron labeling and chronic cochlear pathology. IV. Stereocilia damage and alterations in rate- and phase-level functions
,” Hear. Res.
16
, 75
–90
.50.
Liberman
, M. C.
, and Mulroy
, M. J.
(1982
). “Acute and chronic effects of acoustic trauma: Cochlear pathology and auditory nerve pathophysiology
,” in New Perspectives on Noise-Induced Hearing Loss
, edited by R. P.
Hamernik
, D.
Henderson
, and R.
Salvi
(Raven
, New York
), pp. 105
–135
.51.
Lin
, T.
(1994
), “Quantitative modeling of nonlinear auditory-nerve responses as two-factor interactions
,” Ph.D. thesis, Sever Institute of Technology, Washington University
.52.
Lin
, T.
, and Goldstein
, J. L.
(1995
). “Quantifying 2-factor phase relations in non-linear responses from low characteristic-frequency auditory-nerve fibers
,” Hear. Res.
90
, 126
–138
.53.
Lin
, T.
, and Guinan
, J. J.
, Jr. (2000
). “Auditory-nerve-fiber responses to high-level clicks: Interference patterns indicate that excitation is due to the combination of multiple drives
,” J. Acoust. Soc. Am.
107
, 2615
–2630
.54.
Lin
, T.
, and Guinan
, J. J.
, Jr. (2004
). “Time-frequency analysis of auditory-nerve-fiber and basilar-membrane click responses reveal glide irregularities and non-characteristic-frequency skirts
,” J. Acoust. Soc. Am.
116
, 405
–416
.55.
Lopez-Poveda
, E. A.
(2005
). “Spectral processing by the peripheral auditory system: Facts and models
,” Int. Rev. Neurobiol.
70
, 7
–48
.56.
Matthews
, J. W.
(1983
). “Modeling reverse middle ear transmission of acoustic distortion signals
,” in Mechanics of Hearing: Proceedings of the IUTAM/ICA Symposium
, edited by E.
de Boer
and M. A.
Viergever
(Delft University Press
, Delft
), pp. 11
–18
.57.
Meddis
, R.
, O’Mard
, L. P.
, and Lopez-Poveda
, E. A.
(2001
). “A computational algorithm for computing nonlinear auditory frequency selectivity
,” J. Acoust. Soc. Am.
109
, 2852
–2861
.58.
Miller
, R. L.
, Calhoun
, B. M.
, and Young
, E. D.
(1999
). “Contrast enhancement improves the representation of /ε/-like vowels in the hearing-impaired auditory nerve
,” J. Acoust. Soc. Am.
106
, 2693
–2708
.59.
Miller
, R. L.
, Schilling
, J. R.
, Franck
, K. R.
, and Young
, E. D.
(1997
). “Effects of acoustic trauma on the representation of the vowel /ε/ in cat auditory nerve fibers
,” J. Acoust. Soc. Am.
101
, 3602
–3616
.60.
Møller
, A. R.
(1977
). “Frequency selectivity of single auditory-nerve fibers in response to broad-band noise stimuli
,” J. Acoust. Soc. Am.
62
, 135
–142
.61.
Mountain
, D. C.
, and Cody
, A. R.
(1999
). “Multiple modes of inner hair cell stimulation
,” Hear. Res.
132
, 1
–14
.62.
Narayan
, S. S.
, Temchin
, A. N.
, Recio
, A.
, and Ruggero
, M. A.
(1998
). “Frequency tuning of basilar membrane and auditory nerve fibers in the same cochleae
,” Science
282
, 1882
–1884
.63.
Nuttall
, A. L.
, and Dolan
, D. F.
(1993
). “Two-tone suppression of inner hair cell and basilar membrane responses in the guinea pig
,” J. Acoust. Soc. Am.
94
, 3511
–3514
.64.
Palmer
, A. R.
, and Russell
, I. J.
(1986
). “Phase-locking in the cochlear nerve of the guinea-pig and its relation to the receptor potential of inner hair-cells
,” Hear. Res.
24
, 1
–15
.65.
Patuzzi
, R. B.
(1996
). “Cochlear micromechanics and macromechanics
,” in The Cochlea
, edited by P.
Dallos
, A. N.
Popper
, and R. R.
Fay
(Springer
, New York
), pp. 186
–257
.66.
Patuzzi
, R. B.
, and Robertson
, D.
(1988
). “Tuning in the mammalian cochlea
,” Physiol. Rev.
68
, 1009
–1082
.67.
Peake
, W. T.
, Rosowski
, J. J.
, and Lynch
, T. J.
, III (1992
). “Middle-ear transmission: Acoustic versus ossicular coupling in cat and human
,” Hear. Res.
57
, 245
–268
.68.
Recio
, A.
, Narayan
, S. S.
, and Ruggero
, M. A.
(1997
). “Wiener-kernel analysis of basilar-membrane response to white noise
,” in Diversity in Auditory Mechanics
, edited by E. R.
Lewis
, G. R.
Long
, R. F.
Lyon
, P. M.
Narins
, C. R.
Steele
, and E.
Hecht-Poinar
(World Scientific
, Singapore
), pp. 325
–331
.69.
Recio
, A.
, Rich
, N. C.
, Narayan
, S. S.
, and Ruggero
, M. A.
(1998
). “Basilar-membrane responses to clicks at the base of the chichilla cochlea
,” J. Acoust. Soc. Am.
103
, 1972
–1989
.70.
Rhode
, W. S.
(1971
). “Observations of the vibration of the basilar membrane in squirrel monkeys using the mössbauer technique
,” J. Acoust. Soc. Am.
49
, 1218
–1231
.71.
Rhode
, W. S.
(1973
). “An investigation of postmortem cochlear mechanics using the Mössbauer effects
,” in Basic Mechanisms in Hearing
, edited by A. R.
Møller
(Academic
, New York
), pp. 49
–63
.72.
Rhode
, W. S.
, and Recio
, A.
(2000
). “Study of mechanical motions in the basal region of the chinchilla cochlea
,” J. Acoust. Soc. Am.
107
, 3317
–3332
.73.
Robert
, A.
, and Eriksson
, J. L.
(1999
). “A composite model of the auditory periphery for simulating responses to complex sounds
,” J. Acoust. Soc. Am.
106
, 1852
–1864
.74.
Robertson
, D.
(1982
). “Effects of acoustic trauma on stereocilia structure and spiral ganglion cell tuning properties in the guinea pig cochlea
,” Hear. Res.
7
, 55
–74
.75.
Robles
, L.
, Rhode
, W. S.
, and Geisler
, C. D.
(1976
). “Transient response of the basilar membrane measured in squirrel monkeys using the mössbauer effect
,” J. Acoust. Soc. Am.
59
, 926
–939
.76.
Robles
, L.
, and Ruggero
, M. A.
(2001
). “Mechanics of the mammalian cochlea
,” Physiol. Rev.
81
, 1305
–1352
.77.
Ruggero
, M. A.
, and Rich
, N. C.
(1983
). “Chinchilla auditory-nerve responses to low-frequency toens
,” J. Acoust. Soc. Am.
73
, 2096
–2108
.78.
Ruggero
, M. A.
, and Rich
, N. C.
(1989
). “Peak splitting: Intensity effects in cochlear afferent responses to low frequency tones
,” in Cochlear Mechanisms: Structure, Function and Models
, edited by J. P.
Wilson
and D. T.
Kemp
(Plenum
, New York
), pp. 259
–267
.79.
Ruggero
, M. A.
, Rich
, N. C.
, Recio
, A.
, Narayan
, S. S.
, and Robles
, L.
(1997
). “Basilar-membrane responses to tones at the base of the chinchilla cochlea
,” J. Acoust. Soc. Am.
101
, 2151
–2163
.80.
Ruggero
, M. A.
, Rich
, N. C.
, Shivapuja
, B. G.
, and Temchin
, A. N.
(1996
). “Auditory-nerve responses to low-frequency tones: Intensity dependence
,” Aud. Neurosci.
2
, 159
–185
.81.
Russell
, I. J.
, and Sellick
, P. M.
(1978
). “Intracellular studies of hair cells in the mammalian cochlea
,” J. Physiol. (London)
284
, 261
–290
.82.
Sachs
, M. B.
, Winslow
, R. L.
, and Sokolowski
, B. H. A.
(1989
). “A computational model for rate-level functions from cat auditory-nerve fibers
,” Hear. Res.
41
, 61
–70
.83.
Salvi
, R.
, Perry
, J.
, Hamernik
, R. P.
, and Henderson
, D.
(1982
). “Relationships between cochlear pathologies and auditory nerve and behavioral responses following acoustic trauma
,” in New Perspectives on Noise-Induced Hearing Loss
, edited by R. P.
Hamernik
, D.
Henderson
, and R.
Salvi
(Raven
, New York
), pp. 165
–188
.84.
Schmiedt
, R. A.
, Zwislocki
, J. J.
, and Hamernik
, R. P.
(1980
). “Effects of hair cell lesions on responses of cochlear nerve fibers. I. Lesions, tuning curves, two-tone inhibition, and responses to trapezoidal-wave patterns
,” J. Neurophysiol.
43
, 1367
–1389
.85.
Schoonhoven
, R.
, Keijzer
, J.
, Versnel
, H.
, and Prijs
, V. F.
(1994
). “A dual filter model describing single-fiber responses to clicks in the normal and noise-damaged cochlea
,” J. Acoust. Soc. Am.
95
, 2104
–2121
.86.
Sellick
, P. M.
, Patuzzi
, R.
, and Johnstone
, B. M.
(1982
). “Measurement of basilar membrane motion in the guinea pig using Mössbaeur technique
,” J. Acoust. Soc. Am.
72
, 131
–141
.87.
Sewell
, W. F.
(1984a
). “The effects of furosemide on the endocochlear potential and auditory-nerve fiber tuning curves
,” Hear. Res.
14
, 305
–314
.88.
Sewell
, W. F.
(1984b
). “Furosemide selectively reduces one component in rate-level functions from auditory-nerve fibers
,” Hear. Res.
15
, 69
–72
.89.
Shera
, C. A.
(2001
). “Frequency glides in click responses of the basilar membrane and auditory nerve: Their scaling behavior and origin in traveling-wave dispersion
,” J. Acoust. Soc. Am.
109
, 2023
–2034
.90.
Sumner
, C. J.
, O’Mard
, L. P.
, Lopez-Poveda
, E. A.
, and Meddis
, R.
(2003
). “A non-linear filter-bank model of the guinea-pig cochlear nerve: Rate responses
,” J. Acoust. Soc. Am.
113
, 3264
–3274
.91.
Tan
, Q.
, and Carney
, L. H.
(2003
). “A phenomenological model for the responses of the auditory-nerve fibers. II. Nonlinear tuning with a frequency glide
,” J. Acoust. Soc. Am.
114
, 2007
–2020
.92.
Tchorz
, J.
, and Kollmeier
, B.
(1999
). “A model of auditory perception as a front end for automatic speech recognition
,” J. Acoust. Soc. Am.
106
, 2040
–2050
.93.
van der Heijden
, M.
, and Joris
, P. X.
(2003
). “Cochlear phase and amplitude retrieved from the auditory-nerve at arbitrary frequencies
,” J. Neurosci.
23
, 9194
–9198
.94.
Westerman
, L. A.
, and Smith
, R. L.
(1988
). “A diffusion model of the transient response of the cochlear inner hair cell synapse
,” J. Acoust. Soc. Am.
83
, 2266
–2276
.95.
Wilson
, B. S.
, Schatzer
, R.
, Lopez-Poveda
, E. A.
, Sun
, X.
, Lawson
, D. T.
, and Wolford
, R. D.
(2005
). “Two new directions in speech processor design for cochlear implants
,” Ear Hear.
26
, 73S
–81S
.96.
Wong
, J. C.
(1998
). “Nonlinearities in the representation of the vowel /ε/ in cat auditory nerve at sound levels near SPL
,” Master’s thesis, Johns Hopkins University
.97.
Wong
, J. C.
, Miller
, R. L.
, Calhoun
, B. M.
, Sachs
, M. B.
, and Young
, E. D.
(1998
). “Effects of high sound levels on responses to the vowel /ε/ in cat auditory nerve
,” Hear. Res.
123
, 61
–77
.98.
Zhang
, X.
, Heinz
, M. G.
, Bruce
, I. C.
, and Carney
, L. H.
(2001
). “A phenomenological model for the responses of auditory-nerve fibers. I. Nonlinear tuning with compression and suppression
,” J. Acoust. Soc. Am.
109
, 648
–670
.© 2006 Acoustical Society of America.
2006
Acoustical Society of America
You do not currently have access to this content.
