Auditory-Nerve Rate Responses are Inconsistent with Common Hypotheses for the Neural Correlates of Loudness Recruitment

AbstractA number of perceptual phenomena related to normal and impaired level coding can be accounted for by the degree of compression in the basilar-membrane (BM) magnitude response. However, the narrow dynamic ranges of auditory-nerve (AN) fibers complicate these arguments. Because the AN serves as an information bottleneck, an improved understanding of the neural coding of level may clarify some of the limitations of current hearing aids. Here three hypotheses for the neural correlate of loudness recruitment were evaluated based on AN responses from normal-hearing cats and from cats with a noise-induced hearing loss (NIHL). Auditory-nerve fiber rate-level functions for tones were analyzed to test the following hypotheses: Loudness recruitment results from steeper AN rate functions after impairment. This hypothesis was not supported; AN rate functions were not steeper than normal following NIHL, despite steeper estimated BM responses based on the AN data.Loudness is based on the total AN discharge count, and recruitment results from an abnormally rapid spread of excitation after impairment. Whereas abnormal spread of excitation can be observed, steeper growth of total AN rate is not seen over the range of sound levels where recruitment is observed in human listeners.Loudness of a narrowband stimulus is based on AN responses in a narrow BF region, and recruitment results from compression of the AN-fiber threshold distribution after impairment. This hypothesis was not supported because there was no evidence that impaired AN threshold distributions were compressed and the growth of AN activity summed across BFs near the stimulus frequency was shallower than normal.Overall, these results suggest that loudness recruitment cannot be accounted for based on summed AN rate responses and may depend on neural mechanisms involved in the central representation of intensity.

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

[2]  B C Moore,et al.  Inter-relationship between different psychoacoustic measures assumed to be related to the cochlear active mechanism. , 1999, The Journal of the Acoustical Society of America.

[3]  E. Zwicker,et al.  A MODEL OF LOUDNESS SUMMATION. , 1965, Psychological review.

[4]  B. Moore,et al.  Enhanced frequency discrimination near the hearing loss cut-off: a consequence of central auditory plasticity induced by cochlear damage? , 2003, Brain : a journal of neurology.

[5]  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.

[6]  J. C. Stevens,et al.  Sensation and Measurement , 1974, Springer Netherlands.

[7]  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.

[8]  R A Levine,et al.  Auditory-nerve activity in cats with normal and abnormal cochleas. In: Sensorineural hearing loss. , 1970, Ciba Foundation symposium.

[9]  A. Oxenham,et al.  A behavioral measure of basilar-membrane nonlinearity in listeners with normal and impaired hearing. , 1997, The Journal of the Acoustical Society of America.

[10]  D A Nelson,et al.  Intensity discrimination in normal-hearing and hearing-impaired listeners. , 1994, The Journal of the Acoustical Society of America.

[11]  R V Harrison,et al.  Rate-versus-intensity functions and related AP responses in normal and pathological guinea pig and human cochleas. , 1981, The Journal of the Acoustical Society of America.

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

[13]  Brian C J Moore.  Testing the concept of softness imperception: loudness near threshold for hearing-impaired ears. , 2004, The Journal of the Acoustical Society of America.

[14]  R P Hellman.  Dependence of loudness growth on skirts of excitation patterns. , 1978, The Journal of the Acoustical Society of America.

[15]  R. Snyder,et al.  Chronic intracochlear electrical stimulation in the neonatally deafened cat. I: Expansion of central representation , 1990, Hearing Research.

[16]  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.

[17]  R F Hess,et al.  Effects of flanking noise bands on the rate of growth of loudness of tones in normal and recruiting ears. , 1985, The Journal of the Acoustical Society of America.

[18]  S. S. Stevens,et al.  Critical Band Width in Loudness Summation , 1957 .

[19]  J. O. Pickles,et al.  Auditory-nerve correlates of loudness summation with stimulus bandwidth, in normal and pathological cochleae , 1983, Hearing Research.

[20]  J. Saunders,et al.  Effects of priming for audiogenic seizure on auditory evoked responses in the cochlear nucleus and inferior colliculus of BALB-c mice. , 1972, Experimental neurology.

[21]  D A Nelson,et al.  A new procedure for measuring peripheral compression in normal-hearing and hearing-impaired listeners. , 2001, The Journal of the Acoustical Society of America.

[22]  M. P. Friedman,et al.  HANDBOOK OF PERCEPTION , 1977 .

[23]  R. P. Hamernik,et al.  Response patterns of auditory nerve fibers during temporary threshold shift , 1983, Hearing Research.

[24]  M. Liberman,et al.  Predicting Vulnerability to Acoustic Injury with a Noninvasive Assay of Olivocochlear Reflex Strength , 2000, The Journal of Neuroscience.

[25]  R. A. Schmiedt,et al.  Effects of hair cell lesions on responses of cochlear nerve fibers. II. Single- and two-tone intensity functions in relation to tuning curves. , 1980, Journal of neurophysiology.

[26]  D. Caspary,et al.  Glycine immunoreactivity and receptor binding in the cochlear nucleus of C57BL/6J and CBA/CaJ mice: Effects of cochlear impairment and aging , 1997, The Journal of comparative neurology.

[27]  S. Sterbing,et al.  Electrophysiological characteristics of inferior colliculus neurons in mutant mice with hereditary absence of cochlear outer hair cells , 2002, Hearing Research.

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

[29]  B. Moore,et al.  A revised model of loudness perception applied to cochlear hearing loss , 2004, Hearing Research.

[30]  Julius L. Goldstein,et al.  Is the Power Law Simply Related to the Driven Spike Response Rate from the Whole Auditory Nerve , 1974 .

[31]  J. Kaas,et al.  Neuroplasticity of the adult primate auditory cortex following cochlear hearing loss. , 1993, The American journal of otology.

[32]  Vit Drga,et al.  Inferred basilar-membrane response functions for listeners with mild to moderate sensorineural hearing loss. , 2004, The Journal of the Acoustical Society of America.

[33]  B. Moore,et al.  Psychoacoustic consequences of compression in the peripheral auditory system , 1998 .

[34]  R. A. Schmiedt,et al.  Effects of Furosemide Applied Chronically to the Round Window: A Model of Metabolic Presbyacusis , 2002, The Journal of Neuroscience.

[35]  J. Pickles.  An Introduction to the Physiology of Hearing , 1982 .

[36]  A R Møller,et al.  Evidence of neuronal plasticity within the inferior colliculus after noise exposure: a study of evoked potentials in the rat. , 1996, Electroencephalography and clinical neurophysiology.

[37]  E F Evans,et al.  The sharpening of cochlear frequency selectivity in the normal and abnormal cochlea. , 1975, Audiology : official organ of the International Society of Audiology.

[38]  Catherine G. O’Hanlon,et al.  Forward Masking Additivity and Auditory Compression at Low and High Frequencies , 2003, Journal of the Association for Research in Otolaryngology.

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

[40]  Dan H Sanes,et al.  The effect of bilateral deafness on excitatory and inhibitory synaptic strength in the inferior colliculus , 2002, The European journal of neuroscience.

[41]  B C Moore,et al.  Further evaluation of a model of loudness perception applied to cochlear hearing loss. , 1999, The Journal of the Acoustical Society of America.

[42]  B C Moore,et al.  Characterization and Simulation of Impaired Hearing: Implications for Hearing Aid Design , 1991, Ear and hearing.

[43]  R. Altschuler,et al.  Deafness-induced plasticity in the mature central auditory system , 1995, Neuroreport.

[44]  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.

[45]  R. Schlauch,et al.  Basilar membrane nonlinearity and loudness. , 1998, The Journal of the Acoustical Society of America.

[46]  R J Salvi,et al.  Plasticity of response properties of inferior colliculus neurons following acute cochlear damage. , 1996, Journal of neurophysiology.

[47]  M. Charles Liberman,et al.  Single-neuron labeling and chronic cochlear pathology. II. Stereocilia damage and alterations of spontaneous discharge rates , 1984, Hearing Research.

[48]  B C Moore,et al.  Psychoacoustic consequences of compression in the peripheral auditory system. , 1998, Psychological review.

[49]  E M Relkin,et al.  Is loudness simply proportional to the auditory nerve spike count? , 1997, The Journal of the Acoustical Society of America.

[50]  Harold F. Schuknecht,et al.  Pathology of the Ear , 1974 .

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

[52]  J. Popelář,et al.  Enhancement of the auditory cortex evoked responses in awake guinea pigs after noise exposure , 1994, Hearing Research.

[53]  F. Miskolczy-Fodor,et al.  Relation between Loudness and Duration of Tonal Pulses. III. Response in Cases of Abnormal Loudness Function , 1960 .

[54]  B. Walmsley,et al.  Synaptic transmission in the auditory brainstem of normal and congenitally deaf mice , 2002, The Journal of physiology.

[55]  Michael G. Heinz,et al.  Normal and impaired level encoding: Effects of noise-induced hearing loss on auditory-nerve responses , 2005 .

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

[57]  D. Irvine,et al.  Effect of unilateral partial cochlear lesions in adult cats on the representation of lesioned and unlesioned cochleas in primary auditory cortex , 1993, The Journal of comparative neurology.

[58]  G. Wilkinson.  The Theory of Hearing , 1925, Nature.

[59]  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 .

[60]  Susan G. Emmerson,et al.  Pathology of the Ear (2nd ed.) , 1994 .

[61]  J. E. Rose,et al.  Temporal position of discharges in single auditory nerve fibers within the cycle of a sine-wave stimulus: frequency and intensity effects. , 1971, The Journal of the Acoustical Society of America.

[62]  Laurel H. Carney,et al.  Quantifying the Information in Auditory-Nerve Responses for Level Discrimination , 2003, Journal of the Association for Research in Otolaryngology.

[63]  R. Salvi,et al.  Enhanced evoked response amplitudes in the inferior colliculus of the chinchilla following acoustic trauma , 1990, Hearing Research.

[64]  Ian M. Winter,et al.  Basilar membrane nonlinearity determines auditory nerve rate-intensity functions and cochlear dynamic range , 1990, Hearing Research.

[65]  Mary Florentine,et al.  Growth of Loudness in Listeners with Cochlear Hearing Losses: Recruitment Reconsidered , 2002, Journal of the Association for Research in Otolaryngology.

[66]  B. Moore.  Perceptual Consequences of Cochlear Damage , 1995 .

[67]  J. Pickles,et al.  Psychophysical frequency resolution in the cat as determined by simultaneous masking and its relation to auditory-nerve resolution. , 1979, The Journal of the Acoustical Society of America.

[68]  K. Steel,et al.  Preservation of central auditory function in thedeafness mouse , 1982, Brain Research.

[69]  E. Keithley,et al.  Frequency map of the spiral ganglion in the cat. , 1987, The Journal of the Acoustical Society of America.

[70]  F G Zeng,et al.  Binaural Loudness Matches in Unilaterally Impaired Listeners , 1991, The Quarterly journal of experimental psychology. A, Human experimental psychology.

[71]  J S Reilly,et al.  Sensorineural hearing loss. , 1989, The Pediatric clinics of North America.

[72]  J A Stillman,et al.  Intensity just-noticeable differences at equal-loudness levels in normal and pathological ears. , 1993, The Journal of the Acoustical Society of America.

[73]  M. Sachs,et al.  Rate versus level functions for auditory-nerve fibers in cats: tone-burst stimuli. , 1974, The Journal of the Acoustical Society of America.

[74]  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.

[75]  Stephen McAdams,et al.  Auditory signal processing : physiology, psychoacoustics, and models , 2005 .

[76]  Anders Fridberger,et al.  Alterations of basilar membrane response phase and velocity after acoustic overstimulation , 2002, Hearing Research.

[77]  M. Ruggero,et al.  Furosemide alters organ of corti mechanics: evidence for feedback of outer hair cells upon the basilar membrane , 1991, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[78]  J. Popelář,et al.  Effect of noise on auditory evoked responses in awake guina pigs , 1987, Hearing Research.

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

[80]  M G Heinz,et al.  Rate and timing cues associated with the cochlear amplifier: level discrimination based on monaural cross-frequency coincidence detection. , 2001, The Journal of the Acoustical Society of America.