Spatiotemporal encoding of sound level: Models for normal encoding and recruitment of loudness

This study explores the hypothesis that sound level is encoded in the spatiotemporal response patterns of auditory nerve (AN) fibers. The temporal properties of AN fiber responses depend upon sound level due to nonlinearities in the auditory periphery. In particular, the compressive nonlinearity of the inner ear introduces systematic changes in the timing of the responses of AN fibers as a function of level. Changes in single fiber responses that depend upon both sound level and characteristic frequency (CF) result in systematic changes in the spatiotemporal response patterns across populations of AN fibers. This study investigates the changes in the spatiotemporal response patterns as a function of level using a computational model for responses of low-frequency AN fibers. A mechanism that could extract information encoded in this form is coincidence detection across AN fibers of different CFs. This study shows that this mechanism could play a role in encoding of sound level for simple and complex stimuli. The model demonstrates that this encoding scheme would be influenced by auditory pathology that affects the peripheral compressive nonlinearity in a way that is consistent with the phenomenon of recruitment of loudness, which often accompanies sensorineural hearing loss.

[1]  K. Osen The Intrinsic Organization of the Cochlear Nuclei in the Cat , 1969 .

[2]  Neal F. Viemeister,et al.  Intensity coding and the dynamic range problem , 1988, Hearing Research.

[3]  Robert L. Smith,et al.  Operating range and maximum response of single auditory nerve fibers , 1980, Brain Research.

[4]  L H Carney,et al.  Effects of interaural time delays of noise stimuli on low-frequency cells in the cat's inferior colliculus. III. Evidence for cross-correlation. , 1987, Journal of neurophysiology.

[5]  Raimond L Winslow,et al.  Single-tone intensity discrimination based on auditory-nerve rate responses in backgrounds of quiet, noise, and with stimulation of the crossed olivocochlear bundle , 1988, Hearing Research.

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

[7]  L. Carney Modelling the sensitivity of cells in the anteroventral cochlear nucleus to spatiotemporal discharge patterns. , 1992, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[8]  Raimond L. Winslow,et al.  Some Aspects of Rate Coding in the Auditory Nerve , 1986 .

[9]  R. Hellman Effect of Spread of Excitation on the Loudness Function at 250 Hz , 1974 .

[10]  M B Sachs,et al.  Dynamic range of neural rate responses in the ventral cochlear nucleus of awake cats. , 1992, Journal of neurophysiology.

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

[12]  Robert D Frisina,et al.  Encoding of amplitude modulation in the gerbil cochlear nucleus: II. Possible neural mechanisms , 1990, Hearing Research.

[13]  J. Boudreau,et al.  Binaural interaction in the cat superior olive S segment. , 1967, Journal of neurophysiology.

[14]  M. Charles Liberman,et al.  Chronic ultrastructural changes in acoustic trauma: Serial-section reconstruction of stereocilia and cuticular plates , 1987, Hearing Research.

[15]  Brian C. J. Moore,et al.  Formulae describing frequency selectivity as a function of frequency and level, and their use in calculating excitation patterns , 1987, Hearing Research.

[16]  W. Dreschler,et al.  The Effect of Hearing Impairment on Auditory Filter Shapes in Simultaneous and Forward Masking , 1986 .

[17]  W. S. Rhode,et al.  Structural and functional properties distinguish two types of multipolar cells in the ventral cochlear nucleus , 1989, The Journal of comparative neurology.

[18]  Robert L. Smith,et al.  Response modulation of auditory-nerve fibers by am stimuli: effects of average intensity , 1980, Hearing Research.

[19]  P. Stypulkowski,et al.  Temporal response patterns of single auditory nerve fibers elicited by periodic electrical stimuli , 1987, Hearing Research.

[20]  J W Horst Frequency discrimination of complex signals, frequency selectivity, and speech perception in hearing-impaired subjects. , 1987, The Journal of the Acoustical Society of America.

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

[22]  M. Sachs,et al.  Representation of steady-state vowels in the temporal aspects of the discharge patterns of populations of auditory-nerve fibers. , 1979, The Journal of the Acoustical Society of America.

[23]  G F Pick,et al.  Level dependence of psychophysical frequency resolution and auditory filter shape. , 1980, The Journal of the Acoustical Society of America.

[24]  L. Robles,et al.  Two-tone suppression in the basilar membrane of the cochlea: mechanical basis of auditory-nerve rate suppression. , 1992, Journal of neurophysiology.

[25]  J. Guinan,et al.  Signal processing in brainstem auditory neurons which receive giant endings (calyces of Held) in the medial nucleus of the trapezoid body of the cat , 1990, Hearing Research.

[26]  S. Shamma Speech processing in the auditory system. II: Lateral inhibition and the central processing of speech evoked activity in the auditory nerve. , 1985, The Journal of the Acoustical Society of America.

[27]  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.

[28]  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.

[29]  Bertrand Delgutte,et al.  Peripheral Auditory Processing of Speech Information: Implications from a Physiological Study of Intensity Discrimination , 1987 .

[30]  C. Tsuchitani Functional organization of lateral cell groups of cat superior olivary complex. , 1977, Journal of neurophysiology.

[31]  R. Tyler Cochlear Implants: Audiological Foundations , 1992 .

[32]  J D Hood Loudness balance procedures for the measurement of recruitment. , 1977, Audiology : official organ of the International Society of Audiology.

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

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

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

[36]  R. R. Pfeiffer Anteroventral Cochlear Nucleus:Wave Forms of Extracellularly Recorded Spike Potentials , 1966, Science.

[37]  M. Liberman,et al.  Acute ultrastructural changes in acoustic trauma: Serial-section reconstruction of stereocilia and cuticular plates , 1987, Hearing Research.

[38]  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.

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

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

[41]  Bertrand Delgutte,et al.  Phase-locking of auditory-nerve discharges to sinusoidal electric stimulation of the cochlea , 1992, Hearing Research.

[42]  M. Liberman Central projections of auditory‐nerve fibers of differing spontaneous rate. I. Anteroventral cochlear nucleus , 1991, The Journal of comparative neurology.

[43]  E. Evans,et al.  Intensity coding in the auditory periphery of the cat: Responses of cochlear nerve and cochlear nucleus neurons to signals in the presence of bandstop masking noise , 1982, Hearing Research.

[44]  Raphael Lorente De No,et al.  The Primary Acoustic Nuclei , 1981 .

[45]  J. W. Horst,et al.  Coding of spectral fine structure in the auditory nerve. II: Level-dependent nonlinear responses. , 1990, The Journal of the Acoustical Society of America.

[46]  P. Manis,et al.  Outward currents in isolated ventral cochlear nucleus neurons , 1991, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[47]  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.

[48]  E. Evans Place and time coding of frequency in the peripheral auditory system: some physiological pros and cons. , 1978, Audiology : official organ of the International Society of Audiology.

[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]  M. Sachs,et al.  Classification of unit types in the anteroventral cochlear nucleus: PST histograms and regularity analysis. , 1989, Journal of neurophysiology.

[51]  C. Carr,et al.  Central projections of auditory nerve fibers in the barn owl , 1991, The Journal of comparative neurology.

[52]  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.

[53]  Terrance Raymond Bourk,et al.  Electrical responses of neural units in the anteroventral cochlear nucleus of the cat , 1976 .

[54]  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.

[55]  Ian M. Winter,et al.  Diversity of characteristic frequency rate-intensity functions in guinea pig auditory nerve fibres , 1990, Hearing Research.

[56]  L H Carney,et al.  Enhancement of neural synchronization in the anteroventral cochlear nucleus. I. Responses to tones at the characteristic frequency. , 1994, Journal of neurophysiology.

[57]  B C Moore,et al.  Auditory filter shapes at low center frequencies in young and elderly hearing-impaired subjects. , 1992, The Journal of the Acoustical Society of America.

[58]  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.

[59]  C M Rankovic,et al.  Potential benefits of adaptive frequency-gain characteristics for speech reception in noise. , 1992, The Journal of the Acoustical Society of America.

[60]  Philip H Smith,et al.  Projections of physiologically characterized globular bushy cell axons from the cochlear nucleus of the cat , 1991, The Journal of comparative neurology.

[61]  Alexander Joseph Book reviewDischarge patterns of single fibers in the cat's auditory nerve: Nelson Yuan-Sheng Kiang, with the assistance of Takeshi Watanabe, Eleanor C. Thomas and Louise F. Clark: Research Monograph no. 35. Cambridge, Mass., The M.I.T. Press, 1965 , 1967 .

[62]  A R Palmer,et al.  Intensity coding in low-frequency auditory-nerve fibers of the guinea pig. , 1991, The Journal of the Acoustical Society of America.

[63]  So,et al.  An excitation‐pattern model for intensity discrimination , 1981 .

[64]  D. Oertel Synaptic responses and electrical properties of cells in brain slices of the mouse anteroventral cochlear nucleus , 1983, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[65]  R. Hellman Dependence of loudness growth on skirts of excitation patterns , 1976 .

[66]  Graeme K. Yates,et al.  Changes in cochlear microphonic and neural sensitivity produced by acoustic trauma , 1989, Hearing Research.

[67]  Robert D Frisina,et al.  Encoding of amplitude modulation in the gerbil cochlear nucleus: I. A hierarchy of enhancement , 1990, Hearing Research.

[68]  Gerald M. Edelman,et al.  Auditory function : neurobiological bases of hearing , 1988 .

[69]  J. Goldberg,et al.  Response of binaural neurons of dog superior olivary complex to dichotic tonal stimuli: some physiological mechanisms of sound localization. , 1969, Journal of neurophysiology.

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

[71]  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.

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

[73]  H Steven Colburn,et al.  Coincidence model of MSO responses , 1990, Hearing Research.

[74]  N. Viemeister,et al.  Auditory intensity discrimination at high frequencies in the presence of noise. , 1983, Science.

[75]  B. Moore An Introduction to the Psychology of Hearing , 1977 .

[76]  E. Fowler,et al.  A METHOD FOR THE EARLY DETECTION OF OTOSCLEROSIS: A STUDY OF SOUNDS WELL ABOVE THRESHOLD , 1936 .

[77]  L. Carney Sensitivities of cells in anteroventral cochlear nucleus of cat to spatiotemporal discharge patterns across primary afferents. , 1990, Journal of neurophysiology.

[78]  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.

[79]  Paul B. Manis,et al.  Regularity of Discharge Constrains Models of Ventral Cochlear Nucleus Bushy Cells , 1993 .

[80]  J. D. Hood,et al.  Basic audiological requirements in neuro-otology , 1969, The Journal of Laryngology & Otology.

[81]  B C Moore,et al.  A comparison of four methods of implementing automatic gain control (AGC) in hearing aids. , 1988, British journal of audiology.

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

[83]  D. A. Goodman,et al.  Intensity Functions and Dynamic Responses from the Cochlea to the Cochlear Nucleus , 1938 .

[84]  J. F. Perkins Physiological Considerations , 1959 .

[85]  T. Yin,et al.  Responses to amplitude-modulated tones in the auditory nerve of the cat. , 1992, The Journal of the Acoustical Society of America.