Equivalent-rectangular bandwidth of single units in the anaesthetized guinea-pig ventral cochlear nucleus

Frequency-tuning is a fundamental property of auditory neurons. The filter bandwidth of peripheral auditory neurons determines the frequency resolution of an animal's auditory system. Behavioural studies in animals and humans have defined frequency-tuning in terms of the "equivalent-rectangular bandwidth" (ERB) of peripheral filters. In contrast, most physiological studies report the Q [best frequency/bandwidth] of frequency-tuning curves. This study aims to accurately describe the ERB of primary-like and chopper units in the ventral cochlear nucleus, the first brainstem processing station of the central auditory system. Recordings were made from 1020 isolated single units in the ventral cochlear nucleus of anesthetized guinea pigs in response to pure-tone stimuli which varied in frequency and in sound level. Frequency-threshold tuning curves were constructed for each unit and estimates of the ERB determined using methods previously described for auditory-nerve-fibre data in the same species. Primary-like, primary-notch, and sustained- and transient-chopper units showed frequency selectivity almost identical to that recorded in the auditory nerve. Their tuning at pure-tone threshold can be described as a function of best frequency (BF) by ERB = 0.31 * BF(0.5).

[1]  Mario A. Ruggero,et al.  Physiology and Coding of Sound in the Auditory Nerve , 1992 .

[2]  B. Schofield,et al.  Auditory cortical projections to the cochlear nucleus in guinea pigs , 2005, Hearing Research.

[3]  D. O. Kim,et al.  Auditory nerve spatial encoding of high-frequency pure tones: Population response profiles derived from d' measure associated with nearby places along the cochlea , 1991, Hearing Research.

[4]  C D Geisler,et al.  Responses of "lower-spontaneous-rate" auditory-nerve fibers to speech syllables presented in noise. II: Glottal-pulse periodicities. , 1991, The Journal of the Acoustical Society of America.

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

[6]  Brian R Glasberg,et al.  Derivation of auditory filter shapes from notched-noise data , 1990, Hearing Research.

[7]  Alan R Palmer,et al.  Descending projections from auditory cortex modulate sensitivity in the midbrain to cues for spatial position. , 2008, Journal of neurophysiology.

[8]  Stephen T. Neely,et al.  Signals, Sound, and Sensation , 1997 .

[9]  M. Ruggero,et al.  Mechanical bases of frequency tuning and neural excitation at the base of the cochlea: comparison of basilar-membrane vibrations and auditory-nerve-fiber responses in chinchilla. , 2000, Proceedings of the National Academy of Sciences of the United States of America.

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

[11]  Mario A Ruggero,et al.  Unexceptional sharpness of frequency tuning in the human cochlea. , 2005, Proceedings of the National Academy of Sciences of the United States of America.

[12]  Bertrand Delgutte,et al.  Spatio-Temporal Representation of the Pitch of Complex Tones in the Auditory Nerve , 2007 .

[13]  B Masterton,et al.  Behavioral measurements of absolute and frequency-difference thresholds in guinea pig. , 1971, The Journal of the Acoustical Society of America.

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

[15]  Gerald Langner,et al.  A simulation of chopper neurons in the cochlear nucleus with wideband input from onset neurons , 2008, Biological Cybernetics.

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

[17]  W. S. Rhode,et al.  Encoding timing and intensity in the ventral cochlear nucleus of the cat. , 1986, Journal of neurophysiology.

[18]  B. Delgutte,et al.  Speech coding in the auditory nerve: V. Vowels in background noise. , 1984, The Journal of the Acoustical Society of America.

[19]  E D Young,et al.  Auditory nerve representation of vowels in background noise. , 1983, Journal of neurophysiology.

[20]  J. L. Goldstein An optimum processor theory for the central formation of the pitch of complex tones. , 1973, The Journal of the Acoustical Society of America.

[21]  M. Ruggero,et al.  Similarity of Traveling-Wave Delays in the Hearing Organs of Humans and Other Tetrapods , 2007, Journal for the Association for Research in Otolaryngology.

[22]  B. Grothe,et al.  Inhibiting the Inhibition: A Neuronal Network for Sound Localization in Reverberant Environments , 2007, The Journal of Neuroscience.

[23]  N Suga,et al.  The corticofugal system for hearing: recent progress. , 2000, Proceedings of the National Academy of Sciences of the United States of America.

[24]  A. M. Mimpen,et al.  The ear as a frequency analyzer. II. , 1964, The Journal of the Acoustical Society of America.

[25]  N Suga,et al.  Corticofugal Modulation of Time-Domain Processing of Biosonar Information in Bats , 1996, Science.

[26]  Nace L. Golding,et al.  Synaptic inputs to stellate cells in the ventral cochlear nucleus. , 1998, Journal of neurophysiology.

[27]  I. Winter,et al.  Reverberation Challenges the Temporal Representation of the Pitch of Complex Sounds , 2008, Neuron.

[28]  W. Shofner,et al.  Regularity and latency of units in ventral cochlear nucleus: implications for unit classification and generation of response properties. , 1988, Journal of neurophysiology.

[29]  D B Moody,et al.  Auditory thresholds and kanamycin-induced hearing loss in the guinea pig assessed by a positive reinforcement procedure. , 1978, The Journal of the Acoustical Society of America.

[30]  N. Suga,et al.  Corticofugal amplification of facilitative auditory responses of subcortical combination-sensitive neurons in the mustached bat. , 1999, Journal of neurophysiology.

[31]  I. Winter,et al.  Frequency extent of two-tone facilitation in onset units in the ventral cochlear nucleus. , 1996, Journal of neurophysiology.

[32]  Ian M. Winter,et al.  Responses of Dorsal Cochlear Nucleus Neurons to Signals in the Presence of Modulated Maskers , 2004, The Journal of Neuroscience.

[33]  R. Patterson,et al.  The deterioration of hearing with age: frequency selectivity, the critical ratio, the audiogram, and speech threshold. , 1982, The Journal of the Acoustical Society of America.

[34]  Nobuo Suga,et al.  Multiparametric corticofugal modulation and plasticity in the auditory system , 2003, Nature Reviews Neuroscience.

[35]  J. Fritz,et al.  Adaptive changes in cortical receptive fields induced by attention to complex sounds. , 2007, Journal of neurophysiology.

[36]  J. Ashmore Cochlear outer hair cell motility. , 2008, Physiological reviews.

[37]  T. Duke,et al.  Physical basis of two-tone interference in hearing , 2001, Proceedings of the National Academy of Sciences of the United States of America.

[38]  E F Evans,et al.  The frequency response and other properties of single fibres in the guinea‐pig cochlear nerve , 1972, The Journal of physiology.

[39]  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.

[40]  B C Moore,et al.  Auditory filter shapes in subjects with unilateral and bilateral cochlear impairments. , 1986, The Journal of the Acoustical Society of America.

[41]  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.

[42]  M. Sachs,et al.  Effect of electrical stimulation of the crossed olivocochlear bundle on auditory nerve response to tones in noise. , 1987, Journal of neurophysiology.

[43]  S Rosen,et al.  Auditory filter nonlinearity at 2 kHz in normal hearing listeners. , 1998, The Journal of the Acoustical Society of America.

[44]  I. Winter,et al.  Contralateral inhibitory and excitatory frequency response maps in the mammalian cochlear nucleus , 2006, The European journal of neuroscience.

[45]  J. Rauschecker,et al.  The role of auditory cortex in the formation of auditory streams , 2007, Hearing Research.

[46]  Ray Meddis,et al.  Physiological Correlates of Comodulation Masking Release in the Mammalian Ventral Cochlear Nucleus , 2001, The Journal of Neuroscience.

[47]  R. Patterson Auditory filter shapes derived with noise stimuli. , 1976, The Journal of the Acoustical Society of America.

[48]  Jun Yan,et al.  The midbrain creates and the thalamus sharpens echo-delay tuning for the cortical representation of target-distance information in the mustached bat , 1996, Hearing Research.

[49]  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.

[50]  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.

[51]  J. Rauschecker,et al.  Perceptual Organization of Tone Sequences in the Auditory Cortex of Awake Macaques , 2005, Neuron.

[52]  P. Dallos Cochlear amplification, outer hair cells and prestin , 2008, Current Opinion in Neurobiology.

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

[54]  Daniel Pressnitzer,et al.  The psychophysics and physiology of comodulation masking release , 2003, Experimental Brain Research.

[55]  Mounya Elhilali,et al.  Task Difficulty and Performance Induce Diverse Adaptive Patterns in Gain and Shape of Primary Auditory Cortical Receptive Fields , 2009, Neuron.

[56]  Richard R. Fay,et al.  Comparative Hearing: Mammals , 1994, Springer Handbook of Auditory Research.

[57]  D. Pressnitzer,et al.  Perceptual Organization of Sound Begins in the Auditory Periphery , 2008, Current Biology.

[58]  Joshua G. W. Bernstein,et al.  Pitch discrimination of diotic and dichotic tone complexes: harmonic resolvability or harmonic number? , 2003, The Journal of the Acoustical Society of America.

[59]  W. T. Peake,et al.  Shapes of tuning curves for single auditory-nerve fibers. , 1967, The Journal of the Acoustical Society of America.

[60]  Muhammad S A Zilany,et al.  Modeling auditory-nerve responses for high sound pressure levels in the normal and impaired auditory periphery. , 2006, The Journal of the Acoustical Society of America.

[61]  E. Terhardt Pitch, consonance, and harmony. , 1974, The Journal of the Acoustical Society of America.

[62]  I. Fried,et al.  Ultra-fine frequency tuning revealed in single neurons of human auditory cortex , 2008, Nature.

[63]  F. Wightman The pattern-transformation model of pitch. , 1973, The Journal of the Acoustical Society of America.

[64]  B. Delgutte,et al.  Pitch of complex tones: rate-place and interspike interval representations in the auditory nerve. , 2005, Journal of neurophysiology.

[65]  E D Young,et al.  Excitatory/inhibitory response types in the cochlear nucleus: relationships to discharge patterns and responses to electrical stimulation of the auditory nerve. , 1985, Journal of neurophysiology.

[66]  Ray Meddis,et al.  A computer model of the auditory-nerve response to forward-masking stimuli. , 2005, The Journal of the Acoustical Society of America.

[67]  M. Mulheran The effects of quinine on cochlear nerve fibre activity in the guinea pig , 1999, Hearing Research.

[68]  Ray Meddis,et al.  Virtual pitch in a computational physiological model. , 2006, The Journal of the Acoustical Society of America.

[69]  A. Ainsworth,et al.  Glass-coated platinum-plated tungsten microelectrodes , 1972, Medical and biological engineering.

[70]  Christopher A Shera,et al.  Revised estimates of human cochlear tuning from otoacoustic and behavioral measurements , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[71]  L. Cedolin Neural representations of pitch : role of peripheral frequency selectivity , 2006 .

[72]  Ray Meddis,et al.  The temporal representation of speech in a nonlinear model of the guinea pig cochlea. , 2004, The Journal of the Acoustical Society of America.

[73]  Ray Meddis,et al.  The representation of periodic sounds in simulated sustained chopper units of the ventral cochlear nucleus. , 2004, The Journal of the Acoustical Society of America.

[74]  I. Winter,et al.  The temporal representation of the delay of dynamic iterated rippled noise with positive and negative gain by single units in the ventral cochlear nucleus , 2007, Brain Research.

[75]  R. Fay,et al.  The Mammalian auditory pathway : neurophysiology , 1992 .

[76]  Mounya Elhilali,et al.  Monkey Frequency-Modulation Encoding in the Primary Auditory Cortex of the Awake Owl , 2001 .

[77]  I. Winter,et al.  The time course of recovery from suppression and facilitation from single units in the mammalian cochlear nucleus , 2006, Hearing Research.

[78]  Jun Yan,et al.  Corticofugal shaping of frequency tuning curves in the central nucleus of the inferior colliculus of mice. , 2005, Journal of neurophysiology.

[79]  Andrew J. Oxenham,et al.  Estimates of Human Cochlear Tuning at Low Levels Using Forward and Simultaneous Masking , 2003, Journal of the Association for Research in Otolaryngology.

[80]  E. F. Evans,et al.  Comparisons of Physiological and Behavioural Properties: Auditory Frequency Selectivity , 1992 .

[81]  I. Winter,et al.  Ambiguous Pitch and the Temporal Representation of Inharmonic Iterated Rippled Noise in the Ventral Cochlear Nucleus , 2008, The Journal of Neuroscience.

[82]  E. F. Evans,et al.  The responses of single neurones in the cochlear nucleus of the cat as a function of their location and the anaesthetic state , 1973, Experimental Brain Research.

[83]  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.

[84]  M. Sachs,et al.  Vowel representations in the ventral cochlear nucleus of the cat: effects of level, background noise, and behavioral state. , 1998, Journal of neurophysiology.

[85]  S Shamma,et al.  The case of the missing pitch templates: how harmonic templates emerge in the early auditory system. , 2000, The Journal of the Acoustical Society of America.

[86]  H. Fletcher Loudness, Masking and Their Relation to the Hearing Process and the Problem of Noise Measurement , 1938 .

[87]  B. Moore,et al.  Frequency selectivity as a function of level and frequency measured with uniformly exciting notched noise. , 2000, The Journal of the Acoustical Society of America.

[88]  P. Jen,et al.  Corticofugal modulation of directional sensitivity in the midbrain of the big brown bat, Eptesicus fuscus , 2005, Hearing Research.