Lateral suppression and inhibition in the cochlear nucleus of the cat.

1. The ability of cells in the cochlear nucleus (CN) to encode frequency information in the presence of background noise on the basis of "place/rate" information was investigated by measuring the threshold, magnitude, and extent of lateral suppression in the ventral and dorsal CN of the anesthesized cat. The suppression regions were delineated through the use of "masked" response areas (MRAs). The MRA is a family of isointensity curves derived from the average discharge rate in response to a tone of variable frequency and sound pressure level in the presence of a concurrently presented broadband, quasi-flat-spectrum noise. Tonal stimuli of sufficient intensity are often effective in significantly reducing the average discharge rate of CN neurons over a wide frequency range. 2. Most units in the CN exhibit prominent lateral suppressive sidebands, but the variability in threshold, magnitude, and extent of suppression is large. Primary-like and onset units of the ventral CN manifest the least suppression and have the highest suppression thresholds. Pauser/buildup units in the dorsal division and choppers distributed throughout the CN show the largest amount of suppression and have the lowest suppression thresholds. 3. Auditory nerve fibers manifest some degree of lateral suppression, particularly fibers of low and medium spontaneous rate. However, in few instances are the threshold, magnitude, and extent comparable with that observed among the majority of chopper and pauser/buildup units. For this reason the lateral suppression observed among the latter unit types is unlikely to originate entirely from cochlear processes, but rather is likely to reflect largely neural mechanisms intrinsic to the CN. In contrast, the MRAs of most primary-like and onset units suggest that the suppression behavior of most of these cells originates mostly, if not entirely, in the cochlea and auditory nerve. 4. A primary consequence of lateral suppression is to preserve the sharp frequency selectivity of CN neurons at moderate to high sound pressure levels, particularly in background noise. In this fashion lateral suppressive mechanisms potentially enhance the representation of spectral information on the basis of place/rate information relative to that in the auditory nerve under noisy background conditions. 5. Lateral suppressive mechanisms probably underlie the dynamic range shift seen in the presence of a simultaneously presented noise. This mechanism may be crucial for preserving the ability to perceive signals in a noisy background.

[1]  H. K. Hartline,et al.  INHIBITORY INTERACTION OF RECEPTOR UNITS IN THE EYE OF LIMULUS , 1957, The Journal of general physiology.

[2]  J. R. Hughes,et al.  Microelectrode studies of the cochlear nuclei of the cat. , 1959, Bulletin of the Johns Hopkins Hospital.

[3]  D. D. Greenwood,et al.  Excitatory and inhibitory response areas of auditory neurons in the cochlear nucleus. , 1965, Journal of neurophysiology.

[4]  M. Sachs,et al.  Two-tone inhibition in auditory-nerve fibers. , 1968, The Journal of the Acoustical Society of America.

[5]  D. D. Greenwood,et al.  Response of neurons in the cochlear nuclei to variations in noise bandwidth and to tone-noise combinations. , 1970, The Journal of the Acoustical Society of America.

[6]  E. C. Kane,et al.  Octopus cells in the cochlear nucleus of the cat: heterotypic synapses upon homeotypic neurons. , 1973, The International journal of neuroscience.

[7]  E C Kane,et al.  Synaptic organization in the dorsal cochlear nucleus of the cat: A light and electron microscopic study , 1974 .

[8]  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.

[9]  P J Abbas,et al.  Two-tone suppression in auditory-nerve fibers: extension of a stimulus-response relationship. , 1976, The Journal of the Acoustical Society of America.

[10]  G. Zweig Basilar membrane motion. , 1976, Cold Spring Harbor symposia on quantitative biology.

[11]  E. Young,et al.  Responses to tones and noise of single cells in dorsal cochlear nucleus of unanesthetized cats. , 1976, Journal of neurophysiology.

[12]  C D Geisler,et al.  Auditory nerve fiber response to wide-band noise and tone combinations. , 1978, Journal of neurophysiology.

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

[14]  C. Daniel Geisler,et al.  Responses of primary auditory fibers to combined noise and tonal stimuli , 1980, Hearing Research.

[15]  H. Voigt,et al.  Evidence of inhibitory interactions between neurons in dorsal cochlear nucleus. , 1980, Journal of neurophysiology.

[16]  J. L. Goldstein On the Signal Processing Potential of High Threshold Auditory Nerve Fibers , 1980 .

[17]  N. Cant,et al.  The fine structure of two types of stellate cells in the anterior division of the anteroventral cochlear nucleus of the cat , 1981, Neuroscience.

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

[19]  N. Cant,et al.  Pathways connecting the right and left cochlear nuclei , 1982, The Journal of comparative neurology.

[20]  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.

[21]  D. K. Morest,et al.  The neuronal architecture of the anteroventral cochlear nucleus of the cat in the region of the cochlear nerve root: Electron microscopy , 1982, Neuroscience.

[22]  W. S. Rhode,et al.  Physiological response properties of cells labeled intracellularly with horseradish peroxidase in cat ventral cochlear nucleus , 1983, The Journal of comparative neurology.

[23]  C D Geisler,et al.  Responses of auditory-nerve fibers to consonant-vowel syllables. , 1981, The Journal of the Acoustical Society of America.

[24]  W. S. Rhode,et al.  Physiological response properties of cells labeled intracellularly with horseradish peroxidase in cat dorsal cochlear nucleus , 1983, The Journal of comparative neurology.

[25]  J. Dickson,et al.  Lateral inhibition in the anteroventral cochlear nucleus of the cat: A microiontophoretic study , 1983, Hearing Research.

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

[27]  R. Patuzzi,et al.  The modulation of the sensitivity of the mammalian cochlea by low frequency tones. II. Inner hair cell receptor potentials , 1984, Hearing Research.

[28]  B. M. Johnstone,et al.  The modulation of the sensitivity of the mammalian cochlea by low frequency tones. III. Basilar membrane motion , 1984, Hearing Research.

[29]  W. S. Rhode,et al.  Electron microscopic features of physiologically characterized, HRP‐labeled fusiform cells in the cat dorsal cochlear nucleus , 1985, The Journal of comparative neurology.

[30]  E. Young,et al.  Similarity of dynamic range adjustment in auditory nerve and cochlear nuclei. , 1985, Journal of neurophysiology.

[31]  W. S. Rhode,et al.  Characteristics of tone-pip response patterns in relationship to spontaneous rate in cat auditory nerve fibers , 1985, Hearing Research.

[32]  J. Zempel,et al.  Immunocytochemical localization of GABA in the cochlear nucleus of the guinea pig , 1986, Brain Research.

[33]  D. Oertel,et al.  Inhibitory circuitry in the ventral cochlear nucleus is probably mediated by glycine , 1986, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[34]  E. Rouiller,et al.  The central projections of intracellularly labeled auditory nerve fibers in cats: an analysis of terminal morphology. , 1986, The Journal of comparative neurology.

[35]  W. S. Rhode,et al.  Physiological studies on neurons in the dorsal cochlear nucleus of cat. , 1986, Journal of neurophysiology.

[36]  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.

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

[38]  E D Young,et al.  Rate responses of auditory nerve fibers to tones in noise near masked threshold. , 1986, The Journal of the Acoustical Society of America.

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

[40]  W. S. Rhode,et al.  Physiological study of neurons in the dorsal and posteroventral cochlear nucleus of the unanesthetized cat. , 1987, Journal of neurophysiology.

[41]  W. Shofner,et al.  Inhibitory connections between AVCN and DCN: Evidence from lidocaine injection in AVCN , 1987, Hearing Research.

[42]  W. S. Rhode,et al.  Characterization of HRP‐labeled globular bushy cells in the cat anteroventral cochlear nucleus , 1987, The Journal of comparative neurology.

[43]  Joe C. Adams,et al.  Patterns of glutamate decarboxylase immunostaining in the feline cochlear nuclear complex studied with silver enhancement and electron microscopy , 1987, The Journal of comparative neurology.

[44]  J. A. Hirsch,et al.  Intrinsic properties of neurones in the dorsal cochlear nucleus of mice, in vitro. , 1988, The Journal of physiology.

[45]  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.

[46]  C. Daniel Geisler,et al.  Representation of speech sounds in the auditory nerve , 1988 .

[47]  Neal F. Viemeister Psychophysical aspects of auditory intensity coding: Neurobiological Bases of Hearing , 1988 .

[48]  John J. Guinan,et al.  Effects of electrical stimulation of efferent olivocochlear neurons on cat auditory-nerve fibers. I. Rate-level functions , 1988, 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]  M. Sachs,et al.  Rate-place and temporal-place representations of vowels in the auditory nerve and anteroventral cochlear nucleus , 1988 .

[51]  C D Geisler The responses of models of "high-spontaneous" auditory-nerve fibers in a damaged cochlea to speech syllables in noise. , 1989, The Journal of the Acoustical Society of America.

[52]  C D Geisler,et al.  Responses of "high-spontaneous" auditory-nerve fibers to consonant-vowel syllables in noise. , 1989, The Journal of the Acoustical Society of America.

[53]  D. Oertel,et al.  Morphology and physiology of cells in slice preparations of the dorsal cochlear nucleus of mice , 1989, The Journal of comparative neurology.

[54]  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.

[55]  J. L. Goldstein,et al.  Auditory nerve rate-level functions for two-tone stimuli: Possible relation to basilar membrane nonlinearity , 1989, Hearing Research.

[56]  D. Oertel,et al.  Morphology and physiology of cells in slice preparations of the posteroventral cochlear nucleus of mice , 1990, The Journal of comparative neurology.

[57]  C. Daniel Geisler,et al.  Saturation of outer hair cell receptor currents causes two-tone suppression , 1990, Hearing Research.

[58]  J. Kearney,et al.  Functional Relationship Between , 1991 .

[59]  C D Geisler,et al.  Responses of "lower-spontaneous-rate" auditory-nerve fibers to speech syllables presented in noise. I: General characteristics. , 1991, The Journal of the Acoustical Society of America.

[60]  D. Ryugo,et al.  Synaptic connections of the auditory nerve in cats: Relationship between endbulbs of held and spherical bushy cells , 1991, The Journal of comparative neurology.

[61]  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.

[62]  William S. Rhode,et al.  Two-tone suppression and distortion production on the basilar membrane in the hook region of cat and guinea pig cochleae , 1993, Hearing Research.

[63]  The inhibitory mechanisms of sound processing in the dorsal cochlear nucleus of the guinea pig. , 1995 .