Effects of electrical stimulation of efferent olivocochlear neurons on cat auditory-nerve fibers. III. Tuning curves and thresholds at CF

In order to study the effects of efferent activity, olivocochlear efferents were stimulated with an electrode in the fourth ventricle at the decussation of the crossed olivocochlear bundle (midline-OCB stimulation) or with an electrode at the brainstem origin of medial efferents (MOC stimulation). Tuning curves, or similar measures of threshold, were obtained from auditory-nerve fibers in the presence or absence of efferent stimulation. Efferent stimulation raised the thresholds of fibers for tones at the characteristic frequency (CF) by an amount which varied with the spontaneous rate (SR) of the auditory-nerve fiber. On the average, high-SR fibers had the smallest threshold shifts, and low-SR fibers had the largest threshold shifts. The distribution of threshold shifts as a function of CF peaked at CFs of 3-8 kHz for high-SR and medium-SR fibers but appeared to peak at higher CFs for low-SR fibers. Within the high-SR or medium-SR groups, the fibers with the lowest thresholds had the largest threshold shifts. Efferent stimulation decreased the Q20 of the tuning curves from most fibers (i.e. it made the tuning curves wider), but increased the Q20 from some fibers with CFs below 2 kHz. For fibers with CFs above 4 kHz, efferent stimulation shifted the tuning-curve tails to higher sound levels by about 1 dB on the average. The qualitative patterns of the effects due to midline-OCB stimulation or to MOC stimulation were similar. The distribution of high-SR threshold shifts vs. CF appears to be displaced apically in the cochlea compared to the distribution of MOC endings on outer hair cells. This can be understood in terms of efferent activity depressing basilar membrane motion and affecting regions at, and apical to, the activated efferent synapses. To explain the low-SR threshold shifts, an additional way in which efferent activity inhibits responses appears to be required. The data are consistent with one function of the medial efferents being to raise the thresholds of auditory-nerve fibers and thereby adjust the effective range of the auditory system.

[1]  C. Geisler Model of crossed olivocochlear bundle effects. , 1974, The Journal of the Acoustical Society of America.

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

[3]  D. O. Kim Active and nonlinear cochlear biomechanics and the role of outer-hair-cell subsystem in the mammalian auditory system , 1986, Hearing Research.

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

[5]  A. Nuttall,et al.  Efferent control of cochlear inner hair cell responses in the guinea‐pig. , 1984, The Journal of physiology.

[6]  D Robertson,et al.  Response properties of spiral ganglion neurons in cochleas damaged by direct mechanical trauma. , 1980, The Journal of the Acoustical Society of America.

[7]  M. Liberman Morphological differences among radial afferent fibers in the cat cochlea: An electron-microscopic study of serial sections , 1980, Hearing Research.

[8]  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.

[9]  John J. Guinan,et al.  Effects of electrical stimulation of efferent olivocochlear neurons on cat auditory-nerve fibers. II. Spontaneous rate , 1988, Hearing Research.

[10]  P M Sellick,et al.  Intracellular studies of hair cells in the mammalian cochlea. , 1978, The Journal of physiology.

[11]  Stephen T. Neely,et al.  An active cochlear model showing sharp tuning and high sensitivity , 1983, Hearing Research.

[12]  J. Guinan,et al.  Effects of crossed-olivocochlear-bundle stimulation on cat auditory nerve fiber responses to tones. , 1983, The Journal of the Acoustical Society of America.

[13]  J. P. Wilson,et al.  THE FREQUENCY SELECTIVITY OF THE COCHLEA , 1973 .

[14]  R. A. Schmiedt Boundaries of two-tone rate suppression of cochlear-nerve activity , 1982, Hearing Research.

[15]  M. B. Sachs,et al.  Representation of a low-frequency tone in the discharge rate of populations of auditory nerve fibers , 1986, Hearing Research.

[16]  N. Kiang,et al.  Effects of electric stimulation of the crossed olivocochlear bundle on single auditory-nerve fibers in the cat. , 1970, The Journal of the Acoustical Society of America.

[17]  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.

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

[19]  John J. Guinan,et al.  Efferent innervation of the organ of corti: two separate systems , 1979, Brain Research.

[20]  J. Guinan,et al.  Topographic organization of the olivocochlear projections from the lateral and medial zones of the superior olivary complex , 1984, The Journal of comparative neurology.

[21]  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 .

[22]  D. O. Kim,et al.  Efferent neural control of cochlear mechanics? Olivocochlear bundle stimulation affects cochlear biomechanical nonlinearity , 1982, Hearing Research.

[23]  J. Guinan,et al.  Effect of efferent neural activity on cochlear mechanics. , 1986, Scandinavian audiology. Supplementum.

[24]  J. Guinan,et al.  Differential olivocochlear projections from lateral versus medial zones of the superior olivary complex , 1983, The Journal of comparative neurology.

[25]  M. Liberman Single-neuron labeling in the cat auditory nerve. , 1982, Science.

[26]  J. Cranford,et al.  Behavioral auditory function after transection of crossed olivo-cochlear bundle in the cat. IV. Study on pure-tone frequency discrimination. , 1979, Acta Oto-Laryngologica.

[27]  P Dallos,et al.  Response characteristics of mammalian cochlear hair cells , 1985, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[28]  W. Buño,et al.  Effect of electrical stimulation of the olivo cochlear bundle at the cochlear level. , 1970, Acta neurologica latinoamericana.

[29]  M. C. Brown,et al.  Physiology and anatomy of single olivocochlear neurons in the cat , 1986, Hearing Research.

[30]  D. T. Kemp,et al.  Otoacoustic emissions, travelling waves and cochlear mechanisms , 1986, Hearing Research.

[31]  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.

[32]  C D Geisler,et al.  Thresholds for primary auditory fibers using statistically defined criteria. , 1985, The Journal of the Acoustical Society of America.

[33]  J. Guinan,et al.  Effects of electrical stimulation of medial olivocochlear neurons on ipsilateral and contralateral cochlear responses , 1987, Hearing Research.

[34]  M. Charles Liberman,et al.  Single-neuron labeling and chronic cochlear pathology. I. Threshold shift and characteristic-frequency shift , 1984, Hearing Research.

[35]  D. C. Teas,et al.  Electrophysiological Studies on the Spatial Distribution of the Crossed Olivocochlear Bundle along the Guinea Pig Cochlea , 1970 .

[36]  M. Wiederhold Variations in the effects of electric stimulation of the crossed olivocochlear bundle on cat single auditory-nerve-fiber responses to tone bursts. , 1970, The Journal of the Acoustical Society of America.

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

[38]  W. F. Sewell,et al.  The relation between the endocochlear potential and spontaneous activity in auditory nerve fibres of the cat. , 1984, The Journal of physiology.

[39]  J. Cranford,et al.  Behavioral Auditory Function After Transectlon of Crossed Olivo-Cochlear Bundle in the Cat , 1974 .

[40]  D. Mountain,et al.  Changes in endolymphatic potential and crossed olivocochlear bundle stimulation alter cochlear mechanics. , 1980, Science.