Human Medial Olivocochlear Reflex: Effects as Functions of Contralateral, Ipsilateral, and Bilateral Elicitor Bandwidths

Animal studies have led to the view that the acoustic medial olivocochlear (MOC) efferent reflex provides sharply tuned frequency-specific feedback that inhibits cochlear amplification. To determine if MOC activation is indeed narrow band, we measured the MOC effects in humans elicited by 60-dB sound pressure level (SPL) contralateral, ipsilateral, and bilateral noise bands as a function of noise bandwidth from 1/2 to 6.7 octaves. MOC effects were quantified by the change in stimulus frequency otoacoustic emissions from 40 dB SPL probe tones near 0.5, 1, and 4 kHz. In a second experiment, the noise bands were centered 2 octaves below probe frequencies near 1 and 4 kHz. In all cases, the MOC effects increased as elicitor bandwidth increased, with the effect saturating at about 4 octaves. Generally, the MOC effects increased as the probe frequency decreased, opposite expectations based on MOC innervation density in the cochlea. Bilateral-elicitor effects were always the largest. The ratio of ipsilateral/contralateral effects depended on elicitor bandwidth; the ratio was large for narrow-band probe-centered elicitors and approximately unity for wide-band elicitors. In another experiment, the MOC effects from increasing elicitor bandwidths were calculated from measurements of the MOC effects from adjacent half-octave noise bands. The predicted bandwidth function agreed well with the measured bandwidth function for contralateral elicitors, but overestimated it for ipsilateral and bilateral elicitors. Overall, the results indicate that (1) the MOC reflexes integrate excitation from almost the entire cochlear length, (2) as elicitor bandwidth is increased, the excitation from newly stimulated cochlear regions more than overcomes the reduced excitation at frequencies in the center of the elicitor band, and (3) contralateral, ipsilateral, and bilateral elicitors show MOC reflex spatial summation over most of the cochlea, but ipsilateral spatial summation is less additive than contralateral.

[1]  E. de Boer,et al.  The mechanical waveform of the basilar membrane. II. From data to models--and back. , 2000, The Journal of the Acoustical Society of America.

[2]  D. Velenovsky,et al.  The effect of noise bandwidth on the contralateral suppression of transient evoked otoacoustic emissions , 2002, Hearing Research.

[3]  M. Norman,et al.  Frequency analysis of the contralateral suppression of evoked otoacoustic emissions by narrow-band noise. , 1993, British journal of audiology.

[4]  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.

[5]  C. Micheyl,et al.  Activation of medial olivocochlear efferent system in humans: influence of stimulus bandwidth , 2000, Hearing Research.

[6]  C. Talmadge,et al.  Testing coherent reflection in chinchilla: Auditory-nerve responses predict stimulus-frequency emissions. , 2008, The Journal of the Acoustical Society of America.

[7]  J. Guinan Olivocochlear Efferents: Anatomy, Physiology, Function, and the Measurement of Efferent Effects in Humans , 2006, Ear and hearing.

[8]  H. Schuknecht,et al.  The localization of acetylcholinesterase in the cochlea. , 1959, A.M.A. archives of otolaryngology.

[9]  J. Guinan Physiology of Olivocochlear Efferents , 1996 .

[10]  J. Nadol,et al.  Prevalence and ultrastructural morphology of axosomatic synapses on spiral ganglion cells in humans of different ages 1 1 Presented at the 23rd ARO Midwinter Meeting, St. Petesburgh, FL, USA, February 18–24, 2000. , 2000, Hearing Research.

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

[12]  M. Liberman,et al.  Response properties of cochlear efferent neurons: monaural vs. binaural stimulation and the effects of noise. , 1988, Journal of neurophysiology.

[13]  J. Guinan,et al.  Olivocochlear reflex assays: effects of contralateral sound on compound action potentials versus ear-canal distortion products. , 1996, The Journal of the Acoustical Society of America.

[14]  P. Fuchs,et al.  The Synaptic Physiology of Cochlear Hair Cells , 2002, Audiology and Neurotology.

[15]  M. Charles Liberman,et al.  Reciprocal Synapses Between Outer Hair Cells and their Afferent Terminals: Evidence for a Local Neural Network in the Mammalian Cochlea , 2008, Journal of the Association for Research in Otolaryngology.

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

[17]  Douglas H. Keefe,et al.  Two-tone suppression of stimulus frequency otoacoustic emissions. , 2008, The Journal of the Acoustical Society of America.

[18]  K. Morawski,et al.  Influence of Contralateral Stimulation by Two-tone Complexes, Narrow-band and Broad-band Noise Signals on the 2f 1 -f 2 Distortion Product Otoacoustic Emission Levels in Humans , 2002, Acta oto-laryngologica.

[19]  R. Kalluri,et al.  Comparing stimulus-frequency otoacoustic emissions measured by compression, suppression, and spectral smoothing. , 2007, The Journal of the Acoustical Society of America.

[20]  Alberto Recio-Spinoso,et al.  Delays of stimulus-frequency otoacoustic emissions and cochlear vibrations contradict the theory of coherent reflection filtering. , 2005, The Journal of the Acoustical Society of America.

[21]  C. Micheyl,et al.  Contralateral suppression of transiently evoked otoacoustic emissions by harmonic complex tones in humans. , 1999, The Journal of the Acoustical Society of America.

[22]  J. Nadol,et al.  Patterns of innervation of outer hair cells in a chimpanzee: II. Efferent endings , 1993, Hearing Research.

[23]  D. T. Kemp,et al.  Observations on the Generator Mechanism of Stimulus Frequency Acoustic Emissions — Two Tone Suppression , 1980 .

[24]  M. C. Brown,et al.  Single olivocochlear neurons in the guinea pig. I. Binaural facilitation of responses to high-level noise. , 1998, Journal of neurophysiology.

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

[26]  T Kawase,et al.  Antimasking effects of the olivocochlear reflex. II. Enhancement of auditory-nerve response to masked tones. , 1993, Journal of neurophysiology.

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

[28]  J. Nadol,et al.  Patterns of innervation of outer hair cells in a chimpanzee: I. Afferent and reciprocal synapses , 1993, Hearing Research.

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

[30]  Donald Robertson,et al.  Horseradish peroxidase injection of physiologically characterized afferent and efferent neurones in the guinea pig spiral ganglion , 1984, Hearing Research.

[31]  P. Rabinowitz,et al.  Noise-induced hearing loss. , 2000, American family physician.

[32]  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.

[33]  Watjana Lilaonitkul,et al.  Reflex control of the human inner ear: a half-octave offset in medial efferent feedback that is consistent with an efferent role in the control of masking. , 2009, Journal of neurophysiology.

[34]  Bias due to noise in otoacoustic emission measurements. , 2007, The Journal of the Acoustical Society of America.

[35]  M. C. Brown Morphology and response properties of single olivocochlear fibers in the guinea pig , 1989, Hearing Research.

[36]  D. Kemp,et al.  A new rapid component in the cochlear response to brief electrical efferent stimulation: CM and otoacoustic observations , 1988, Hearing Research.

[37]  Christopher A Shera,et al.  Laser amplification with a twist: traveling-wave propagation and gain functions from throughout the cochlea. , 2007, The Journal of the Acoustical Society of America.

[38]  John J. Guinan,et al.  Measurement of the Distribution of Medial Olivocochlear Acoustic Reflex Strengths Across Normal-Hearing Individuals via Otoacoustic Emissions , 2007, Journal of the Association for Research in Otolaryngology.

[39]  M. M. Henson,et al.  Synaptic specializations associated with the outer hair cells of the Japanese macaque , 1997, Hearing Research.

[40]  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.

[41]  J. Nadol,et al.  Axodendritic and dendrodendritic synapses within outer spiral bundles in a human , 2002, Hearing Research.

[42]  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.

[43]  Peter Dallos,et al.  Prestin-Based Outer Hair Cell Motility Is Necessary for Mammalian Cochlear Amplification , 2008, Neuron.

[44]  Watjana Lilaonitkul,et al.  Medial Olivocochlear Efferent Reflex in Humans: Otoacoustic Emission (OAE) Measurement Issues and the Advantages of Stimulus Frequency OAEs , 2003, Journal of the Association for Research in Otolaryngology.

[45]  John J Guinan,et al.  Effects of electrical stimulation of efferent olivocochlear neurons on cat auditory-nerve fibers. III. Tuning curves and thresholds at CF , 1988, Hearing Research.

[46]  J. Guinan Changes in Stimulus Frequency Otoacoustic Emissions Produced by Two-Tone Suppression and Efferent Stimulation in Cats , 1990 .

[47]  Nigel P. Cooper,et al.  Efferent‐mediated control of basilar membrane motion , 2006, The Journal of physiology.

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

[49]  G. C. Thompson,et al.  Olivocochlear neurons in the squirrel monkey brainstem , 1986, The Journal of comparative neurology.