Medial Olivocochlear Efferent Reflex in Humans: Otoacoustic Emission (OAE) Measurement Issues and the Advantages of Stimulus Frequency OAEs

Otoacoustic emissions (OAEs) are useful for studying medial olivocochlear (MOC) efferents, but several unresolved methodological issues cloud the interpretation of the data they produce. Most efferent assays use a “probe stimulus” to produce an OAE and an “elicitor stimulus” to evoke efferent activity and thereby change the OAE. However, little attention has been given to whether the probe stimulus itself elicits efferent activity. In addition, most studies use only contralateral (re the probe) elicitors and do not include measurements to rule out middle-ear muscle (MEM) contractions. Here we describe methods to deal with these problems and present a new efferent assay based on stimulus frequency OAEs (SFOAEs) that incorporates these methods. By using a postelicitor window, we make measurements in individual subjects of efferent effects from contralateral, ipsilateral, and bilateral elicitors. Using our SFOAE assay, we demonstrate that commonly used probe sounds (clicks, tone pips, and tone pairs) elicit efferent activity, by themselves. Thus, results of efferent assays using these probe stimuli can be confounded by unwanted efferent activation. In contrast, the single 40 dB SPL tone used as the probe sound for SFOAE-based measurements evoked little or no efferent activity. Since they evoke efferent activation, clicks, tone pips, and tone pairs can be used in an adaptation efferent assay, but such paradigms are limited in measurement scope compared to paradigms that separate probe and elicitor stimuli. Finally, we describe tests to distinguish middle-ear muscle (MEM) effects from MOC effects for a number of OAE assays and show results from SFOAE-based tests. The SFOAE assay used in this study provides a sensitive, flexible, frequency-specific assay of medial efferent activation that uses a low-level probe sound that elicits little or no efferent activity, and thus provides results that can be interpreted without the confound of unintended efferent activation.

[1]  L. J. Hood,et al.  Contralateral suppression of non-linear click-evoked otoacoustic emissions , 1993, Hearing Research.

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

[3]  L. Collet,et al.  Effect of contralateral acoustic stimulation on active cochlear micromechanical properties in human subjects: dependence on stimulus variables. , 1991, Journal of Neurophysiology.

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

[5]  S. Kujawa,et al.  Time-varying alterations in the f 2−f 1 DPOAE response to continuous primary stimulation I: Response characterization and contribution of the olivocochlear efferents , 1995, Hearing Research.

[6]  TS Sridhar,et al.  A novel cholinergic "slow effect" of efferent stimulation on cochlear potentials in the guinea pig , 1995, The Journal of neuroscience : the official journal of the Society for Neuroscience.

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

[8]  M G Evans,et al.  Acetylcholine activates two currents in guinea‐pig outer hair cells. , 1996, The Journal of physiology.

[9]  L Collet,et al.  Sinusoidal amplitude modulation alters contralateral noise suppression of evoked otoacoustic emissions in humans , 1999, Neuroscience.

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

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

[12]  G. Tavartkiladze,et al.  Ipsilateral suppression of transient evoked otoacoustic emission: role of the medial olivocochlear system. , 1996, Acta oto-laryngologica.

[13]  G. Zweig,et al.  The origin of periodicity in the spectrum of evoked otoacoustic emissions. , 1995, The Journal of the Acoustical Society of America.

[14]  P. A. Dorn,et al.  Adaptation of Distortion Product Otoacoustic Emission in Humans , 2001, Journal of the Association for Research in Otolaryngology.

[15]  R. H. Wilson,et al.  Threshold and growth of the acoustic reflex. , 1978, The Journal of the Acoustical Society of America.

[16]  A. Thornton,et al.  Effect of olivocochlear bundle section on evoked otoacoustic emissions recorded using maximum length sequences , 1997, Hearing Research.

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

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

[19]  J. Guinan,et al.  Separate mechanical processes underlie fast and slow effects of medial olivocochlear efferent activity , 2003, The Journal of physiology.

[20]  Dt Kemp.  Exploring cochlear status with otoacoustic emissions - the potential for new clinical applications , 2001 .

[21]  C. Micheyl,et al.  Contralateral frequency-modulated tones suppress transient-evoked otoacoustic emissions in humans , 1998, Hearing Research.

[22]  David T. Kemp,et al.  Effect of contralateral auditory stimuli on active cochlear micro-mechanical properties in human subjects , 1990, Hearing Research.

[23]  R. Bobbin,et al.  Additional pharmacological evidence that endogenous ATP modulates cochlear mechanics , 1998, Hearing Research.

[24]  J. Guinan,et al.  The ipsilaterally evoked olivocochlear reflex causes rapid adaptation of the 2f1-f2 distortion product otoacoustic emission. , 1996, The Journal of the Acoustical Society of America.

[25]  C. Micheyl,et al.  Medial olivocochlear efferent system in humans studied with amplitude-modulated tones. , 1997, Journal of neurophysiology.

[26]  Christopher A Shera,et al.  Stimulus-frequency-emission group delay: a test of coherent reflection filtering and a window on cochlear tuning. , 2003, The Journal of the Acoustical Society of America.

[27]  S. Gelfand.  5 – The Contralateral Acoustic-Reflex Threshold , 1984 .

[28]  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.

[29]  John J. Guinan,et al.  Asymmetries in the acoustic reflexes of the cat stapedius muscle , 1987, Hearing Research.

[30]  Jjg Bradford Backus,et al.  The Time Course of the Medial Olivocochlear Efferent Reflex in Humans. , 2003 .

[31]  J F Ashmore,et al.  Direct measurement of the action of acetylcholine on isolated outer hair cells of the guinea pig cochlea , 1991, Proceedings of the Royal Society of London. Series B: Biological Sciences.

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

[33]  The behaviour of the F 2−F 1 acoustic distortion product: Lack of effect of brainstem lesions in anaesthetized guinea pigs , 1995, Hearing Research.

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

[35]  D. Robertson,et al.  Physiological and morphological characterization of efferent neurones in the guinea pig cochlea , 1985, Hearing Research.

[36]  C. Berlin,et al.  Binaural noise suppresses linear click-evoked otoacoustic emissions more than ipsilateral or contralateral noise , 1995, Hearing Research.

[37]  Hendrikus Duifhuis,et al.  Biophysics of Hair Cell Sensory Systems , 1993 .

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

[39]  Martin S. Robinette,et al.  Otoacoustic Emissions: Clinical Applications , 1997 .

[40]  C. Talmadge,et al.  Interrelations among distortion-product phase-gradient delays: their connection to scaling symmetry and its breaking. , 2000, The Journal of the Acoustical Society of America.

[41]  J. Guinan,et al.  Evoked otoacoustic emissions arise by two fundamentally different mechanisms: a taxonomy for mammalian OAEs. , 1999, The Journal of the Acoustical Society of America.

[42]  P. Avan,et al.  Olivocochlear efferent vs. middle-ear contributions to the alteration of otoacoustic emissions by contralateral noise , 2000, Brain Research.

[43]  Bcb Watjana Lilaonitkul,et al.  Tuning of Ipsilateral, Contralateral and Binaural Medial Efferent Reflexes in Humans. , 2002 .

[44]  B. M. Johnstone,et al.  Stimulus‐related potassium changes in the organ of Corti of guinea‐pig. , 1989, The Journal of physiology.

[45]  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.