John J. Guinan

Single Auditory Units in the Superior Olivary Complex: II: Locations of Unit Categories and Tonotopic Organization

The locations of various categories of units are described and correlations are found between unit properties and unit locations. Units on the edges of the medial superior olive (MSO) and the lateral superior olive (LSO) appear to have properties different from units inside these nuclei. Many units in the dorsomedial periolivary nucleus had wide tuning curves and some had very long latencies. Almost all units in the medial nucleus of the trapezoid body (MNTB) had irregular firing patterns, but most units in the LSO and the dorsolateral periolivary nucleus had regular firing patterns. Class 2 (off) units may correspond to ‘stellate’ cells of the MNTB.With few exceptions, units dorsolateral to the MSO were excited by ipsilateral sounds, and units ventromedial to the MSO, or in the ventral nucleus of the lateral lemniscus (VNLL), were excited by contralateral sounds.Best frequencies were arranged from high to low (1) from ventromedial to dorsolateral in the MSO, (2) from the medial limb to the lateral limb i...

Olivocochlear efferents: anatomy, physiology, function, and the measurement of efferent effects in humans.

This review covers the basic anatomy and physiology of the olivocochlear reflexes and the use of otoacoustic emissions (OAEs) in humans to monitor the effects of one group, the medial olivocochlear (MOC) efferents. MOC fibers synapse on outer hair cells (OHCs), and activation of these fibers inhibits basilar membrane responses to low-level sounds. This MOC-induced decrease in the gain of the cochlear amplifier is reflected in changes in OAEs. Any OAE can be used to monitor MOC effects on the cochlear amplifier. Each OAE type has its own advantages and disadvantages. The most straightforward technique for monitoring MOC effects is to elicit MOC activity with an elicitor sound contralateral to the OAE test ear. MOC effects can also be monitored using an ipsilateral elicitor of MOC activity, but the ipsilateral elicitor brings additional problems caused by suppression and cochlear slow intrinsic effects. To measure MOC effects accurately, one must ensure that there are no middle-ear-muscle contractions. Although standard clinical middle-ear-muscle tests are not adequate for this, adequate tests can usually be done with OAE-measuring instruments. An additional complication is that most probe sounds also elicit MOC activity, although this does not prevent the probe from showing MOC effects elicited by contralateral sound. A variety of data indicate that MOC efferents help to reduce acoustic trauma and lessen the masking of transients by background noise; for instance, they aid in speech comprehension in noise. However, much remains to be learned about the role of efferents in auditory function. Monitoring MOC effects in humans using OAEs should continue to provide valuable insights into the role of MOC efferents and may also provide clinical benefits.

Middle‐Ear Characteristics of Anesthetized Cats

Ossicular motion was measured visually with stroboscopic illumination. Tonal stimulation ranged from 30 to 10 000 Hz. Up to 130 dB SPL (sound‐pressure level), the motion of the stapes is predominantly piston‐like, and its displacement amplitude is linearly related to sound pressure. At frequencies under 3000 Hz, the ossicles move as one rigid body; at higher frequencies, the stapes and incus displacements lag behind the malleus displacement, which suggests that the incudo‐malleolar joint flexes. From measurements of stapes displacement at known sound pressures, we calculate a transfer characteristic for the middle ear with the tympanic cavities open. The effects of closing the tympanic cavities on the transfer characteristic were determined from measurements in which the electric response recorded from the round window was used as an indicator of middle‐ear output. By combining these data, we obtain a transfer characteristic for the middle ear with the tympanic cavities intact. An attempt is made to compa...

Revised estimates of human cochlear tuning from otoacoustic and behavioral measurements

We develop an objective, noninvasive method for determining the frequency selectivity of cochlear tuning at low and moderate sound levels. Applicable in humans at frequencies of 1 kHz and above, the method is based on the measurement of stimulus-frequency otoacoustic emissions and, unlike previous noninvasive physiological methods, does not depend on the frequency selectivity of masking or suppression. The otoacoustic measurements indicate that at low sound levels human cochlear tuning is more than twice as sharp as implied by standard behavioral studies and has a different dependence on frequency. New behavioral measurements designed to minimize the influence of nonlinear effects such as suppression agree with the emission-based values. A comparison of cochlear tuning in cat, guinea pig, and human indicates that, contrary to common belief, tuning in the human cochlea is considerably sharper than that found in the other mammals. The sharper tuning may facilitate human speech communication.

Single Auditory Units in the Superior Olivary Complex: I: Responses to Sounds and Classifications Based on Physiological Properties

Response properties to sounds were examined in single auditory units in the superior olivary complex and the ventral nucleus of the lateral lemniscus. Units were divided into ten ‘classes’; four classes were defined by single properties (spike waveshape or the timing of responses to sound bursts) and the remaining six classes were defined by which ear excited or inhibited the units. Units were also divided according to the types of poststimulus-time histograms they produced in response to sound bursts, and they were separately divided according to the shape of their inter-spike interval histograms. These latter two groupings were highly correlated with each other and with unit class, and were combined into a single classification scheme called ‘firing-pattern type’.Units were divided into six groups based on the shapes of their tuning curves; data on the bandwidths of tuning curves are also presented. Data are presented on spontaneous firing rate, thresholds to best-frequency tones, and latency of respons...

Acoustically Responsive Fibers in the Vestibular Nerve of the Cat

Recordings were made from single afferent fibers in the inferior vestibular nerve, which innervates the saccule and posterior semicircular canal. A substantial portion of the fibers with irregular background activity increased their firing in response to moderately intense clicks and tones. In responsive fibers, acoustic clicks evoked action potentials with minimum latencies of < or = 1.0 msec. Fibers fell into two classes, with the shortest latency either to condensation clicks (PUSH fibers) or to rarefaction clicks (PULL fibers). Low- frequency (800 Hz) tone bursts at moderately high sound levels (> 80 dB SPL) caused synchronization of spikes to preferred phases of the tone cycle. PUSH and PULL fibers had preferred response phases approximately 180 degrees apart. These two response classes are consistent with fibers that innervate hair cells having opposite morphological polarizations, an arrangement found in the saccule. With low-frequency tone bursts, sound levels of > or = 90 dB SPL evoked increases in mean spike rate. Spike rates increased monotonically with sound level without saturating at levels < or = 115 dB SPL. Contraction of the middle-ear muscles decreased responses to sound, consistent with the sound transmission path being through the middle ear. Several fibers were labeled with biocytin and traced. All labeled fibers had bipolar cell bodies in the inferior vestibular ganglion with peripheral processes extending toward the saccular nerve and central processes in the vestibular nerve. Two fibers were traced to the saccular epithelium. One fiber was traced centrally and arborized extensively in vestibular nuclei and a region ventromedial to the cochlear nucleus. Our results confirm and extend previous suggestions that the mammalian saccule responds to sound at frequencies and levels within the normal range of human hearing. We suggest a number of auditory roles that these fibers may play in the everyday life of mammals.

Stimulus-frequency-emission group delay: A test of coherent reflection filtering and a window on cochlear tuning

This paper tests and applies a key prediction of the theory of coherent reflection filtering for the generation of reflection-source otoacoustic emissions. The theory predicts that reflection-source-emission group delay is determined by the group delay of the basilar-membrane (BM) transfer function at its peak. This prediction is tested over a seven-octave frequency range in cats and guinea pigs using measurements of stimulus-frequency-emission (SFOAE) group delay. A comparison with group delays calculated from published measurements of BM mechanical transfer functions supports the theory at the basal end of the cochlea. A comparison across the whole frequency range based on variations in the sharpness of neural tuning with characteristic frequency (CF) suggests that the predicted relation holds in the basal-most 60% of the cochlea. At the apical end of the cochlea, however, the measurements disagree with neural and mechanical group delays. This disagreement suggests that there are important differences in cochlear mechanics and/or mechanisms of emission generation between the base and apex of the cochlea. Measurements in humans over a four-octave range indicate that human SFOAE group delays are roughly a factor of 3 longer than their counterparts in cat and guinea pig but manifest similar trends across CF. The measurements thus reveal global deviations from scaling whose form appears quantitatively similar in all three species. Interpreted using the theory of coherent reflection filtering, the group delay measurements indicate that the wavelength at the peak of the traveling wave decreases with increasing CF at a rate of roughly 25% per octave in the base of the cochlea. The measurements and analysis reported here illustrate the rich potential inherent in OAE measurements for obtaining valuable information about basic cochlear properties such as tuning.

THE IPSILATERALLY EVOKED OLIVOCOCHLEAR REFLEX CAUSES RAPID ADAPTATION OF THE 2 F1-F2 DISTORTION PRODUCT OTOACOUSTIC EMISSION

The onset behavior of the distortion product otoacoustic emission (DPOAE) at 2f1-f2 in anesthetized cats was measured with temporal resolution finer than 70 ms. The amplitude of the DPOAE adapts after onset of the primary tones by as much as 6 dB for monaural stimulation and 10 dB when the primaries are presented binaurally. DPOAE adaptation consists of a large, rapid component, with a time constant of roughly 100 ms, and a small, slower component with a time constant of roughly 1000 ms. The rapid component disappears when only the crossed olivocochlear bundle (OCB) is cut, whereas the slow adaptation persists after complete OCB section. The loss of rapid adaptation upon OC section is accompanied by a concomitant increase in the steady-state amplitude of the DPOAE. Thus an intact OC reflex can significantly alter DPOAEs obtained during routine measurement. Rapid adaptation of the monaurally evoked 2f1-f2 DPOAE is probably mediated by reflex activity in ipsilaterally responsive OC neurons innervating outer hair cells. The effects of this ipsilateral reflex on DPOAE amplitudes are typically twice as large as those of the contralateral reflex, presumably because there are twice as many ipsilaterally responsive OC neurons. Tests for the ipsilateral OC reflex based on the phenomenon of rapid adaptation should be both feasible and useful in human subjects.

Vestibular evoked myogenic potentials show altered tuning in patients with Ménière's disease.

Objective: Acoustic stimulation of the saccule gives rise to a vestibulocollic reflex, the output of which can be measured in the neck as inhibition of activity in the ipsilateral sternocleidomastoid muscle. This vestibular evoked myogenic potential has been promoted as a means of assessing integrity of saccular function. In this study, we test the hypothesis that the cochleosaccular hydrops of Ménière’s syndrome leads to alterations in saccular motion that change the dynamics of the vestibular evoked myogenic potential. Study Design: Prospective cohort study. Setting: Large specialty hospital, department of otolaryngology. Subjects: Fourteen normal adult volunteers and 34 consecutive consenting adult patients with unilateral Ménière’s disease by American Academy of Otolaryngology–Head and Neck Surgery diagnostic criteria. Interventions: All subjects underwent vestibular evoked myogenic potential testing using ipsilateral broadband click and short tone-burst stimuli at 250, 500, 1,000, 2,000, and 4,000 Hz. Main Outcome Measures: Threshold, amplitude, and latency of vestibular evoked myogenic potential responses in normal and Ménière’s affected and unaffected ears. Results: Vestibular evoked myogenic potential was present in all ears tested. Normal subjects show a frequency-dependent vestibular evoked myogenic potential threshold, with best response (“frequency tuning”) at 500 Hz. Compared with normal subjects and unaffected ears of Ménière’s subjects, affected Ménière’s ears had significantly increased vestibular evoked myogenic potential thresholds. Affected Ménière’s ears showed threshold shifts at all frequencies and there was less tuning apparent at 500 Hz. Unaffected ears of Ménière’s subjects also showed significantly elevated vestibular evoked myogenic potential thresholds compared with normal subjects. Analyses of vestibular evoked myogenic potential thresholds for effects of age, hearing loss, and audiometric configuration showed no significant differences. Conclusions: Ménière’s ears display alterations in vestibular evoked myogenic potential threshold and tuning, supporting our hypothesis of altered saccular motion mechanics arising from hydropic distention. Unaffected ears of unilateral Ménière’s subjects show similar changes, though to a lesser degree. This finding may be because of occult saccular hydrops in the asymptomatic ear or binaural interactions in the vestibular evoked myogenic potential otolith–cervical reflex arc.

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.