Dataset Information

Fast and slow effects of medial olivocochlear efferent activity in humans.

ABSTRACT:

Background

The medial olivocochlear (MOC) pathway modulates basilar membrane motion and auditory nerve activity on both a fast (10-100 ms) and a slow (10-100 s) time scale in guinea pigs. The slow MOC modulation of cochlear activity is postulated to aide in protection against acoustic trauma. However in humans, the existence and functional roles of slow MOC effects remain unexplored.

Methodology/principal findings

By employing contralateral noise at moderate to high levels (68 and 83 dB SPL) as an MOC reflex elicitor, and spontaneous otoacoustic emissions (SOAEs) as a non-invasive probe of the cochlea, we demonstrated MOC modulation of human cochlear output both on a fast and a slow time scale, analogous to the fast and slow MOC efferent effects observed on basilar membrane vibration and auditory nerve activity in guinea pigs. The magnitude of slow effects was minimal compared with that of fast effects. Consistent with basilar membrane and auditory nerve activity data, SOAE level was reduced by both fast and slow MOC effects, whereas SOAE frequency was elevated by fast and reduced by slow MOC effects. The magnitudes of fast and slow effects on SOAE level were positively correlated.

Conclusions/significance

Contralateral noise up to 83 dB SPL elicited minimal yet significant changes in both SOAE level and frequency on a slow time scale, consistent with a high threshold or small magnitude of slow MOC effects in humans.

SUBMITTER: Zhao W

PROVIDER: S-EPMC3073004 | biostudies-literature | 2011 Apr

REPOSITORIES: biostudies-literature

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Publications

Fast and slow effects of medial olivocochlear efferent activity in humans.

Zhao Wei W Dhar Sumitrajit S

PloS one 20110408 4

<h4>Background</h4>The medial olivocochlear (MOC) pathway modulates basilar membrane motion and auditory nerve activity on both a fast (10-100 ms) and a slow (10-100 s) time scale in guinea pigs. The slow MOC modulation of cochlear activity is postulated to aide in protection against acoustic trauma. However in humans, the existence and functional roles of slow MOC effects remain unexplored.<h4>Methodology/principal findings</h4>By employing contralateral noise at moderate to high levels (68 and ...[more]

PMID: 21494578

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Project description:The descending auditory system modulates the ascending system at every level. The final descending, or efferent, stage comprises lateral olivocochlear and medial olivocochlear (MOC) neurons. MOC somata in the ventral brainstem project axons to the cochlea to synapse onto outer hair cells (OHC), inhibiting OHC-mediated cochlear amplification. MOC suppression of OHC function is implicated in cochlear gain control with changing sound intensity, detection of salient stimuli, attention and protection against acoustic trauma. Thus, sound excites MOC neurons to provide negative feedback of the cochlea. Sound also inhibits MOC neurons via medial nucleus of the trapezoid body (MNTB) neurons. However, MNTB-MOC synapses exhibit short-term depression, suggesting reduced MNTB-MOC inhibition during sustained stimuli. Further, due to high rates of both baseline and sound-evoked activity in MNTB neurons in vivo, MNTB-MOC synapses may be tonically depressed. To probe this, we characterized short-term plasticity of MNTB-MOC synapses in mouse brain slices. We mimicked in vivo-like temperature and extracellular calcium conditions, and in vivo-like activity patterns of fast synaptic activation rates, sustained activation and prior tonic activity. Synaptic depression was sensitive to extracellular calcium concentration and temperature. During rapid MNTB axon stimulation, postsynaptic currents in MOC neurons summated but with concurrent depression, resulting in smaller, sustained currents, suggesting tonic inhibition of MOC neurons during rapid circuit activity. Low levels of baseline MNTB activity did not significantly reduce responses to subsequent rapid activity that mimics sound stimulation, indicating that, in vivo, MNTB inhibition of MOC neurons persists despite tonic synaptic depression. KEY POINTS: Inhibitory synapses from the medial nucleus of the trapezoid body (MNTB) onto medial olivocochlear (MOC) neurons exhibit short-term plasticity that is sensitive to calcium and temperature, with enhanced synaptic depression occurring at higher calcium concentrations and at room temperature. High rates of background synaptic activity that mimic the upper limits of spontaneous MNTB activity cause tonic synaptic depression of MNTB-MOC synapses that limits further synaptic inhibition. High rates of activity at MNTB-MOC synapses cause synaptic summation with concurrent depression to yield a response with an initial large amplitude that decays to a tonic inhibition.

Project description:Research suggests that college-aged adults are vulnerable to tinnitus and hearing loss due to exposure to traumatic levels of noise on a regular basis. Recent human studies have associated exposure to high noise exposure background (NEB, i.e., routine noise exposure) with the reduced cochlear output and impaired speech processing ability in subjects with clinically normal hearing sensitivity. While the relationship between NEB and the functions of the auditory afferent neurons are studied in the literature, little is known about the effects of NEB on functioning of the auditory efferent system. The objective of the present study was to investigate the relationship between medial olivocochlear reflex (MOCR) strength and NEB in subjects with clinically normal hearing sensitivity. It was hypothesized that subjects with high NEB would exhibit reduced afferent input to the MOCR circuit which would subsequently lead to reduced strength of the MOCR. In normal-hearing listeners, the study examined (1) the association between NEB and baseline click-evoked otoacoustic emissions (CEOAEs) and (2) the association between NEB and MOCR strength. The MOCR was measured using CEOAEs evoked by 60 dB pSPL linear clicks in a contralateral acoustic stimulation (CAS)-off and CAS-on (a broadband noise at 60 dB SPL) condition. Participants with at least 6 dB signal-to-noise ratio (SNR) in the CAS-off and CAS-on conditions were included for analysis. A normalized CEOAE inhibition index was calculated to express MOCR strength in a percentage value. NEB was estimated using a validated questionnaire. The results showed that NEB was not associated with the baseline CEOAE amplitude (r = -0.112, p = 0.586). Contrary to the hypothesis, MOCR strength was positively correlated with NEB (r = 0.557, p = 0.003). NEB remained a significant predictor of MOCR strength (β = 2.98, t(19) = 3.474, p = 0.003) after the unstandardized coefficient was adjusted to control for effects of smoking, sound level tolerance (SLT) and tinnitus. These data provide evidence that MOCR strength is associated with NEB. The functional significance of increased MOCR strength is discussed.

Project description:ObjectivesThe medial olivocochlear (MOC) efferent system can modify cochlear function to improve sound detection in noise, but its role in speech perception in noise is unclear. The purpose of this study was to determine the association between MOC efferent activity and performance on two speech-in-noise tasks at two signal-to-noise ratios (SNRs). It was hypothesized that efferent activity would be more strongly correlated with performance at the more challenging SNR, relative to performance at the less challenging SNR.DesignSixteen adults aged 35 to 73 years participated. Subjects had pure-tone averages ≤25 dB HL and normal middle ear function. High-frequency pure-tone averages were computed across 3000 to 8000 Hz and ranged from 6.3 to 48.8 dB HL. Efferent activity was assessed using contralateral suppression of transient-evoked otoacoustic emissions (TEOAEs) measured in right ears, and MOC activation was achieved by presenting broadband noise to left ears. Contralateral suppression was expressed as the decibel change in TEOAE magnitude obtained with versus without the presence of the broadband noise. TEOAE responses were also examined for middle ear muscle reflex activation and synchronous spontaneous otoacoustic emissions (SSOAEs). Speech-in-noise perception was assessed using the closed-set coordinate response measure word recognition task and the open-set Institute of Electrical and Electronics Engineers sentence task. Speech and noise were presented to right ears at two SNRs. Performance on each task was scored as percent correct. Associations between contralateral suppression and speech-in-noise performance were quantified using partial rank correlational analyses, controlling for the variables age and high-frequency pure-tone average.ResultsOne subject was excluded due to probable middle ear muscle reflex activation. Subjects showed a wide range of contralateral suppression values, consistent with previous reports. Three subjects with SSOAEs had similar contralateral suppression results as subjects without SSOAEs. The magnitude of contralateral suppression was not significantly correlated with speech-in-noise performance on either task at a single SNR (p > 0.05), contrary to hypothesis. However, contralateral suppression was significantly correlated with the slope of the psychometric function, computed as the difference between performance levels at the two SNRs divided by 3 (decibel difference between the 2 SNRs) for the coordinate response measure task (partial rs = 0.59; p = 0.04) and for the Institute of Electrical and Electronics Engineers task (partial rs = 0.60; p = 0.03).ConclusionsIn a group of primarily older adults with normal hearing or mild hearing loss, olivocochlear efferent activity assessed using contralateral suppression of TEOAEs was not associated with speech-in-noise performance at a single SNR. However, auditory efferent activity appears to be associated with the slope of the psychometric function for both a word and sentence recognition task in noise. Results suggest that individuals with stronger MOC efferent activity tend to be more responsive to changes in SNR, where small increases in SNR result in better speech-in-noise performance relative to individuals with weaker MOC efferent activity. Additionally, the results suggest that the slope of the psychometric function may be a more useful metric than performance at a single SNR when examining the relationship between speech recognition in noise and MOC efferent activity.

Project description: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.

Dataset Information

Fast and slow effects of medial olivocochlear efferent activity in humans.

Background

Methodology/principal findings

Conclusions/significance

Publications

Fast and slow effects of medial olivocochlear efferent activity in humans.

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