Cochlear microphonics and otoacoustic emissions in chronically de-efferented chinchilla

doi:10.1016/S0378-5955(99)00217-8

Hearing Research

Volume 143, Issues 1–2, May 2000, Pages 14-22

https://doi.org/10.1016/S0378-5955(99)00217-8 Get rights and content

Abstract

The effects of eliminating the olivocochlear bundle (OCB) on cochlear electromechanical properties were examined by measuring cochlear microphonics (CM) and distortion product otoacoustic emissions (DPOAEs) in chronically de-efferented chinchillas. The OCB fibers to the right ears were successfully sectioned in six out of 15 adult chinchillas via a posterior paraflocular fossa approach. At the end of the experiment, these ears were histologically verified as being deprived of both lateral and medial OCB fibers. The opposite (left) ears from the animals served as controls. Following de-efferentation, changes of the inter-modulation distortion components (2f₁−f₂, f₂−f₁, 3f₁−2f₂, 3f₂−2f₁) varied, depending on the frequencies and levels of the stimuli. DPOAE amplitudes to low-level stimuli were within the 95% confidence intervals around mean DPOAE amplitudes of the control ears at all the frequencies (1–8 kHz). At high stimulus levels, DPOAE amplitudes increased by 5–20 dB at 1 and 2 kHz while remaining in the normal range at 4 and 8 kHz. In contrast, the CM input/output functions to stimuli from 1 to 8 kHz were significantly reduced by approximately 40–50% at all input levels. The results suggest that the OCB may play a role in modulating electrical properties of the outer hair cells and in reducing the magnitude of cochlear distortion to high-level stimuli.

Introduction

The olivocochlear bundle (OCB) consists of two separate fiber bundles. Fibers of the medial olivocochlear (MOC) bundle arise from cells in the medial region of the superior olivary complex and innervate the outer hair cells (OHCs). Fibers of the lateral OCB arise from cells in and around the lateral superior olive and innervate afferent dendrites under the inner hair cells (Brown, 1987, Guinan et al., 1983, Iurato et al., 1978, Rasmussen, 1946, Warr, 1992). As the MOC fibers directly innervate the OHCs with large synapses, they may influence cochlear mechanics through direct modulation of the OHCs. In fact, electrical stimulation of the MOC fibers increases the amplitude of the cochlear microphonics (CM) (Fex, 1959), reduces auditory nerve input to the central nervous system (see Wiederhold, 1986 for review) and alters the amplitude of distortion product otoacoustic emissions (DPOAEs) (Mountain, 1980, Siegel and Kim, 1982). Presentation of sound to one ear can alter DPOAEs in the opposite ear (Kujawa et al., 1993) and elimination of the MOC fibers abolishes this effect (Liberman et al., 1996, Puel and Rebillard, 1990). Auditory nerve fiber tuning, which largely depends on active mechanical processing of the OHCs (Khanna and Leonard, 1982, Robles et al., 1986), is broadened when cochlear efferents are eliminated (Zheng et al., 1999). Collectively, these studies indicate that the cochlear efferent system plays a role in modulating the OHCs, and consequently cochlear function.

The normal inner ear contains an active biomechanical mechanism, which underlies the selectivity of hearing (Brownell et al., 1985, Santos-Sacchi, 1989). This biomechanical mechanism involves the active participation of non-linear and vulnerable elements that are very sensitive to changes in OHC receptor current (Patuzzi et al., 1989). There are little available data concerning the tonic influence of the OCB on the electromechanical activity of the cochlea. Both CM and DPOAE are considered to be reflections of OHC electromotility and basilar membrane vibration. In the present study, CM and DPOAEs were measured in chinchillas devoid of both LOC and MOC efferent fibers, as verified by cochlear acetylcholinesterase (AChE) staining. The completely de-efferented animal model provides a unique perspective on the tonic effects of the OCB on the hair cells and cochlear electromechanics.

Section snippets

Materials and methods

The OCB innervating the right cochlea was transected via a posterior fossa approach in 15 adult chinchillas. Each animal was deeply anesthetized by an intramuscular injection of ketamine (54 mg/kg) and acepromazine (0.64 mg/kg). After a right postauricular incision was made, the cerebellum was exposed via a posterior craniotomy. The posterior lateral hemisphere of the cerebellum was gently aspirated to expose the internal auditory meatus. A fine hook was used to avulse the inferior vestibular

Results

No AChE staining could be discerned in five of the six operated right ears, verifying that the OCB was completely sectioned. Fig. 1 shows the AChE staining at the basal (8 kHz region, Fig. 1A) and apical (1 kHz region, Fig. 1B) turns in one left (efferent-innervated) cochlea and basal turns from two right (de-efferented) cochleae (Fig. 1C,D). As seen in Fig. 1A,B, the efferent-innervated ear was intensely stained for AChE at both the inner hair cell and OHC regions. Both the inner and tunnel

Discussion

The current data show that cochlear de-efferentation results in significant CM depression at all frequencies and DPOAE enhancement at low frequencies. Specifically, CM amplitude was decreased at 1–8 kHz (Fig. 6) whereas DPOAE amplitudes were increased at 1 and 2 kHz to high-level stimuli (Fig. 2, Fig. 3, Fig. 4, Fig. 5). These results complement previous reports that stimulation of the cochlear efferents increases CM (Fex, 1959, Patuzzi and Rajan, 1990, Wiederhold and Peake, 1966) and depresses

Acknowledgements

This work was supported by the Edward H. Rosen Grant for Auditory Science (National Organization for Hearing Research 150-1409A) to X.Y.Z. and NIH150-1596P to S.L.M.

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The cochlea has highly specialized receptor cells, the hair cells, that transduce mechanical vibrations from acoustic stimuli into changes of cell-membrane electrical potentials. These electrical responses give origin to action potentials that are conducted through afferent neural pathways to the central nervous system, where auditory perception takes place. However, in addition to afferent pathways, the auditory system has conspicuous efferent pathways that project from the central nervous structures to the periphery, reaching as far as the hair cells and afferent nerve fibers from the inner ear. These efferent fibers modify the incoming sensory information at various levels of the afferent pathway. This chapter provides a general and comprehensive summary of the current knowledge about the auditory efferent system in mammals, discussing research data obtained in animals as well as in humans. It reviews the main findings on the anatomy, neurotransmission, and physiology of the auditory efferent system and discusses possible clinical implications and some of the functions that have been proposed for the efferent system.
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It is interesting that the recovery and enhancement occurred after SP and CAP had stabilized (Fig. 3D). The results are consistent with previous data showing faster recovery of IC-EVP amplitudes than CAP amplitudes following temporary deafferentation by kainic acid (Zheng et al., 2000). The results are also consistent with previous studies showing that evoked response amplitudes can decrease, increase or remain unchanged after carboplatin, depending on the recording site.
Carboplatin produces progressive damage to auditory nerve fibers, spiral ganglion neurons (SGNs) and inner hair cells (IHC) in the chinchilla cochlea but leaves outer hair cells intact. Within 1 h after injection, many afferent terminals beneath IHCs and myelin lamellae surrounding SGN processes are vacuolated. One day after injection, approximately half of the nerve fibers are missing. IHCs are intact at 2 days, but 20–30% are missing at 3 days. We studied the electrophysiological correlates of this progressive morphological damage by recording cochlear microphonics (CM), distortion product otoacoustic emissions (DPOAE), summating potentials (SP), compound action potentials (CAP) and midbrain evoked potentials (IC-EVP) before and 1 h, 12 h, 1 days, 3 days, 5 days, 7 days and 14 days after carboplatin injection (75 mg/kg IP) in four chinchillas. CM and DPOAEs tended to be unchanged or enhanced. CAP and SP showed little change until Day 3, when amplitudes were reduced in all animals and CAP thresholds were elevated by 9 dB; amplitudes declined further between Days 3 and 5 but not thereafter. IC-EVP amplitudes decreased on Days 3 or 5 but thresholds were relatively unchanged. All animals showed some recovery of IC-EVP between Days 7 and 14, including one with 70% enhancement on Day 14. The results indicate that threshold and amplitude measures fail to detect peripheral pathology until some relatively high threshold level of damage has been exceeded. This has important implications for monitoring peripheral damage and interpreting electrophysiological test results in animals and humans.
Chlorpromazine inhibits cochlear function in guinea pigs
2004, Hearing Research
Outer hair cell (OHC) electromotility provides mechanical positive feedback that functions as the cochlear amplifier. In isolated OHCs, chlorpromazine shifts the electromotility voltage–displacement transfer function in a depolarizing direction without affecting its magnitude. This study sought to measure the effects of chlorpromazine on cochlear function in vivo. Salicylate, a drug that greatly reduces the magnitude of electromotility, was used for comparison. Perilymphatic perfusion of the guinea pig cochlea with chlorpromazine or salicylate increased the compound action potential (CAP) threshold across the frequency spectrum (1–20 kHz). Both drugs also increased distortion product otoacoustic emission (DPOAE) thresholds in the higher frequencies (10–20 kHz). Complete reversibility of these effects occurred after washout. Both drugs demonstrated concentration-dependent reductions in cochlear function that followed sigmoidal curves with similar fits to previously reported results in isolated OHCs. The endolymphatic potential was not affected by either of these drugs. Thus, chlorpromazine inhibits cochlear function in a manner consistent with what would be expected from data in isolated OHCs. This suggests that shifting the electromotility transfer function correspondingly reduces the gain of the cochlear amplifier.
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DPOAE temporary level shift (TLS) at 2f₁ − f₂ and f₂ − f₁, ABR temporary threshold shift (TTS), and detailed histopathological findings were compared in three groups of chinchillas that were exposed for 24 h to an octave band of noise (OBN) centered at 4 kHz with a sound pressure level (SPL) of 80, 86 or 92 dB (n = 3, 4, 6). DPOAE levels at 39 frequencies from f₁ = 0.3 to 16 kHz (f₂/f₁ = 1.23; L₂ and L₁ = 55, 65 and 75 dB, equal and differing by 10 dB) and ABR thresholds at 13 frequencies from 0.5 to 20 kHz were collected pre- and immediately post-exposure. The functional data were converted to pre- minus post-exposure shift and overlaid upon the cytocochleogram of cochlear damage using the frequency-place map for the chinchilla. The magnitude and frequency place of components in the 2f₁−f₂ TLS patterns were determined and group averages for each OBN SPL and L₁, L₂ combination were calculated. The f₂ − f₁ TLS was also examined in ears with focal lesions equal to or greater than 0.4 mm. The 2f₁ − f₂ TLS (plotted at f₁) and TTS aligned with the extent and location of damaged supporting cells. The TLS patterns over frequency had two features which were unexpected: (1) a peak at about a half octave above the center of the OBN with a valley just above and below it and (2) a peak (often showing enhancement) at the apical boundary of the supporting-cell damage. The magnitudes of the TLS and TTS generally increased with increasing SPL of the exposure. The peaks of the TLS and TTS, as well as the peaks and valleys of the TLS pattern moved apically as the SPL of the OBN was increased. However, there was little consistency in the pattern relations with differing L₁, L₂ combinations. In addition, neither the 2f₁ − f₂ nor f₂ − f₁ TLS for any L₁, L₂ combination reliably detected focal lesions (100% OHC loss) from 0.4 to 1.2 mm in size. Often, the TLS went in the opposite direction from what would be expected at focal lesions. Recovery from TLS and TTS was also examined in seven animals. Both TLS and TTS recovered partially or completely, the magnitude depending upon exposure SPL.

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Cochlear microphonics and otoacoustic emissions in chronically de-efferented chinchilla

Abstract

Introduction

Section snippets

Materials and methods

Results

Discussion

Acknowledgements

Hear. Res.

Cell

Hear. Res.

Hear. Res.

Hear. Res.

Hear. Res.

Hear. Res.

Hear. Res.

Hear. Res.

Hear. Res.

A fast motile response in guinea-pig outer hair cells: The cellular basis of the cochlear amplifier

J. Physiol. (Lond.)

Variations of cochlear microphonic potential after sectioning efferent fibers to the cochlea

Hear. Res.

Morphology of labeled efferent fibers in the guinea pig cochlea

Neurology

Evoked mechanical responses of isolated cochlear outer hair cells

Science

Cochlear inner and outer hair cells: Functional differences

Science

Acetylcholine, outer hair cell electromotility, and the cochlear amplifier

J. Neurosci.

Augmentation of the cochlear microphonics by stimulation of efferent fibres to the cochlea

Acta Otolaryngol. (Stockh.)