Afferent synaptic changes in auditory hair cells during noise-induced temporary threshold shift

doi:10.1016/0378-5955(95)00014-U

Hearing Research

Volume 84, Issues 1–2, April 1995, Pages 81-90

https://doi.org/10.1016/0378-5955(95)00014-U Get rights and content

Abstract

This study presents evidence in support of the hypothesis that one of the sites of failure during noise-induced temporary threshold shift (TTS) is the afferent synapse between auditory hair cells and auditory nerve fibers. Our results show clear evidence indicating changes in the quantity of afferent synapses and the morphology of presynaptic structures in the alligator lizard auditory hair cells during TTS. In TTS hair cells there are statistically significant decreases in: 1) the number of afferent synapses, 2) the number of synaptic vesicles at the afferent synapses, 3) the size of synaptic bodies, and 4) the packing density of synaptic vesicles around the synaptic body. These results suggest that the presynaptic components of the afferent synapse reflect the functional state of the synapse, and that the reduction of these synapses, both in number and component size, contributes to TTS.

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Citation Excerpt :
Cochlear afferent synapses between inner hair cells (IHCs) and type I spiral ganglion neurons (SGNs) are sensitive to noise-induced damage, the mechanism for which has been attributed to glutamate excitotoxicity (Pujol et al., 1990; Pujol et al., 1993; Henry and Mulroy, 1995; Puel, 1995; Puel et al., 1997, 1998; Pujol and Puel, 1999).
A single brief noise exposure can cause a significant loss of cochlear afferent synapses without causing permanent threshold shift. Previously we reported that the initial synaptic loss is partially reversible in Guinea pigs, indicating that synaptic loss can be categorized as either temporary or permanent. Since synaptic loss is biased to innervating auditory nerve fibers (ANFs) with low spontaneous spike rates (SSR), which are critical to the coding of in-background noise, coding-in-noise deficits (CIND) have been predicted to result from noise-induced synaptic damage. However, recent study of the noise masking of amplitude-modulation (AM) evoked compound action potentials (CAP) tailed to find evidence for such deficits in either mice or Guinea pigs. The present study sought to determine the effects of repeated noise exposure on temporary and permanent synaptic loss in Guinea pigs and C57 mice, whether such effects were additive, and whether repeated noise exposure induced CIND in Guinea pigs. The results show that the second noise exposure caused much less temporary synaptic loss and no additional permanent loss in Guinea pigs; however, an additional permanent loss was seen after the second noise was in the mice, although it was not significant. In Guinea pigs, the observed increased masking of the AM CAP provides evidence for CIND after repeated noise exposure.
No longer falling on deaf ears: Mechanisms of degeneration and regeneration of cochlear ribbon synapses
2015, Hearing Research
Citation Excerpt :
TTS noise has been also reported to increase the volume of cytoplasmic vacuoles in presynaptic IHC compartments, presumably caused by buildup of recycled synaptic membranes that are not efficiently reconstituted to functional synaptic vesicles (Mulroy et al., 1990). These events are accompanied by dramatically decreased ribbon synaptic densities within 2–24 h post-exposure (Kujawa and Liberman, 2009; Wan et al., 2014) and also dramatic reduction in the number of synaptic vesicles, size and packing density of the synaptic bodies (Henry and Mulroy, 1995). Importantly, despite a complete reversal of auditory brain-stem response (ABR) thresholds at 2 weeks post-exposure, the loss of ribbon synapses appears to be permanent (Kujawa and Liberman, 2009; Lin et al., 2011; Wan et al., 2014).
Cochlear ribbon synapses are required for the rapid and precise neural transmission of acoustic signals from inner hair cells to the spiral ganglion neurons. Emerging evidence suggests that damage to these synapses represents an important form of cochlear neuropathy that might be highly prevalent in sensorineural hearing loss. In this review, we discuss our current knowledge on how ribbon synapses are damaged by noise and during aging, as well as potential strategies to promote ribbon synapse regeneration for hearing restoration.
This article is part of a Special Issue entitled <Annual Reviews 2015>.
Effects of substance P during the recovery of hearing function after noise-induced hearing loss
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Citation Excerpt :
For the mild hearing loss group, damage to the OHCs was difficult to detect (Control; 39±0.447, SP10−3 M; 39±0.632, SP10−2 M; 38.8±0.8, AT; 38.8±0.97, ANOVA, F=0.024, p=0.9946). The results for both the severe and moderate noise-induced hearing loss groups were in agreement with previously reported findings on PTS (Spoendlin, 1985; Sugahara et al., 2003; Hu et al., 2006) and TTS (Henry and Mulroy, 1995; Pujol and Puel, 1999). Changes over time in the number of synaptic ribbons beneath the IHC nuclei with and without pretreatment with SP at 10−2 M were analyzed in the moderate noise-induced hearing loss groups through evaluation of the number of CtBP2 signals beneath the IHC nuclei under a fluorescent microscope (Fig. 5).
Substance P (SP) is a widely distributed neurotransmitter in living tissues and is involved in various repair processes. We investigated the possibility that SP may ameliorate cochlear hair cell damage produced by noise exposure. The present study examined the effect of SP in protecting the cochlea from noise damage in guinea pigs exposed to noise after an infusion of SP into the inner ear. Changes in the hearing threshold (auditory brain response, ABR), number of synaptic ribbons, and the appearance of the outer hair cells after noise exposure were analyzed at 2 severity levels of noise-induced hearing loss. The moderate noise-induced hearing loss (110 dB, 3 h) group showed recovery in the ABR threshold over time, finally reaching a level slightly above pre-exposure levels, with only slight injury to the synaptic ribbons and minimal changes in the appearance of the outer hair cells. Our results indicated that in moderate hearing loss, SP exhibited a protective effect on the inner ear, both functionally and structurally. While the final magnitude of ABR threshold elevation was greater in severe noise-induced hearing loss, the synaptic ribbons and outer hair cells showed signs of severe damage.
Antioxidant treatment reduces blast-induced cochlear damage and hearing loss
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Citation Excerpt :
The failure to detect a TTS in the control blast-exposed group by DPOAE testing suggests that the damage to the OHC may be so severe that it is not reversible without the therapeutic intervention, whereas, the neural component can partially recover as reflected by the ABR data showing a TTS. Henry and Mulroy (1995) have shown that noise exposure results in reduction of the afferent synapses between the auditory hair cells and auditory nerve fibers contributes to the TTS. Kujawa and Lieberman (2009) have demonstrated that noise overexposure results in acute loss of afferent nerve terminals and delayed degeneration of the cochlear nerve.
Exposure to blast overpressure has become one of the hazards of both military and civilian life in many parts of the world due to war and terrorist activity. Auditory damage is one of the primary sequela of blast trauma, affecting immediate situational awareness and causing permanent hearing loss. Protecting against blast exposure is limited by the inability to anticipate the timing of these exposures, particularly those caused by terrorists. Therefore a therapeutic regimen is desirable that is able to ameliorate auditory damage when administered after a blast exposure has occurred. The purpose of this study was to determine if administration of a combination of antioxidants 2,4-disulfonyl α-phenyl tertiary butyl nitrone (HPN-07) and N-acetylcysteine (NAC) beginning 1 h after blast exposure could reduce both temporary and permanent hearing loss. To this end, a blast simulator was developed and the operational conditions established for exposing rats to blast overpressures comparable to those encountered in an open-field blast of 14 pounds per square inch (psi). This blast model produced reproducible blast overpressures that resulted in physiological and physical damage to the auditory system that was proportional to the number and amplitude of the blasts. After exposure to 3 consecutive 14 psi blasts 100% of anesthetized rats had permanent hearing loss as determined at 21 days post exposure by auditory brainstem response (ABR) and distortion product otoacoustic emission (DPOAE) testing. Animals treated with HPN-07 and NAC after blast exposure showed a significant reduction in ABR threshold shifts and DPOAE level shifts at 2–16 kHz with significant reduction in inner hair cell (IHC) and outer hair cell (OHC) loss across the 5–36 kHz region of the cochlea compared with control animals.
The time course of changes in the auditory system was documented at 3 h, 24 h, 7 day and 21 day after blast exposure. At 3 h after blast exposure the auditory brainstem response (ABR) threshold shifts were elevated by 60 dB in both treated and control groups. A partial recovery of to 35 dB was observed at 24 h in the controls, indicative of a temporary threshold shift (TTS) and there was essentially no further recovery by 21 days representing a permanent threshold shift (PTS) of about 30 dB. Antioxidant treatment increased the amount of both TTS and PTS recovery relative to controls by 10 and 20 dB respectively. Distortion product otoacoustic emission (DPOAE) reached a maximum level shift of 25–30 dB measured in both control and treated groups at 3 h after blast exposure. These levels did not change by day 21 in the control group but in the treatment group the level shifts began to decline at 24 h until by day 21 they were 10–20 dB below that of the controls. Loss of cochlear hair cells measured at 21 day after blast exposure was mostly in the outer hair cells (OHC) and broadly distributed across the basilar membrane, consistent with the distribution of loss of frequency responses as measured by ABR and DPOAE analysis and typical of blast-induced damage. OHC loss progressively increased after blast exposure reaching an average loss of 32% in the control group and 10% in the treated group at 21 days. These findings provide the first evidence that a combination of antioxidants, HPN-07 and NAC, can both enhance TTS recovery and prevent PTS by reducing damage to the mechanical and neural components of the auditory system when administered shortly after blast exposure.
Depolarization redistributes synaptic membrane and creates a gradient of vesicles on the synaptic body at a ribbon synapse
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We used electron tomography of frog saccular hair cells to reconstruct presynaptic ultrastructure at synapses specialized for sustained transmitter release. Synaptic vesicles at inhibited synapses were abundant in the cytoplasm and covered the synaptic body at high density. Continuous maximal stimulation depleted 73% of the vesicles within 800 nm of the synapse, with a concomitant increase in surface area of intracellular cisterns and plasmalemmal infoldings. Docked vesicles were depleted 60%–80% regardless of their distance from the active zone. Vesicles on the synaptic body were depleted primarily in the hemisphere facing the plasmalemma, creating a gradient of vesicles on its surface. We conclude that formation of new synaptic vesicles from cisterns is rate limiting in the vesicle cycle.
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1999, Brain Research
Intense sound exposure to the chick ear produces cochlear damage and losses in auditory function. At twelve days post exposure there is considerable structural repair, although a defect on the sensory epithelium remains in the form of an incompletely healed `patch' lesion. Auditory function significantly recovers 12 days after the exposure, but it, too, is incomplete. In this paper we describe the relationship between stimulus intensity and cochlear nerve discharge rate (the rate–intensity function) in two groups of chicks. One is exposed to damaging sound levels but allowed 12 days to recover, while the other is a group of non-exposed and age-matched control animals. Three different types of rate–intensity functions were identified; saturating, sloping, and straight. The percentage of saturating and sloping functions was compared across all characteristic frequencies in both groups of animals. A significant change was observed in the distribution of these types for recovered units with characteristic frequencies within the region of the patch lesion. In addition, the rate–intensity functions of these units exhibited a steeper slope and a higher maximum response. The distribution of rate–intensity function types and their slope and maximum responses, for units with characteristic frequencies outside of the patch lesion, was similar to those found in control ears. The changes in the cochlear nerve response in exposed chicks may be due to alterations in cochlear mechanics, hair cell or synaptic membrane properties, hair cell innervation, or the loss of a tonic suppression of afferent activity exerted by the damaged short hair cells.

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Afferent synaptic changes in auditory hair cells during noise-induced temporary threshold shift

Abstract

Brain. Res.

Hear. Res.

Hear. Res.

Hear. Res.

Hear. Res.

Hear. Res.

Exp. Neurol.

Brain Res.

Hear. Res.

Hear. Res.

Hear. Res.

Hear. Res.

Brain Res.

Neuroscience

Neuroscience

A study of the structure of the papilla neglecta in the lizard, Anolis carolinsis

Anat. Rec.

Stimulation-induced depletion of vesicles, fatigue of transmission, and recovery processes at a vertebrate central synapse

Ultrastructure of synapses in the lateral line canal organ

Acta Otolaryngol. (Stock.)

Connections between stereocilia in auditory hair cells of the alligator lizard

Hear. Res.

Effets de la section du nerf lateral sur le jonctions sensorineurals des ampoules de Lorenzini de la torpille, Torpedo marmorata

J. Micr.

Electrophysiological and morphological correlates of TTS in chinchilla

Receptor synapses without synaptic ribbons in the cochlea of the cat

Frequency selectivity of hair cells and nerve fibers in the alligator lizard cochlea

J. Physiol.

Morphology of the normal and the acoustically damaged cochlea

Scanning Electron Microsc.

On a possible hair cell turn-over in the inner ear of the caecilian Icthyophis glutinosus (Amphibia: Gymnophiona)

Acta Zool.

Sensitive period to acoustic trauma in the rat pup cochlea

Acta Otolaryngol.

Acute and chronic effects of acoustic trauma: cochlear pathology and auditory nerve and pathophysiology

Quantitative studies of auditory hair cells and nerves in lizards

J. Comp. Neurol.

Heterotopic synaptic bodies in the auditory hair cells of adult lizards

Anat. Rec.