The active process is affected first by intense sound exposure

doi:10.1016/0378-5955(88)90077-9

Hearing Research

Volume 37, Issue 1, December 1988, Pages 53-63

https://doi.org/10.1016/0378-5955(88)90077-9 Get rights and content

Abstract

Evidence exists to suggest that intense sound releases excess neurotransmitter from the inner hair cells. However, it has been previously reported that intense sound affects the cochlear micromechanics by altering the stereocilia. Therefore, we tested the hypothesis that intense sound affects structures involved in transduction before it affects the nerve endings. In order to test this hypothesis, we examined the interaction of intense sound with kynurenate which blocks the action of the neurotransmitter on the afferent nerve endings. Intracochlear perfusion of artificial perilymph containing 5 mM kynurenate did not reduce the effect of intense sound when we compare the results with a control group perfused with artificial perilymph alone. These results show that blockade of afferent transmitter receptors did not reduce the effect of acoustic trauma, and the acoustic trauma used herein affected structures involved in transduction before it affected the postsynaptic structures. We speculate that the active process is affected first during acoustic trauma. This interpretation is consistent with the notion that stereocilia are structures that make up part of the active process.

References (46)

R.P. Bobbin et al.
Kynurenic acid and gamma-d-glutamylaminomethylsulfonic acid suppress the compound action potential of the auditory nerve
Hear. Res.
(1987)
B. Canlon et al.
Pure tone overstimulation changes the micromechanical properties of the inner hair cell stereocilia
Hear. Res.
(1987)
P. Dallos
Neurobiology of cochlear inner and outer hair cells: Intracellular recordings
Hear. Res.
(1986)
H. Davis
An active process in cochlear mechanics
Hear. Res.
(1983)
B. Engstrom et al.
Ultrastructural studies of stereocilia in noise-exposed rabbits
Hear. Res.
(1983)
P.L. Herrling
Pharmacology of the corticocaudate excitatory postsynaptic potential in the cat: Evidence for its mediation by quisqualate or kainate-receptors
Neuroscience
(1985)
B.M. Johnstone et al.
Basilar membrane measurements and the travelling wave
Hear. Res.
(1986)
D.O. Kim
Active and nonlinear cochlear biomechanics and the role of outer-hair-cell subsystem in the mammalian auditory system
Hear. Res.
(1986)
M. Lenoir et al.
Dose-dependent changes in the rat cochlea following aminoglycoside intoxication: II. Histological study
Hear. Res.
(1987)
M.C. Liberman et al.
Single-neuron labeling and chronic cochlear pathology. III. Stereocilia damage and alterations of threshold tuning curves
Hear. Res.
(1984)

S.T. Neely et al.

An active cochlear-model showing sharp tuning and high sensitivity

Hear. Res.

(1983)

J.-L. Puel et al.

Dose-dependent changes in the rat cochlea following aminoglycoside intoxication: I. Physiological study

Hear Res.

(1987)

D. Robertson

Effects of acoustic trauma on stereocilia structure and spiral ganglion cell tuning properties in the guinea pig cochlea

Hear. Res.

(1982)

D. Robertson

Functional significance of dendrite swelling after loud sounds in the guinea pig cochlea

Hear. Res.

(1983)

S.M. Rothman et al.

Excitotoxicity and the NMDA receptor

TINS

(1987)

L.G. Tilney et al.

Changes in the organization of actin filaments in the stereocilia of noise-damaged cochleae

Hear. Res.

(1982)

J.-M. Aran

Electrophysiology of cochlear toxicity

S.E. Barron et al.

Cytochalasin D suppresses sound evoked potentials in guinea-pig cochlea

Hear. Res.

(1987)

H.A. Beagley

Acoustic trauma in the guinea pig

Acta Oto-Laryngol.

(1965)

G.von Békésy

Experiments in Hearing

S.C. Bledsoe

Pharmacology and neurotransmission of sensory transduction in the inner ear

R.P. Bobbin et al.

Action of cholinergic and anticholinergic drugs at the crossed olivocochlear bundle-hair cell junction

Acta Oto-Laryngol.

(1974)

A.R. Cody et al.

Acoustic trauma: Single neuron basis for the ‘half-octave shift’

J. Acoust. Soc. Am.

(1981)

Cited by (46)

Caffeine and ryanodine demonstrate a role for the ryanodine receptor in the organ of Corti
2002, Hearing Research
The hypothesis that the release of Ca²⁺ from ryanodine receptor activated Ca²⁺ stores in vivo can affect the function of the cochlea was tested by examining the effects of caffeine (1–10 mM) and ryanodine (1–333 μM), two drugs that release Ca²⁺ from these intracellular stores. The drugs were infused into the perilymph compartment of the guinea pig cochlea while sound (10 kHz) evoked cochlear potentials and distortion product otoacoustic emissions (DPOAEs; 2f₁−f₂=8 kHz, f₂=12 kHz) were monitored. Caffeine significantly suppressed the compound action potential of the auditory nerve (CAP) at low intensity (56 dB SPL; 3.3 and 10 mM) and high intensity (92 dB SPL; 10 mM), increased N1 latency at high and low intensity (3 and 10 mM) and suppressed low intensity summating potential (SP; 10 mM) without an effect on high intensity SP. Ryanodine significantly suppressed the CAP at low intensity (100 and 333 μM) and at high intensity (333 μM), increased N1 latency at low intensity (33, 100 and 333 μM) and at high intensity (333 μM) and suppressed low intensity SP (100 and 333 μM) and increased high intensity SP (333 μM). The cochlear microphonic (CM) evoked by 10 kHz tone bursts was not affected by caffeine at high or low intensity, and ryanodine had no effect on it at low intensity but decreased it at high intensity (10, 33, 100 and 333 μM). In contrast, caffeine (10 mM) and ryanodine (33 and 100 μM) significantly increased CM evoked by l kHz tone bursts and recorded from the round window. Caffeine (10 mM) and ryanodine (100 μM) reversibly suppressed the cubic DPOAEs evoked by low intensity primaries. Overall, low intensity evoked responses were more sensitive and were suppressed to a greater extent by both drugs. This is consistent with the hypothesis that release of Ca²⁺ from ryanodine receptor Ca²⁺ stores, possibly in outer hair cells and supporting cells, affects the function of the cochlear amplifier.
PPADS, an ATP antagonist, attenuates the effects of a moderately intense sound on cochlear mechanics
2001, Hearing Research
Increasing attention is being given to the role of neurotransmitters and other signaling substances in the damage induced by intense sound to the cochlea. Adenosine triphosphate (ATP) is one example of a putative neurotransmitter that may alter cochlear mechanics during sound exposure. The purpose of the present study was to test the hypothesis that endogenous extracellular ATP has a role in the generation of the changes in cochlear mechanics induced by moderate intense sound exposure. Guinea pigs were exposed to either: (1) a perilymphatic administration of pyridoxal-phosphate-6-azophenyl-2′,4′-disulphonic acid (PPADS, 1 mM), an ATP antagonist; (2) a moderately intense sound (6 kHz tone, 95 dB SPL, 15 min); or (3) a combination of the PPADS and the sound. The effects on the cubic distortion product otoacoustic emissions (DPOAEs; 2f₁−f₂) were monitored using three sets of equal level primaries (f₁=9.25 kHz, f₂=10.8 kHz, 2f₁−f₂=7.7 kHz; f₁=7.2 kHz, f₂=8.4 kHz, 2f₁−f₂=6 kHz; f₁=5.55 kHz, f₂=6.5 kHz, 2f₁−f₂=4.6 kHz). PPADS alone had no effect on the cubic DPOAEs monitored. The intense sound alone suppressed all three cubic DPOAEs. The combination of PPADS with the intense sound induced a suppression of the cubic DPOAEs that was equal to or greater than induced by the intense sound alone at f₂=10.8 kHz but was equal to or less than induced by the intense sound at f₂=8.4 and 6.5 kHz. After washing the PPADS out of the cochlea with artificial perilymph, all three cubic DPOAEs were suppressed less in the PPADS with intense sound treatment group than in the intense sound alone group. The PPADS appeared to provide protection from the intense sound. Results are consistent with the hypothesis that extracellular ATP is involved in the changes in cochlear mechanics induced by moderately intense sound exposure.
An interaction between PPADS, an ATP antagonist, and a moderately intense sound in the cochlea
1999, Hearing Research
In the organ of Corti ionotropic receptors for ATP (ATPRs) on cells that are bathed by perilymph have been suggested to modulate cochlear mechanics. The purpose of the present study was to test the hypothesis that endogenous extracellular ATP acting through ATPRs is involved in modulating cochlear mechanics during moderately intense sound exposure. Guinea pigs were exposed to either: (1) a perilymphatic administration of pyridoxal-phosphate-6-azophenyl-2′,4′-disulfonic acid (PPADS, 1 mM), an ATP antagonist; (2) a moderately intense sound (6.7 kHz tone, 95 dB SPL, 15 min); or (3) a combination of both the PPADS and the sound. The effects on cochlear potentials (cochlear microphonic, CM; negative summating potential, SP; compound action potential of the auditory nerve, CAP; and N₁ latency) evoked by a 10 kHz tone pip were monitored. PPADS alone reduced the CAP and the SP and increased N₁ latency. The intense sound alone reduced the CAP and SP. The combination of PPADS with the intense tone induced reversible effects on cochlear potentials that were greater than induced by either treatment alone. The effect on N₁ latency and low intensity CM was a potentiation since the effect was greater than a simple addition of the effect of either treatment alone. The effects of the combination treatment on CAP, SP and high intensity CM were not different from additive. Results are consistent with the hypothesis that ATPRs in the organ of Corti are involved in modulating cochlear mechanics during moderately intense sound exposure.
Vulnerability of the gerbil cochlea to sound exposure during reversible ischemia
1999, Hearing Research
Cochlear ischemia induces a sensorineural hearing loss, in part through a fast functional impairment of outer hair cellls. Assuming that the cochlea is rendered fragile during ischemia and reperfusion and that stimulation itself can jeopardize its functional recovery, we used a model of reversible selective cochlear ischemia in Mongolian gerbils to establish what type of sound exposure can be deleterious during and immediately after reversible ischemia. Several groups of gerbils were used, with different ischemia durations and levels of sound exposure. Control groups were only exposed to tones at 80 and 90 dB SPL during 30 min, while other groups underwent complete and fully reversible blockage of the labyrinthine artery, during 5.5 or 8 min, and were exposed to 60 or 80 dB SPL tones during 30 min. The amount of ischemia and reperfusion was measured by means of laser Doppler velocimetry, whereas outer hair cells’ function was continuously monitored through distortion-product otoacoustic emissions (DPOAEs). The losses of DPOAE levels after 8 min transient ischemia and 60 dB SPL exposure were as large as those induced by 80 dB SPL exposures combined with 5.5 min ischemia, or 90 dB SPL exposures without ischemia, with a maximum loss around 25–30 dB, half an octave above the stimulus frequency. These results give evidence for an extremely high cochlear vulnerability to low-level sound exposure when associated with reversible ischemia. This vulnerability may have important clinical consequences in patients with cochlear circulatory disturbances.
Exponential onset and recovery of temporary threshold shift after loud sound: Evidence for long-term inactivation of mechano-electrical transduction channels
1998, Hearing Research
The onset and recovery of temporary threshold shift (TTS) in one human subject (the author) has been studied during and after pure-tone overstimulation lasting between minutes and days. Under the conditions of these experiments the time courses appeared reproducible, and thresholds always recovered to normal within 3 days. The onset and recovery followed a multiple-exponential time course, with the time constants for the onset being 6.5 and 800 min, and the recovery time constants being 30, 240 and 800 min. The observed time courses were consistent with data previously reported in humans, and with the view that the threshold elevation was due to an inactivation and reactivation of the stretch-activated channels at the apex of the outer hair cells of the cochlea. The time constants of the multi-exponential onset and recovery do not appear to depend on the duration of the overstimulation, but the exponential coefficients do. A simple kinetic model of the onset and recovery is described (for more detail see Patuzzi (1998)). It is suggested that the rapid recovery in the first 5 min after exposure is due to a short-lived disruption of the synapses between the inner hair cells and the primary afferent neurones. Intermittent exposures were found to produce much less TTS than continuous tones, and this reduction was found to be inconsistent with the Equal Energy Hypothesis, in that the TTS produced by intermittent tones was much less than predicted using the Equal Energy model, and the recovery time course was also different from that expected from a shorter exposure to a continuous tone of equal energy.
Molecular organization of a type of peripheral glutamate synapse: The afferent synapses of hair cells in the inner ear
1998, Progress in Neurobiology
The synapses between sensory cells in the inner ear and the afferent dendrites of ganglion cells are well suited to investigations of fundamental mechanisms of fast synaptic signalling. The presynaptic elements can be isolated for electrophysiological and functional studies while the synapses can be easily recognized in the electron microscope due to their distinct morphological features. This allows for a broader range of correlative functional and structural analyses than can be applied to synapses in the central nervous system (CNS). As in most fast excitatory synapses in the CNS the transmitter in the afferent hair cell synapses appears to be glutamate or a closely related compound. Recent studies have revealed many of the key molecular players at this type of synapse and how they are spatially and functionally coupled. By use of high resolution immunogold cytochemistry it has been shown that AMPA glutamate receptors are specifically expressed in the postsynaptic specialization of afferent hair cell synapses (except at those established by outer hair cells in the organ of Corti) and that their density varies as a function of the distance from the release sites (demonstrated for the afferent contacts of inner hair cells). The glutamate transporter GLAST is localized in supporting cell membranes and concentrated in those membrane domains that face the synaptic regions. Glutamine synthetase and phosphate-activated glutaminase—which are responsible for the interconversion of glutamate and glutamine—are selectively localized in non-neuronal and neuronal elements, respectively. Taken together with quantitative immunogold data on the cellular compartmentation of glutamate and glutamine the above findings suggest that the sensory epithelia in the inner ear sustain a cycling of glutamate carbon skeletons. In this process, the supporting cells may carry out functions analogous to those of glial cells in the CNS. Functional and morphological analyses of the presynaptic membrane indicate that l-type Ca²⁺-channels and Ca²⁺-activated K⁺-channels are colocalized and clustered at the active zone. Influx through the l-type channels triggers synaptic release and their close spatial association with Ca²⁺-activated K⁺-channels appears to be critical for frequency tuning. The focal expression of different Ca²⁺-channels combined with a high intracellular buffering capacity permits several Ca²⁺-signalling pathways to operate in parallel without undue interference. The molecular organization of the afferent hair cell synapsesreflects the functional demand for speed and precision and attests to the ability of the pre- andpostsynaptic elements to target and anchor key proteins at specific membrane domains.

View all citing articles on Scopus

View full text

The active process is affected first by intense sound exposure

Abstract

Hear. Res.

Hear. Res.

Hear. Res.

Hear. Res.

Hear. Res.

Neuroscience

Hear. Res.

Hear. Res.

Hear. Res.

Hear. Res.

Hear. Res.

Hear Res.

Hear. Res.

Hear. Res.

TINS

Hear. Res.

Electrophysiology of cochlear toxicity

Cytochalasin D suppresses sound evoked potentials in guinea-pig cochlea

Hear. Res.

Acoustic trauma in the guinea pig

Acta Oto-Laryngol.

Experiments in Hearing

Pharmacology and neurotransmission of sensory transduction in the inner ear

Action of cholinergic and anticholinergic drugs at the crossed olivocochlear bundle-hair cell junction

Acta Oto-Laryngol.

Acoustic trauma: Single neuron basis for the ‘half-octave shift’

J. Acoust. Soc. Am.