Tinnitus with a normal audiogram: Relation to noise exposure but no evidence for cochlear synaptopathy

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Abstract

In rodents, exposure to high-level noise can destroy synapses between inner hair cells and auditory nerve fibers, without causing hair cell loss or permanent threshold elevation. Such “cochlear synaptopathy” is associated with amplitude reductions in wave I of the auditory brainstem response (ABR) at moderate-to-high sound levels. Similar ABR results have been reported in humans with tinnitus and normal audiometric thresholds, leading to the suggestion that tinnitus in these cases might be a consequence of synaptopathy. However, the ABR is an indirect measure of synaptopathy and it is unclear whether the results in humans reflect the same mechanisms demonstrated in rodents. Measures of noise exposure were not obtained in the human studies, and high frequency audiometric loss may have impacted ABR amplitudes. To clarify the role of cochlear synaptopathy in tinnitus with a normal audiogram, we recorded ABRs, envelope following responses (EFRs), and noise exposure histories in young adults with tinnitus and matched controls. Tinnitus was associated with significantly greater lifetime noise exposure, despite close matching for age, sex, and audiometric thresholds up to 14 kHz. However, tinnitus was not associated with reduced ABR wave I amplitude, nor with significant effects on EFR measures of synaptopathy. These electrophysiological measures were also uncorrelated with lifetime noise exposure, providing no evidence of noise-induced synaptopathy in this cohort, despite a wide range of exposures. In young adults with normal audiograms, tinnitus may be related not to cochlear synaptopathy but to other effects of noise exposure.

Highlights

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Tinnitus participants matched with controls for age, sex, & audiogram up to 14 kHz.
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Tinnitus participants more noise exposed, despite close audiometric matching.
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No ABR or EFR evidence for cochlear synaptopathy in tinnitus participants.
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No association between ABR or EFR measures and lifetime noise exposure.

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Most cited references 44

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Noise-induced cochlear neuropathy is selective for fibers with low spontaneous rates.

Adam C Furman, Sharon G Kujawa, M. Liberman (2013)

Acoustic overexposure can cause a permanent loss of auditory nerve fibers without destroying cochlear sensory cells, despite complete recovery of cochlear thresholds (Kujawa and Liberman 2009), as measured by gross neural potentials such as the auditory brainstem response (ABR). To address this nominal paradox, we recorded responses from single auditory nerve fibers in guinea pigs exposed to this type of neuropathic noise (4- to 8-kHz octave band at 106 dB SPL for 2 h). Two weeks postexposure, ABR thresholds had recovered to normal, while suprathreshold ABR amplitudes were reduced. Both thresholds and amplitudes of distortion-product otoacoustic emissions fully recovered, suggesting recovery of hair cell function. Loss of up to 30% of auditory-nerve synapses on inner hair cells was confirmed by confocal analysis of the cochlear sensory epithelium immunostained for pre- and postsynaptic markers. In single fiber recordings, at 2 wk postexposure, frequency tuning, dynamic range, postonset adaptation, first-spike latency and its variance, and other basic properties of auditory nerve response were all completely normal in the remaining fibers. The only physiological abnormality was a change in population statistics suggesting a selective loss of fibers with low- and medium-spontaneous rates. Selective loss of these high-threshold fibers would explain how ABR thresholds can recover despite such significant noise-induced neuropathy. A selective loss of high-threshold fibers may contribute to the problems of hearing in noisy environments that characterize the aging auditory system.

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Toward a Differential Diagnosis of Hidden Hearing Loss in Humans

M. Liberman, Michael Epstein, Sandra Cleveland … (2016)

Recent work suggests that hair cells are not the most vulnerable elements in the inner ear; rather, it is the synapses between hair cells and cochlear nerve terminals that degenerate first in the aging or noise-exposed ear. This primary neural degeneration does not affect hearing thresholds, but likely contributes to problems understanding speech in difficult listening environments, and may be important in the generation of tinnitus and/or hyperacusis. To look for signs of cochlear synaptopathy in humans, we recruited college students and divided them into low-risk and high-risk groups based on self-report of noise exposure and use of hearing protection. Cochlear function was assessed by otoacoustic emissions and click-evoked electrocochleography; hearing was assessed by behavioral audiometry and word recognition with or without noise or time compression and reverberation. Both groups had normal thresholds at standard audiometric frequencies, however, the high-risk group showed significant threshold elevation at high frequencies (10–16 kHz), consistent with early stages of noise damage. Electrocochleography showed a significant difference in the ratio between the waveform peaks generated by hair cells (Summating Potential; SP) vs. cochlear neurons (Action Potential; AP), i.e. the SP/AP ratio, consistent with selective neural loss. The high-risk group also showed significantly poorer performance on word recognition in noise or with time compression and reverberation, and reported heightened reactions to sound consistent with hyperacusis. These results suggest that the SP/AP ratio may be useful in the diagnosis of “hidden hearing loss” and that, as suggested by animal models, the noise-induced loss of cochlear nerve synapses leads to deficits in hearing abilities in difficult listening situations, despite the presence of normal thresholds at standard audiometric frequencies.

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Cochlear neuropathy in human presbycusis: Confocal analysis of hidden hearing loss in post-mortem tissue.

Lucas Viana, Jennifer O'Malley, Barbara J Burgess … (2015)

Recent animal work has suggested that cochlear synapses are more vulnerable than hair cells in both noise-induced and age-related hearing loss. This synaptopathy is invisible in conventional histopathological analysis, because cochlear nerve cell bodies in the spiral ganglion survive for years, and synaptic analysis requires special immunostaining or serial-section electron microscopy. Here, we show that the same quadruple-immunostaining protocols that allow synaptic counts, hair cell counts, neuronal counts and differentiation of afferent and efferent fibers in mouse can be applied to human temporal bones, when harvested within 9 h post-mortem and prepared as dissected whole mounts of the sensory epithelium and osseous spiral lamina. Quantitative analysis of five "normal" ears, aged 54-89 yrs, without any history of otologic disease, suggests that cochlear synaptopathy and the degeneration of cochlear nerve peripheral axons, despite a near-normal hair cell population, may be an important component of human presbycusis. Although primary cochlear nerve degeneration is not expected to affect audiometric thresholds, it may be key to problems with hearing in noise that are characteristic of declining hearing abilities in the aging ear.

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Author and article information

Contributors

Hannah Guest

Journal

Journal ID (nlm-ta): Hear Res

Journal ID (iso-abbrev): Hear. Res

Title: Hearing Research

Publisher: Elsevier/North-Holland Biomedical Press

ISSN (Print): 0378-5955

ISSN (Electronic): 1878-5891

Publication date PMC-release: 1 February 2017

Publication date (Print): February 2017

Volume: 344

Pages: 265-274

Affiliations

[a ]Manchester Centre for Audiology and Deafness, University of Manchester, Manchester Academic Health Science Centre, UK

[b ]Audiology Department, James Cook University Hospital, South Tees Hospitals NHS Foundation Trust, Middlesbrough, UK

[c ]Central Manchester University Hospitals NHS Foundation Trust, Manchester, UK

[d ]Department of Psychology, Lancaster University, Lancaster, UK

Author notes

[∗ ]Corresponding author. Manchester Centre for Audiology and Deafness, HCDH Office, Ellen Wilkinson Building, University of Manchester, Oxford Road, Manchester M13 9PL, UK.Manchester Centre for Audiology and DeafnessUniversity of ManchesterHCDH OfficeEllen Wilkinson BuildingOxford RoadManchesterM13 9PLUK hannah.guest@ 123456manchester.ac.uk

Article

Publisher ID: S0378-5955(16)30354-9

DOI: 10.1016/j.heares.2016.12.002

PMC ID: 5256478

PubMed ID: 27964937

SO-VID: 0318cb96-3ebf-49a3-82c5-8945e4b396fa

License:

This is an open access article under the CC BY license (http://creativecommons.org/licenses/by/4.0/).

History

Date received : 13 August 2016

Date revision received : 6 December 2016

Date accepted : 8 December 2016

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Tinnitus with a normal audiogram: Relation to noise exposure but no evidence for cochlear synaptopathy

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Abstract

Highlights

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Hearing Loss and Restoration

Most cited references 44

Noise-induced cochlear neuropathy is selective for fibers with low spontaneous rates.

Toward a Differential Diagnosis of Hidden Hearing Loss in Humans

Cochlear neuropathy in human presbycusis: Confocal analysis of hidden hearing loss in post-mortem tissue.

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