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      Effects of noise exposure on young adults with normal audiograms II: Behavioral measures

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          Abstract

          An estimate of lifetime noise exposure was used as the primary predictor of performance on a range of behavioral tasks: frequency and intensity difference limens, amplitude modulation detection, interaural phase discrimination, the digit triplet speech test, the co-ordinate response speech measure, an auditory localization task, a musical consonance task and a subjective report of hearing ability. One hundred and thirty-eight participants (81 females) aged 18–36 years were tested, with a wide range of self-reported noise exposure. All had normal pure-tone audiograms up to 8 kHz. It was predicted that increased lifetime noise exposure, which we assume to be concordant with noise-induced cochlear synaptopathy, would elevate behavioral thresholds, in particular for stimuli with high levels in a high spectral region. However, the results showed little effect of noise exposure on performance. There were a number of weak relations with noise exposure across the test battery, although many of these were in the opposite direction to the predictions, and none were statistically significant after correction for multiple comparisons. There were also no strong correlations between electrophysiological measures of synaptopathy published previously and the behavioral measures reported here. Consistent with our previous electrophysiological results, the present results provide no evidence that noise exposure is related to significant perceptual deficits in young listeners with normal audiometric hearing. It is possible that the effects of noise-induced cochlear synaptopathy are only measurable in humans with extreme noise exposures, and that these effects always co-occur with a loss of audiometric sensitivity.

          Highlights

          • •

            Large study on the effects of lifetime noise exposure in normal-hearing young adults.

          • •

            Performance on a range of behavioral tasks unrelated to noise exposure history.

          • •

            Effects of cochlear synaptopathy not evident in young audiometrically normal cohort.

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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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            Cochlear synaptopathy in acquired sensorineural hearing loss: Manifestations and mechanisms.

            M. Liberman, Sharon G Kujawa (2017)
            Common causes of hearing loss in humans - exposure to loud noise or ototoxic drugs and aging - often damage sensory hair cells, reflected as elevated thresholds on the clinical audiogram. Recent studies in animal models suggest, however, that well before this overt hearing loss can be seen, a more insidious, but likely more common, process is taking place that permanently interrupts synaptic communication between sensory inner hair cells and subsets of cochlear nerve fibers. The silencing of affected neurons alters auditory information processing, whether accompanied by threshold elevations or not, and is a likely contributor to a variety of perceptual abnormalities, including speech-in-noise difficulties, tinnitus and hyperacusis. Work described here will review structural and functional manifestations of this cochlear synaptopathy and will consider possible mechanisms underlying its appearance and progression in ears with and without traditional 'hearing loss' arising from several common causes in humans.
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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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                Author and article information

                Contributors
                Garreth Prendergast
                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 December 2017
                Publication date (Print): December 2017
                Volume: 356
                Pages: 74-86
                Affiliations
                [a ]Manchester Centre for Audiology and Deafness, University of Manchester, Manchester Academic Health Science Centre, M13 9PL, UK
                [b ]NIHR Manchester Biomedical Research Centre, Central Manchester University Hospitals NHS Foundation Trust, Manchester Academic Health Science Centre, Manchester, M13 9WL, UK
                [c ]Sir Peter Mansfield Imaging Centre, School of Physics and Astronomy, University of Nottingham Nottingham, NG7 2RD, UK
                [d ]National Institute for Health Research (NIHR) Nottingham Biomedical Research Centre, Nottingham, NG1 5DU, UK
                [e ]Otology and Hearing Group, Division of Clinical Neuroscience, School of Medicine, University of Nottingham, Nottingham, NG7 2UH, UK
                [f ]Department of Speech, Language, & Hearing Sciences and Biomedical Engineering, Purdue University, West Lafayette, IN, 47907, USA
                [g ]Department of Psychology, Lancaster University, Lancaster, LA1 4YF, UK
                Author notes
                Article
                Publisher ID: S0378-5955(17)30325-8
                DOI: 10.1016/j.heares.2017.10.007
                PMC ID: 5714059
                PubMed ID: 29126651
                SO-VID: 42494d80-6484-4841-913c-019ba54dc279
                Copyright © © 2017 The Authors
                License:

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

                History
                Date received : 10 July 2017
                Date revision received : 17 October 2017
                Date accepted : 23 October 2017
                Categories
                Subject: Article

                ScienceOpen disciplines: Audiology
                Keywords: cochlear synaptopathy,hidden hearing loss,noise-induced hearing loss,speech-in-noise,psychophysics
                Data availability:
                ScienceOpen disciplines: Audiology
                Keywords: cochlear synaptopathy, hidden hearing loss, noise-induced hearing loss, speech-in-noise, psychophysics

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