Abstract
In animal models, prolonged exposure (2 h) to high-level noise causes an irreparable damage to the synapses between the inner hair cells and auditory nerve fibers within the cochlea. Nevertheless, this injury does not necessarily alter the hearing threshold. Similar findings have been observed as part of typical aging in animals. This type of cochlear synaptopathy, popularly called “hidden hearing loss,” has been a significant issue in neuroscience research and clinical audiology scientists. The results obtained in different investigations are inconclusive in their diagnosis and suggest new strategies for both prognosis and treatment of cochlear synaptopathy. Here we review the major physiological findings regarding cochlear synaptopathy in animals and humans and discuss mathematical models. We also analyze the potential impact of these results on clinical practice and therapeutic options.
Funding source: Universidad de Chile
Award Identifier / Grant number: U-inicia 10/16
Author contribution: All the authors have accepted responsibility for the entire content of this submitted manuscript and approved submission.CA and EA wrote the paper; EA interacted with reviewers.
Research funding: Work supported by a grant of the University of Chile (UI-10/16) to EA.
Conflict of interest statement: The authors declare no conflicts of interest regarding this article.
References
Bakay, W.M.H., Anderson, L.A., Garcia-Lazaro, J.A., McAlpine, D., and Schaette, R. (2018). Hidden hearing loss selectively impairs neural adaptation to loud sound environments. Nat. Commun. 9: 1–11, https://doi.org/10.1038/s41467-018-06777-y.Search in Google Scholar PubMed PubMed Central
Bharadwaj, H.M., Verhulst, S., Shaheen, L., Charles Liberman, M., and Shinn-Cunningham, B.G. (2014). Cochlear neuropathy and the coding of supra-threshold sound. Front. Syst. Neurosci. 8: 26, https://doi.org/10.3389/fnsys.2014.00026.Search in Google Scholar PubMed PubMed Central
Bharadwaj, H.M., Masud, S., Mehraei, G., Verhulst, S., and Shinn-Cunningham, B.G. (2015). Individual differences reveal correlates of hidden hearing deficits. J. Neurosci. 35: 2161–2172, https://doi.org/10.1523/jneurosci.3915-14.2015.Search in Google Scholar
Bramhall, N.F., Konrad-Martin, D., McMillan, G.P., and Griest, S.E. (2017). Auditory brainstem response altered in humans with noise exposure despite normal outer hair cell function. Ear Hear. 38: e1–e12, https://doi.org/10.1097/aud.0000000000000370.Search in Google Scholar
Bramhall, N., Beach, E.F., Epp, B., Le Prell, C.G., Lopez-Poveda, E.A., Plack, C.J., Schaette, R., Verhulst, S., and Canlon, B. (2019). The search for noise-induced cochlear synaptopathy in humans: mission impossible? Hear. Res. 377: 88–103, https://doi.org/10.1016/j.heares.2019.02.016.Search in Google Scholar PubMed
Coffey, E.B.J., Nicol, T., White-Schwoch, T., Chandrasekaran, B., Krizman, J., Skoe, E., Zatorre, R.J., and Kraus, N. (2019). Evolving perspectives on the sources of the frequency-following response. Nat. Commun. 10, https://doi.org/10.1038/s41467-019-13003-w.Search in Google Scholar PubMed PubMed Central
Eggermont, J.J. (2008). The role of sound in adult and developmental auditory cortical plasticity. Ear Hear. 29: 819–829, https://doi.org/10.1097/aud.0b013e3181853030.Search in Google Scholar
Flamme, G.A., Deiters, K.K., Tasko, S.M., and Ahroon, W.A. (2017). Acoustic reflexes are common but not pervasive: evidence from the National Health and Nutrition Examination Survey, 1999–2012. Int. J. Audiol. 56: 52–62, https://doi.org/10.1080/14992027.2016.1257164.Search in Google Scholar PubMed
Fulbright, A.N.C., Le Prell, C.G., Griffiths, S.K., Lobarinas, E., 2017. Effects of recreational noise on threshold and suprathreshold measures of auditory function. Semin. Hear. 38, 298–318. https://doi.org/10.1055/s-0037-1606325.Search in Google Scholar PubMed PubMed Central
Furman, A.C., Kujawa, S.G., and Charles Liberman, M. (2013). Noise-induced cochlear neuropathy is selective for fibers with low spontaneous rates. J. Neurophysiol. 110: 577–586, https://doi.org/10.1152/jn.00164.2013.Search in Google Scholar PubMed PubMed Central
Gorga, M.P., Neely, S.T., Ohlrich, B., Hoover, B., Redner, J., and Peters, J. (1997). From laboratory to clinic: A large scale study of distortion product otoacoustic emissions in ears with normal hearing and ears with hearing loss. Ear Hear. 18: 440–455, https://doi.org/10.1097/00003446-199712000-00003.Search in Google Scholar PubMed
Gourévitch, B., Edeline, J.M., Occelli, F., and Eggermont, J.J. (2014). Is the din really harmless? Long-term effects of non-traumatic noise on the adult auditory system. Nat. Rev. Neurosci. 15: 483–491, https://doi.org/10.1038/nrn3744.Search in Google Scholar PubMed
Grinn, S.K., Wiseman, K.B., Baker, J.A., and Le Prell, C.G. (2017). Hidden hearing loss? No effect of common recreational noise exposure on cochlear nerve response amplitude in humans. Front. Neurosci. 11: 465, https://doi.org/10.3389/fnins.2017.00465.Search in Google Scholar PubMed PubMed Central
Grose, J.H., Buss, E., and Hall, J.W. (2017). Loud music exposure and cochlear synaptopathy in young adults: isolated auditory brainstem response effects but no perceptual consequences. Trends Hear. 21:2331216517737417, https://doi.org/10.1177/2331216517737417.Search in Google Scholar PubMed PubMed Central
Guest, H., Munro, K.J., Prendergast, G., Howe, S., and Plack, C.J. (2017). Tinnitus with a normal audiogram: relation to noise exposure but no evidence for cochlear synaptopathy. Hear. Res. 344: 265–274, https://doi.org/10.1016/j.heares.2016.12.002.Search in Google Scholar PubMed PubMed Central
Guest, H, Munro, KJ, Prendergast, G, Millman, RE, Plack, CJ, 2018. Impaired speech perception in noise with a normal audiogram: no evidence for cochlear synaptopathy and no relation to lifetime noise exposure. Hear. Res. 364, 142–151. https://doi.org/10.1016/j.heares.2018.03.008.Search in Google Scholar PubMed PubMed Central
Hashimoto, K., Hickman, T.T., Suzuki, J., Ji, L., Kohrman, D.C., Corfas, G., and Liberman, M.C. (2019). Protection from noise-induced cochlear synaptopathy by virally mediated overexpression of NT3. Sci. Rep. 9: 1–12, https://doi.org/10.1038/s41598-019-51724-6.Search in Google Scholar PubMed PubMed Central
Hickman, T.T., Smalt, C., Bobrow, J., Quatieri, T., and Liberman, M.C. (2018). Blast-induced cochlear synaptopathy in chinchillas. Sci. Rep. 8: 1–12, https://doi.org/10.1038/s41598-018-28924-7.Search in Google Scholar PubMed PubMed Central
Jewett, D.L. and Williston, J.S. (1971). Auditory-evoked far fields averaged from the scalp of humans. Brain 94: 681–696, https://doi.org/10.1093/brain/94.4.681.Search in Google Scholar PubMed
Kabzińska, D., Korwin-Piotrowska, T., Drechsler, H., Drac, H., Hausmanowa-Petrusewicz, I., and Kochański, A. (2007). Late-onset Charcot-Marie-Tooth type 2 disease with hearing impairment associated with a novel Pro105Thr mutation in theMPZ gene. Am. J. Med. Genet. 143A: 2196–2199.10.1002/ajmg.a.31908Search in Google Scholar PubMed
King, A., Hopkins, K., and Plack, C.J. (2016). Differential group delay of the frequency following response measured vertically and horizontally. J. Assoc. Res. Otolaryngol. 17: 133–143, https://doi.org/10.1007/s10162-016-0556-x.Search in Google Scholar PubMed PubMed Central
Kujawa, S.G. and Liberman, M.C. (2009). Adding insult to injury: cochlear nerve degeneration after “temporary” noise-induced hearing loss. J. Neurosci. 29: 14077–14085, https://doi.org/10.1523/jneurosci.2845-09.2009.Search in Google Scholar PubMed PubMed Central
Kujawa, S.G. and Liberman, M.C. (2015). Synaptopathy in the noise-exposed and aging cochlea: primary neural degeneration in acquired sensorineural hearing loss. Hear. Res. 330: 191–199, https://doi.org/10.1016/j.heares.2015.02.009.Search in Google Scholar PubMed PubMed Central
Kujawa, S.G. and Liberman, M.C. (2019). Translating animal models to human therapeutics in noise-induced and age-related hearing loss. Hear. Res. 377: 44–52, https://doi.org/10.1016/j.heares.2019.03.003.Search in Google Scholar PubMed PubMed Central
Kumar, U.A., Ameenudin, S., Sangamanatha, A.V., 2012. Temporal and speech processing skills in normal hearing individuals exposed to occupational noise. Noise Health 14, 100–105. https://doi.org/10.1007/978-1-4939-2981-8_1.Search in Google Scholar PubMed
Liberman, M.C. (2016). Noise-induced hearing loss: permanent versus temporary threshold shifts and the effects of hair cell versus neuronal degeneration. In: Advances in experimental medicine and biology. Springer New York LLC, pp. 1–7.10.1007/978-1-4939-2981-8_1Search in Google Scholar
Liberman, M.C., Epstein, M.J., Cleveland, S.S., Wang, H., and Maison, S.F. (2016). Toward a differential diagnosis of hidden hearing loss in humans. PloS One 11: e0162726, https://doi.org/10.1371/journal.pone.0162726.Search in Google Scholar PubMed PubMed Central
Lobarinas, E., Salvi, R., and Ding, D. (2013). Insensitivity of the audiogram to carboplatin induced inner hair cell loss in chinchillas. Hear. Res. 302: 113–120, https://doi.org/10.1016/j.heares.2013.03.012.Search in Google Scholar PubMed PubMed Central
Lopez-Poveda, E.A. and Barrios, P. (2013). Perception of stochastically undersampled sound waveforms: a model of auditory deafferentation. Front. Neurosci. 7, https://doi.org/10.3389/fnins.2013.00124.Search in Google Scholar PubMed PubMed Central
Makary, C.A., Shin, J., Kujawa, S.G., Liberman, M.C., and Merchant, S.N. (2011). Age-related primary cochlear neuronal degeneration in human temporal bones. J. Assoc. Res. Otolaryngol. 12: 711–717, https://doi.org/10.1007/s10162-011-0283-2.Search in Google Scholar PubMed PubMed Central
Marsh, J.T., Worden, F.G., and Smith, J.C. (1970). Auditory frequency-following response: neural or artifact? Science 169: 1222–1223, https://doi.org/10.1126/science.169.3951.1222.Search in Google Scholar PubMed
Mehraei, G., Hickox, A.E., Bharadwaj, H.M., Goldberg, H., Verhulst, S., Charles Liberman, M., and Shinn-Cunningham, B.G. (2016). Auditory brainstem response latency in noise as a marker of cochlear synaptopathy. J. Neurosci. 36: 3755–3764, https://doi.org/10.1523/jneurosci.4460-15.2016.Search in Google Scholar PubMed PubMed Central
Nelson, K.R., Gilmore, R.L., and Massey, A. (1988). Acoustic nerve conduction abnormalities in Guillain-Barré syndrome. Neurology 38: 1263–1266, https://doi.org/10.1212/wnl.38.8.1263.Search in Google Scholar PubMed
Oxenham, A.J. (2016). Predicting the perceptual consequences of hidden hearing loss. Trends Hear. 20: 233121651668676, https://doi.org/10.1177/2331216516686768.Search in Google Scholar PubMed PubMed Central
Paul, B.T., Bruce, I.C., and Roberts, L.E. (2017). Evidence that hidden hearing loss underlies amplitude modulation encoding deficits in individuals with and without tinnitus. Hear. Res. 344: 170–182, https://doi.org/10.1016/j.heares.2016.11.010.Search in Google Scholar PubMed
Plack, C.J., Barker, D., and Prendergast, G. (2014). Perceptual consequences of “hidden” hearing loss. Trends Hear. 18, https://doi.org/10.1177/2331216514550621.Search in Google Scholar PubMed PubMed Central
Prendergast, G., Guest, H., Munro, K.J., Kluk, K., Léger, A., Hall, D.A., Heinz, M.G., and Plack, C.J. (2017a). Effects of noise exposure on young adults with normal audiograms I: electrophysiology. Hear. Res. 344: 68–81, https://doi.org/10.1016/j.heares.2016.10.028.Search in Google Scholar PubMed PubMed Central
Prendergast, G., Millman, R.E., Guest, H., Munro, K.J., Kluk, K., Dewey, R.S., Hall, D.A., Heinz, M.G., and Plack, C.J. (2017b) Effects of noise exposure on young adults with normal audiograms II: behavioral measures. Hear. Res. 356: 74–86, https://doi.org/10.1016/j.heares.2017.10.007.Search in Google Scholar PubMed PubMed Central
Prendergast, G., Tu, W., Guest, H., Millman, R.E., Kluk, K., Couth, S., Munro, K.J., and Plack, C.J. (2018). Supra-threshold auditory brainstem response amplitudes in humans: test-retest reliability, electrode montage and noise exposure. Hear. Res. 364: 38–47, https://doi.org/10.1016/j.heares.2018.04.002.Search in Google Scholar PubMed PubMed Central
Reed, N.S., Betz, J., Kendig, N., Korczak, M., and Lin, F.R. (2017). Personal sound amplification products vs a conventional hearing aid for speech understanding in noise. J. Am. Med. Assoc. 318: 89–90, https://doi.org/10.1001/jama.2017.6905.Search in Google Scholar PubMed PubMed Central
Schaette, R. and McAlpine, D. (2011). Tinnitus with a normal audiogram: physiological evidence for hidden hearing loss and computational model. J. Neurosci. 31: 13452–13457, https://doi.org/10.1523/jneurosci.2156-11.2011.Search in Google Scholar PubMed PubMed Central
Sergeyenko, Y., Lall, K., Charles Liberman, M., and Kujawa, S.G. (2013). Age-related cochlear synaptopathy: an early-onset contributor to auditory functional decline. J. Neurosci. 33: 13686–13694, https://doi.org/10.1523/jneurosci.1783-13.2013.Search in Google Scholar PubMed PubMed Central
Shaheen, LA, Valero, MD, Liberman, MC, 2015. Towards a diagnosis of cochlear neuropathy with envelope following responses. JARO - J. Assoc. Res. Otolaryngol. 16, 727–745. https://doi.org/10.1007/s10162-015-0539-3.Search in Google Scholar PubMed PubMed Central
Skoe, E. and Tufts, J. (2018). Evidence of noise-induced subclinical hearing loss using auditory brainstem responses and objective measures of noise exposure in humans. Hear. Res. 361: 80–91, https://doi.org/10.1016/j.heares.2018.01.005.Search in Google Scholar PubMed
Stamper, G.C. and Johnson, T.A. (2015a). Auditory function in normal-hearing, noise-exposed human ears. Ear Hear. 36: 172–184, https://doi.org/10.1097/aud.0000000000000107.Search in Google Scholar
Stamper, G.C. and Johnson, T.A. (2015b). Letter to the editor: Examination of potential sex influences in Stamper, G.C. and Johnson, T.A. (2015). Auditory function in normal-hearing, noise-exposed human ears, Ear Hear. 36: 172–184. Ear Hear. 36: 738–740. https://doi.org/10.1097/AUD.0000000000000228.Search in Google Scholar PubMed PubMed Central
Suzuki, J., Corfas, G., and Liberman, M.C. (2016). Round-window delivery of neurotrophin 3 regenerates cochlear synapses after acoustic overexposure. Sci. Rep. 6: 1–11, https://doi.org/10.1038/srep24907.Search in Google Scholar PubMed PubMed Central
Valderrama, J.T., Beach, E.F., Yeend, I., Sharma, M., Van Dun, B., and Dillon, H. (2018). Effects of lifetime noise exposure on the middle-age human auditory brainstem response, tinnitus and speech-in-noise intelligibility. Hear. Res. 365: 36–48, https://doi.org/10.1016/j.heares.2018.06.003.Search in Google Scholar PubMed
Valero, M.D., Hancock, K.E., and Liberman, M.C. (2016). The middle ear muscle reflex in the diagnosis of cochlear neuropathy. Hear. Res. 332: 29–38, https://doi.org/10.1016/j.heares.2015.11.005.Search in Google Scholar PubMed PubMed Central
Valero, M.D., Burton, J.A., Hauser, S.N., Hackett, T.A., Ramachandran, R., and Liberman, M.C. (2017). Noise-induced cochlear synaptopathy in rhesus monkeys (Macaca mulatta). Hear. Res. 353: 213–223, https://doi.org/10.1016/j.heares.2017.07.003.Search in Google Scholar PubMed PubMed Central
Verhulst, S., Jagadeesh, A., Mauermann, M., and Ernst, F. (2016). Individual differences in auditory brainstem response wave characteristics: relations to different aspects of peripheral hearing loss. Trends Hear. 20: 233121651667218, https://doi.org/10.1177/2331216516672186.Search in Google Scholar PubMed PubMed Central
Wan, G. and Corfas, G. (2017). Transient auditory nerve demyelination as a new mechanism for hidden hearing loss. Nat. Commun. 8: 1–13, https://doi.org/10.1038/ncomms14487.Search in Google Scholar PubMed PubMed Central
Wong, S.J., Abrams, K.S., Amburgey, K.N., Wang, Y., and Henry, K.S. (2019). Effects of selective auditory-nerve damage on the behavioral audiogram and temporal integration in the budgerigar. Hear. Res. 374: 24–34, https://doi.org/10.1016/j.heares.2019.01.019.Search in Google Scholar PubMed PubMed Central
Yeend, I., Beach, E.F., Sharma, M., and Dillon, H. (2017). The effects of noise exposure and musical training on suprathreshold auditory processing and speech perception in noise. Hear. Res. 353: 224–236, https://doi.org/10.1016/j.heares.2017.07.006.Search in Google Scholar PubMed
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