Abstract
Auditory function declines with age, as evidenced by communication difficulties in challenging listening environments for older adults. Declining auditory function may arise, in part, from an age-related loss and/or inactivity of low-spontaneous-rate (SR) auditory nerve (AN) fibers, a subgroup of neurons important for suprathreshold processing. Compared to high-SR fibers, low-SR fibers take longer to recover from prior stimulation. Taking advantage of this difference, the forward-masked recovery function paradigm estimates the relative proportions of low- and high-SR fibers in the AN by quantifying the time needed for AN responses to recover from prior stimulation (ΔTrecovery). Due to the slower recovery of low-SR fibers, ANs that need more time to fully recover (longer ΔTrecovery) are estimated to have a larger proportion of low-SR fibers than ANs that need less time (shorter ΔTrecovery). To test the hypothesis that low-SR fiber activity is reduced in older humans, the current study assessed recovery functions in 32 older and 16 younger adults using the compound action potential. Results show that ΔTrecovery is shorter for older adults than for younger adults, consistent with a theorized age-related loss and/or inactivity of low-SR fibers. ΔTrecovery did not differ between individuals with and without a prior history of noise exposure as assessed by self-report. This study is the first to successfully assess forward-masked recovery functions in both younger and older adults and provides important insights into the structural and functional changes occurring in the AN with increasing age.
Similar content being viewed by others
References
ANSI (2018) Specification for Audiometers. American National Standards Institute
Bharadwaj HM, Masud S, Mehraei G et al (2015) Individual differences reveal correlates of hidden hearing deficits. J Neurosci 35:2161–2172. https://doi.org/10.1523/JNEUROSCI.3915-14.2015
Bourien J, Tang Y, Batrel C et al (2014) Contribution of auditory nerve fibres to compound action potential of the auditory nerve. J Neurophysiol 112:1025–1039. https://doi.org/10.1152/jn.00738.2013
Bramhall NF, Beach EF, Epp B et al (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
Bramhall NF, Konrad-Martin D, McMillan GP, Griest SE (2017) Auditory brainstem response altered in humans with noise exposure despite normal outer hair cell function. Ear Hear 38:1–27. https://doi.org/10.1097/AUD.0000000000000370.Auditory
Brown DJ, Patuzzi RB (2010) Evidence that the compound action potential (CAP) from the auditory nerve is a stationary potential generated across dura mater. Hear Res 267:12–26. https://doi.org/10.1016/j.heares.2010.03.091
Carney LH (2018) Supra-threshold hearing and fluctuation profiles: implications for sensorineural and hidden hearing loss. J Assoc Res Otolaryngol 1–22. https://doi.org/10.1007/s10162-018-0669-5
Delorme A, Makeig S (2004) EEGLAB: an open source toolbox for analysis of single-trial EEG dynamics including independent component analysis. J Neurosci Methods 134:9–21. https://doi.org/10.1016/j.jneumeth.2003.10.009
Dubno JR, Dirks DD, Morgan DE (1984) Effects of age and mild hearing loss on speech recognition in noise. J Acoust Soc Am 76:87–96
Dubno JR, Eckert MA, Lee FS et al (2013) Classifying human audiometric phenotypes of age-related hearing loss from animal models. J Assoc Res Otolaryngol 14:687–701. https://doi.org/10.1007/s10162-013-0396-x
Evans EF, Palmer AR (1980) Relationship between the dynamic range of cochlear nerve fibres and their spontaneous activity. Exp Brain Res 40:115–118. https://doi.org/10.1007/BF00236671
Fernandez KA, Guo D, Micucci S et al (2020) Noise-induced cochlear synaptopathy with and without sensory cell loss. Neuroscience 427:43–57. https://doi.org/10.1016/j.neuroscience.2019.11.051
Fernandez KA, Jeffers PWC, Lall K et al (2015) Aging after noise exposure: acceleration of cochlear synaptopathy in “recovered” ears. J Neurosci 35:7509–7520. https://doi.org/10.1523/JNEUROSCI.5138-14.2015
Fulbright ANC, Le Prell CG, Griffiths SK, 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
Furman AC, Kujawa SG, Liberman MC (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
Grant KJ, Mepani AM, Wu P et al (2020) Electrophysiological markers of cochlear function correlate with hearing-innoise performance among audiometrically normal subjects. J Neurophysiol 124:418–431. https://doi.org/10.1152/jn.00016.2020
Grinn SK, Wiseman KB, Baker JA, Le Prell CG (2017) Hidden hearing loss? No effect of common recreational noise exposure on cochlear nerve response amplitude in humans. Front Neurosci 11:465
Grose JH, Buss E, Hall JW (2017) Loud music exposure and cochlear synaptopathy in young adults: isolated auditory brainstem response effects but no perceptual consequences. Trends Hear 21. https://doi.org/10.1177/2331216517737417
Guest H, Munro KJ, Prendergast G et al (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
Guest H, Munro KJ, Prendergast G et al (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
Harris KC, Vaden KI, McClaskey CM et al (2018) Complementary metrics of human auditory nerve function derived from compound action potentials. J Neurophysiol 119:1019–1028. https://doi.org/10.1152/jn.00638.2017
Hellstrom LI, Schmiedt RA (1990) Compound action potential input/output functions in young and quiet-aged gerbils. Hear Res 50:163–174. https://doi.org/10.1016/0378-5955(90)90042-N
Humes LE (2008) Aging and Speech Communication ASHA Lead 13:10–33. https://doi.org/10.1044/leader.ftr1.13052008.10
IBM Corp (2017) IBM SPSS Statistics for Windows, Version 25.0
Jesteadt W, Bacon SP, Lehmanb JR (1982) Forward masking as a function of frequency, masker level, and signal delay. J Acoust Soc Am 71:950–962. https://doi.org/10.1121/1.387576
Johannesen PT, Buzo BC, Lopez-Poveda EA (2019) Evidence for age-related cochlear synaptopathy in humans unconnected to speech-in-noise intelligibility deficits. Hear Res 374:35–48. https://doi.org/10.1016/j.heares.2019.01.017
Kamerer AM, Kopun JG, Fultz SE et al (2019) Reliability of measures intended to assess threshold-independent hearing disorders. Ear Hear 40:1267–1279. https://doi.org/10.1097/AUD.0000000000000711
Kiang NY, Watanabe T, Thomas EC, Clark LF (1965) Discharge patterns of single fibers in the cat’s auditory nerve. MIT Press, Cambridge MA
Konrad-Martin D, Dille MF, McMillan GP et al (2012) Age-related changes in the auditory brainstem response. J Am Acad Audiol 23:18–35. https://doi.org/10.3766/jaaa.23.1.3
Kujawa SG, Liberman MC (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
Kujawa SG, Liberman MC (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
Lang H, Jyothi V, Smythe NM et al (2010) Chronic reduction of endocochlear potential reduces auditory nerve activity: further confirmation of an animal model of metabolic presbyacusis. J Assoc Res Otolaryngol 11:419–434. https://doi.org/10.1007/s10162-010-0214-7
Lang H, Schulte BA, Schmiedt RA (2002) Endocochlear potentials and compound action potential recovery: functions in the C57BL/6J mouse. Hear Res 172:118–126. https://doi.org/10.1016/S0378-5955(02)00552-X
Liberman MC (1978) Auditory-nerve response from cats raised in a low-noise chamber. J Acoust Soc Am 63:442–455. https://doi.org/10.1121/1.381736
Liberman MC, Epstein MJ, Cleveland SS et al (2016) Toward a differential diagnosis of hidden hearing loss in humans. PLoS One 11:1–15. https://doi.org/10.1371/journal.pone.0162726
Lopez-Calderon J, Luck SJ (2014) ERPLAB: an open-source toolbox for the analysis of event-related potentials. Front Hum Neurosci 8:1–14. https://doi.org/10.3389/fnhum.2014.00213
Makary CA, Shin J, Kujawa SG et al (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
McClaskey CM, Dias JW, Dubno JR, Harris KC (2018) Reliability of measures of N1 peak amplitude of the compound action potential in younger and older adults. J Speech Lang Hear Res 61:2422–2430. https://doi.org/10.1044/2018_JSLHR-H-18-0097
Mehraei G, Hickox AE, Bharadwaj HM et al (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
Mepani AM, Kirk SA, Hancock KE et al (2020) Middle ear muscle reflex and word recognition in “normal-Hearing” adults: evidence for cochlear synaptopathy? Ear Hear 25–38. https://doi.org/10.1097/AUD.0000000000000804
Muggeo VMR (2016) Testing with a nuisance parameter present only under the alternative: a score-based approach with application to segmented modelling. J Stat Comput Simul 86:3059–3067. https://doi.org/10.1080/00949655.2016.1149855
Muggeo VMR (2019) segmented: regression models with break-points / change-points estimation. R package version 0.5–1.1
Murnane OD, Prieve BA, Relkin EM (1998) Recovery of the human compound action potential following prior stimulation. Hear Res 124:182–189. https://doi.org/10.1016/S0378-5955(98)00136-1
Pinheiro J, Bates D, DebRoy S et al (2020) nlme: linear and nonlinear mixed effects models. R package version 3:1–153. https://CRAN.R-project.org/package=nlme
Prendergast G, Couth S, Millman RE et al (2019) Effects of age and noise exposure on proxy measures of cochlear synaptopathy. Trends Hear 23:1–16. https://doi.org/10.1177/2331216519877301
Prendergast G, Guest H, Munro KJ et al (2017) 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
Prendergast G, Tu W, Guest H et al (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
R Core Team (2020) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. https://www.R-project.org
Relkin EM, Doucet JR (1991) Recovery from prior stimulation. I: relationship to spontaneous firing rates of primary auditory neurons. Hear Res 55:215–222. https://doi.org/10.1016/0378-5955(91)90106-J
Relkin EM, Doucet JR, Sterns A (1995) Recovery of the compound action potential following prior stimulation: evidence for a slow component that reflects recovery of low spontaneous-rate auditory neurons. Hear Res 83:183–189. https://doi.org/10.1016/0378-5955(95)00004-N
Ridley CL, Kopun JG, Neely ST et al (2018) Using thresholds in noise to identify hidden hearing loss in humans. Ear Hear 39:829–844. https://doi.org/10.1097/AUD.0000000000000543
Ryugo DK (2008) Projections of low spontaneous rate, high threshold auditory nerve fibers to the small cell cap of the cochlear nucleus in cats. Neuroscience 154:114–126. https://doi.org/10.1016/j.neuroscience.2007.10.052
Schaette R, McAlpine D (2011) Tinnitus with a normal adiogram: physiological evidence for hidden hearing loss and computational model. J Neurosci 31:13452–13457. https://doi.org/10.1523/JNEUROSCI.2156-11.2011
Schmiedt RA (1989) Spontaneous rates, thresholds and tuning of auditory-nerve fibers in the gerbil: comparisons to cat data. Hear Res 42:23–35. https://doi.org/10.1016/0378-5955(89)90115-9
Schmiedt RA, Mills JH, Boettcher FA (1996) Age-related loss of activity of auditory-nerve fibers. J Neurophysiol 76:2799–2803
Schulte BA, Schmiedt RA (1992) Lateral wall Na, K-ATPase and endocochlear potentials decline with age in quiet-reared gerbils. Hear Res 61:35–46. https://doi.org/10.1016/0378-5955(92)90034-K
Skoe E, 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
Stamper GC, Johnson TA (2015a) Auditory function in normal-hearing, noise-exposed human ears. Ear Hear 36:172–184. https://doi.org/10.1097/AUD.0000000000000107
Stamper GC, Johnson TA (2015b) Letter to the editor: examination of potential sex influences in Stamper, G. C., & 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
Suthakar K, Ryugo DK (2016) Descending projections from the inferior colliculus to medial olivocochlear efferents: mice with normal hearing, early onset hearing loss, and congenital deafness. Hear Res 343:34–39. https://doi.org/10.1016/j.heares.2016.06.014
Taberner AM, Liberman MC (2005) Response properties of single auditory nerve fibers in the mouse. J Neurophysiol 93:557–569. https://doi.org/10.1152/jn.00574.2004
Tanner D, Norton JJS, Morgan-Short K, Luck SJ (2016) On high-pass filter artifacts (they’re real) and baseline correction (it’s a good idea) in ERP/ERMF analysis. J Neurosci Methods 266:166–170. https://doi.org/10.1016/j.jneumeth.2016.01.002
Valderrama JT, Beach EF, Yeend I et al (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
Viana LM, O’Malley JT, Burgess BJ et al (2015) Cochlear neuropathy in human presbycusis: confocal analysis of hidden hearing loss in post-mortem tissue. Hear Res 327:78–88. https://doi.org/10.1016/j.heares.2015.04.014
Wu P, O’Malley JT, de Gruttola V, Liberman MC (2020) Age-related hearing loss is dominated by damage to inner ear sensory cells, not the cellular battery that powers them. J Neurosci 40:6357–6366. https://doi.org/10.1523/JNEUROSCI.0937-20.2020
Zeng F-G, Shannon RV (1995) Possible origins of the non-monotonic intensity discrimination function in forward masking. Hear Res 82:216–224. https://doi.org/10.1016/0378-5955(94)00179-T
Zeng F-G, Turner CW (1992) Intensity discrimination in forward masking. J Acoust Soc Am 92:782–787. https://doi.org/10.1121/1.403947
Zeng F-G, Turner CW, Relkin EM (1991) Recovery from prior stimulation II: effects upon intensity discrimination. Hear Res 55:223–230. https://doi.org/10.1016/0378-5955(91)90107-K
Acknowledgements
We thank the participants of our study. We also thank Lilyana Kerouac and Brendan J. Balken for their assistance with data collection.
Funding
This work was supported (in part) by grants from the National Institute on Deafness and Other Communication Disorders (NIDCD) and the National Institutes of Health (NIH), R01 DC 014467, R01 DC 017619, R01 DC 000184, P50 DC 000422, and T32 DC 014435. The project also received support from the South Carolina Clinical and Translational Research (SCTR) Institute with an academic home at the Medical University of South Carolina, NIH/NCRR Grant Number UL1 RR 029882. This investigation was conducted in a facility constructed with support from Research Facilities Improvement Program Grant Number C06 RR 014516 from the National Center for Research Resources, NIH.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of Interest
The authors declare no competing interests.
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
About this article
Cite this article
McClaskey, C.M., Dias, J.W., Schmiedt, R.A. et al. Evidence for Loss of Activity in Low-Spontaneous-Rate Auditory Nerve Fibers of Older Adults. JARO 23, 273–284 (2022). https://doi.org/10.1007/s10162-021-00827-x
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10162-021-00827-x