Abstract
Animal models of noise-induced hearing loss (NIHL) show a dramatic mismatch between cochlear characteristic frequency (CF, based on place of innervation) and the dominant response frequency in single auditory-nerve-fiber responses to broadband sounds (i.e., distorted tonotopy, DT). This noise trauma effect is associated with decreased frequency-tuning-curve (FTC) tip-to-tail ratio, which results from decreased tip sensitivity and enhanced tail sensitivity. Notably, DT is more severe for noise trauma than for metabolic (e.g., age-related) losses of comparable degree, suggesting that individual differences in DT may contribute to speech intelligibility differences in patients with similar audiograms. Although DT has implications for many neural-coding theories for real-world sounds, it has primarily been explored in single-neuron studies that are not viable with humans. Thus, there are no noninvasive measures to detect DT. Here, frequency following responses (FFRs) to a conversational speech sentence were recorded in anesthetized male chinchillas with either normal hearing or NIHL. Tonotopic sources of FFR envelope and temporal fine structure (TFS) were evaluated in normal-hearing chinchillas. Results suggest that FFR envelope primarily reflects activity from high-frequency neurons, whereas FFR-TFS receives broad tonotopic contributions. Representation of low- and high-frequency speech power in FFRs was also assessed. FFRs in hearing-impaired animals were dominated by low-frequency stimulus power, consistent with oversensitivity of high-frequency neurons to low-frequency power. These results suggest that DT can be diagnosed noninvasively. A normalized DT metric computed from speech FFRs provides a potential diagnostic tool to test for DT in humans. A sensitive noninvasive DT metric could be used to evaluate perceptual consequences of DT and to optimize hearing-aid amplification strategies to improve tonotopic coding for hearing-impaired listeners.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Aiken SJ, Picton TW (2008) Envelope and spectral frequency-following responses to vowel sounds. Hear Res 245(1):35–47. https://doi.org/10.1016/j.heares.2008.08.004
Ananthakrishnan S, Krishnan A, Bartlett E (2016) Human frequency following response: neural representation of envelope and temporal fine structure in listeners with normal hearing and sensorineural hearing loss. Ear Hear 37(2):e91–e103. https://doi.org/10.1097/AUD.0000000000000247
Babadi B, Brown EN (2014) A review of multitaper spectral analysis. IEEE Trans Biomed Eng 61(5):1555–1564. https://doi.org/10.1109/TBME.2014.2311996
Bharadwaj HM, Verhulst S, Shaheen L, Liberman MC, Shinn-Cunningham BG (2014) Cochlear neuropathy and the coding of supra-threshold sound. Front Syst Neurosci 8. https://doi.org/10.3389/fnsys.2014.00026
Bharadwaj HM, Mai AR, Simpson JM, Choi I, Heinz MG, Shinn-Cunningham BG (2019) Non-invasive assays of cochlear Synaptopathy candidates and considerations. Neuroscience 407:53–66. https://doi.org/10.1016/j.neuroscience.2019.02.031, http://www.sciencedirect.com/science/article/pii/S0306452219301423
Bones O, Plack CJ (2015) Subcortical representation of musical dyads: individual differences and neural generators. Hear Res 323:9–21. https://doi.org/10.1016/j.heares.2015.01.009
Chambers AR, Resnik J, Yuan Y, Whitton JP, Edge AS, Liberman MC, Polley DB (2016) Central gain restores auditory processing following near-complete cochlear denervation. Neuron 89(4):867–879. https://doi.org/10.1016/j.neuron.2015.12.041
Clark JG (1981) Uses and abuses of hearing loss classification. ASHA 23(7):493–500
Dau T (2003) The importance of cochlear processing for the formation of auditory brainstem and frequency following responses. J Acoust Soc Am 113(2):936–950. https://doi.org/10.1121/1.1534833
Dolphin WF, Mountain DC (1993) The envelope following response (EFR) in the Mongolian gerbil to sinusoidally amplitude-modulated signals in the presence of simultaneously gated pure tones. J Acoust Soc Am 94(6):3215–3226. https://doi.org/10.1121/1.407227
Gockel HE, Krugliak A, Plack CJ, Carlyon RP (2015) Specificity of the human frequency following response for carrier and modulation frequency assessed using adaptation. J Assoc Res Otolaryngol 16(6):747–762. https://doi.org/10.1007/s10162-015-0533-9
Heinz MG, Young ED (2004) Response growth with sound level in auditory-nerve fibers after noise-induced hearing loss. J Neurophysiol, 91(2):784–795. https://doi.org/10.1152/jn.00776.2003
Henry KS, Kale S, Scheidt RE, Heinz MG (2011) Auditory brainstem responses predict auditory nerve fiber thresholds and frequency selectivity in hearing impaired chinchillas. Hear Res 280(1–2):236–244. https://doi.org/10.1016/j.heares.2011.06.002
Henry KS, Kale S, Heinz MG (2016) Distorted tonotopic coding of temporal envelope and fine structure with noise-induced hearing loss. J Neurosci 36(7):2227–2237. https://doi.org/10.1523/JNEUROSCI.3944-15.2016
Henry KS, Sayles M, Hickox AE, Heinz MG (2019) Divergent auditory-nerve encoding deficits between two common etiologies of sensorineural hearing loss. J Neurosci 39(35):6879–6887. https://doi.org/10.1523/JNEUROSCI.0038-19.2019
Joris PX, Yin TCT (1992) Responses to amplitude-modulated tones in the auditory nerve of the cat. J Acoust Soc Am 91(1):215–232. https://doi.org/10.1121/1.402757
Joris PX, Schreiner CE, Rees A (2004) Neural processing of amplitude-modulated sounds. Physiol Rev 84(2):541–577. https://doi.org/10.1152/physrev.00029.2003
Kale S, Heinz MG (2010) Envelope coding in auditory nerve fibers following noise-induced hearing loss. J Assoc Res Otolaryngol 11(4):657–673. https://doi.org/10.1007/s10162-010-0223-6
King A, Hopkins K, Plack CJ (2016) Differential group delay of the frequency following response measured vertically and horizontally. J Assoc Res Otolaryngol 17(2):133–143. https://doi.org/10.1007/s10162-016-0556-x
Krishnan A, Xu Y, Gandour J, Cariani P (2005) Encoding of pitch in the human brainstem is sensitive to language experience. Brain Res Cogn Brain Res 25(1):161–168. https://doi.org/10.1016/j.cogbrainres.2005.05.004
Kuwada S, Batra R, Maher VL (1986) Scalp potentials of normal and hearing-impaired subjects in response to sinusoidally amplitude-modulated tones. Hear Res 21(2):179–192. https://doi.org/10.1016/0378-5955(86)90038-9
Langner G, Schreiner C, Merzenich MM (1987) Covariation of latency and temporal resolution in the inferior colliculus of the cat. Hear Res 31(2):197–201. https://doi.org/10.1016/0378-5955(87)90127-4
Liberman MC, Dodds LW (1984a) Single-neuron labeling and chronic cochlear pathology. III. Stereocilia damage and alterations of threshold tuning curves. Hear Res 16(1):55–74. https://doi.org/10.1016/0378-5955(84)90025-X
Liberman MC, Dodds LW (1984b) Single-neuron labeling and chronic cochlear pathology. II. Stereocilia damage and alterations of spontaneous discharge rates. Hear Res 16(1):43–53. https://doi.org/10.1016/0378-5955(84)90024-8,
Lindblom BEF, Studdert Kennedy M (1967) On the role of formant transitions in vowel recognition. J Acoust Soc Am 42(4):830–843. https://doi.org/10.1121/1.1910655
Miller RL, Schilling JR, Franck KR, Young ED (1997) Effects of acoustic trauma on the representation of the vowel /ε/ in cat auditory nerve fibers. J Acoust Soc Am 101(6):3602–3616. https://doi.org/10.1121/1.418321
Mitra PP, Pesaran B (1999) Analysis of dynamic brain imaging data. Biophys J 76(2):691–708. https://doi.org/10.1016/S0006-3495(99)77236-X
Nielsen JB, Dau T (2009) Development of a Danish speech intelligibility test. Int J Audiol 48(10):729–741. https://doi.org/10.1080/14992020903019312
Parthasarathy A, Cunningham PA, Bartlett EL (2010) Age-related differences in auditory processing as assessed by amplitude-modulation following responses in quiet and in noise. Front Aging Neurosci 2. https://doi.org/10.3389/fnagi.2010.00152
Sachs MB, Young ED (1979) Encoding of steady-state vowels in the auditory nerve: representation in terms of discharge rate. J Acoust Soc Am 66(2):470–479. https://doi.org/10.1121/1.383098
Salvi RJ, Saunders SS, Gratton MA, Arehole S, Powers N (1990) Enhanced evoked response amplitudes in the inferior colliculus of the chinchilla following acoustic trauma. Hear Res 50(1):245–257. https://doi.org/10.1016/0378-5955(90)90049-U
Salvi RJ, Wang J, Ding D (2000) Auditory plasticity and hyperactivity following cochlear damage. Hear Res 147(1):261–274. https://doi.org/10.1016/S0378-5955(00)00136-2
Schmiedt RA, Mills JH, Adams JC (1990) Tuning and suppression in auditory nerve fibers of aged gerbils raised in quiet or noise. Hear Res 45(3):221–236. https://doi.org/10.1016/0378-5955(90)90122-6
Shaheen LA, Valero MD, Liberman MC (2015) Towards a diagnosis of cochlear neuropathy with envelope following responses. J Assoc Res Otolaryngol 16:727–745. https://doi.org/10.1007/s10162-015-0539-3
Shinn-Cunningham B, Ruggles DR, Bharadwaj H (2013) How early aging and environment interact in everyday listening: from brainstem to behavior through modeling. In: Moore BCJ, Patterson RD, Winter IM, Carlyon RP, Gockel HE (eds) Basic aspects of hearing, Advances in Experimental Medicine and Biology. Springer, New York, pp 501–510
Thomson DJ (1982) Spectrum estimation and harmonic analysis. Proc IEEE 70(9):1055–1096. https://doi.org/10.1109/PROC.1982.12433
Verhulst S, Ernst F, Garrett M, Vasilkov V (2018) Suprathreshold psychoacoustics and envelope-following response relations: Normal-hearing, synaptopathy and cochlear gain loss. Acta Acust Acust 104(5):800–803
Wang L, Bharadwaj H, Shinn-Cunningham B (2019) Assessing cochlear-place specific temporal coding using multi-band complex tones to measure envelope-following responses. Neuroscience 407:67–74. https://doi.org/10.1016/j.neuroscience.2019.02.003
Wible B, Nicol T, Kraus N (2004) Atypical brainstem representation of onset and formant structure of speech sounds in children with language-based learning problems. Biological Psychology 67(3):299–317. https://doi.org/10.1016/j.biopsycho.2004.02.002
Wible B, Nicol T, Kraus N (2005) Encoding of complex sounds in an animal model: implications for understanding speech perception in humans. Auditory Cortex: Towards a Synthesis of Human and Animal Research Lawrence Erlbaum Associates, Oxford, pp 241–254
Zhong Z, Henry KS, Heinz MG (2014) Sensorineural hearing loss amplifies neural coding of envelope information in the central auditory system of chinchillas. Hear Res 309:55–62. https://doi.org/10.1016/j.heares.2013.11.006
Zhu L, Bharadwaj H, Xia J, Shinn-Cunningham B (2013) A comparison of spectral magnitude and phase-locking value analyses of the frequency-following response to complex tones. J Acoust Soc Am 134(1):384–395. https://doi.org/10.1121/1.4807498
Acknowledgments
We would like to thank Ravi Krishnan and Hari Bharadwaj for stimulating discussions at various stages of this study. We would also like to thank Amanda Maulden, Caitlin Heffner, Hannah Ginsberg, Vibha Viswanathan, and two anonymous reviewers for valuable comments that significantly improved this manuscript.
Funding
This research was supported by an International Project Grant from Action on Hearing Loss (UK) and by NIH (R01-DC009838).
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of Interest
The authors declare that they have no conflict of interest.
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
Parida, S., Heinz, M.G. Noninvasive Measures of Distorted Tonotopic Speech Coding Following Noise-Induced Hearing Loss. JARO 22, 51–66 (2021). https://doi.org/10.1007/s10162-020-00755-2
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10162-020-00755-2