Research ArticleSensory Processing

Envelope following responses predict speech-in-noise performance in normal-hearing listeners

Published Online:https://doi.org/10.1152/jn.00620.2020

Permanent threshold elevation after noise exposure or aging is caused by loss of sensory cells; however, animal studies show that hair cell loss is often preceded by degeneration of the synapses between sensory cells and auditory nerve fibers. Silencing these neurons is likely to degrade auditory processing and may contribute to difficulties understanding speech in noisy backgrounds. Reduction of suprathreshold ABR amplitudes can be used to quantify synaptopathy in inbred mice. However, ABR amplitudes are highly variable in humans, and thus more challenging to use. Since noise-induced neuropathy preferentially targets fibers with high thresholds and low spontaneous rate and because phase locking to temporal envelopes is particularly strong in these fibers, measuring envelope following responses (EFRs) might be a more robust measure of cochlear synaptopathy. A recent auditory model further suggests that modulation of carrier tones with rectangular envelopes should be less sensitive to cochlear amplifier dysfunction and, therefore, a better metric of cochlear neural damage than sinusoidal amplitude modulation. In this study, we measure performance scores on a variety of difficult word-recognition tasks among listeners with normal audiograms and assess correlations with EFR magnitudes to rectangular versus sinusoidal modulation. Higher harmonics of EFR magnitudes evoked by a rectangular-envelope stimulus were significantly correlated with word scores, whereas those evoked by sinusoidally modulated tones did not. These results support previous reports that individual differences in synaptopathy may be a source of speech recognition variability despite the presence of normal thresholds at standard audiometric frequencies.

NEW & NOTEWORTHY Recent studies suggest that millions of people may be at risk of permanent impairment from cochlear synaptopathy, the age-related and noise-induced degeneration of neural connections in the inner ear. This study examines electrophysiological responses to stimuli designed to improve detection of neural damage in subjects with normal hearing sensitivity. The resultant correlations with word recognition performance are consistent with a contribution of cochlear neural damage to deficits in hearing in noise abilities.

REFERENCES

  • 1. Kujawa SG , Liberman MC . Adding insult to injury: cochlear nerve degeneration after "temporary" noise-induced hearing loss. J Neurosci 29: 14077–14085, 2009. doi:10.1523/JNEUROSCI.2845-09.2009.
    Crossref | PubMed | ISI | Google Scholar
  • 2. Viana LM , O'Malley JT , Burgess BJ , Jones DD , Oliveira CA , Santos F , Merchant SN , Liberman LD , Liberman MC . Cochlear neuropathy in human presbycusis: confocal analysis of hidden hearing loss in post-mortem tissue. Hear Res 327: 78–88, 2015. doi:10.1016/j.heares.2015.04.014.
    Crossref | PubMed | ISI | Google Scholar
  • 3. Wu PZ , Liberman LD , Bennett K , de Gruttola V , O'Malley JT , Liberman MC . Primary neural degeneration in the human cochlea: evidence for hidden hearing loss in the aging ear. Neuroscience 407: 8–20, 2019. doi:10.1016/j.neuroscience.2018.07.053.
    Crossref | PubMed | ISI | Google Scholar
  • 4. Felder E , Schrott-Fischer A . Quantitative evaluation of myelinated nerve fibres and hair cells in cochleae of humans with age-related high-tone hearing loss. Hear Res 91: 19–32, 1995. doi:10.1016/0378-5955(95)00158-1.
    Crossref | PubMed | ISI | Google Scholar
  • 5. Lobarinas E , Salvi R , Ding D . Insensitivity of the audiogram to carboplatin induced inner hair cell loss in chinchillas. Hear Res 302: 113–120, 2013. doi:10.1016/j.heares.2013.03.012.
    Crossref | PubMed | ISI | Google Scholar
  • 6. Woellner RC , Schuknecht HF . Hearing loss from lesions of the cochlear nerve: an experimental and clinical study. Trans Am Acad Ophthalmol Otolaryngol 59: 147–149, 1955.
    PubMed | Google Scholar
  • 7. Furman AC , Kujawa SG , Liberman MC . Noise-induced cochlear neuropathy is selective for fibers with low spontaneous rates. J Neurophysiol 110: 577–586, 2013. doi:10.1152/jn.00164.2013.
    Link | ISI | Google Scholar
  • 8. Schmiedt RA , Mills JH , Boettcher FA . Age-related loss of activity of auditory-nerve fibers. J Neurophysiol 76: 2799–2803, 1996. doi:10.1152/jn.1996.76.4.2799.
    Link | ISI | Google Scholar
  • 9. Costalupes JA , Young ED , Gibson DJ . Effects of continuous noise backgrounds on rate response of auditory nerve fibers in cat. J Neurophysiol 51: 1326–1344, 1984. doi:10.1152/jn.1984.51.6.1326.
    Link | ISI | Google Scholar
  • 10. Alvord LS . Cochlear dysfunction in “normal hearing” patients with history of noise exposure. Ear Hear 4: 247–250, 1983. doi:10.1097/00003446-198309000-00005.
    Crossref | PubMed | ISI | Google Scholar
  • 11. Dubno JR , Dirks DD , Morgan DE . Effects of age and mild hearing loss on speech recognition in noise. J Acoust Soc Am 76: 87–96, 1984. doi:10.1121/1.391011.
    Crossref | PubMed | ISI | Google Scholar
  • 12. Grant KJ , Mepani AM , Wu P , Hancock KE , de Gruttola V , Liberman MC , Maison SF . Electrophysiological markers of cochlear function correlate with hearing-in-noise performance among audiometrically normal subjects. J Neurophysiol 124: 418–431, 2020. doi:10.1152/jn.00016.2020.
    Link | ISI | Google Scholar
  • 13. Kujawa SG , Liberman MC . Synaptopathy in the noise-exposed and aging cochlea: primary neural degeneration in acquired sensorineural hearing loss. Hear Res 330: 191–199, 2015. doi:10.1016/j.heares.2015.02.009.
    Crossref | PubMed | ISI | Google Scholar
  • 14. Mepani AM , Kirk SA , Hancock KE , Bennett K , de Gruttola V , Liberman MC , Maison SF . Middle-ear muscle reflex and word-recognition in "normal hearing" adults: evidence for cochlear synaptopathy? Ear Hear 41: 25–38, 2020. doi:10.1097/AUD.0000000000000804.
    Crossref | PubMed | ISI | Google Scholar
  • 15. Okada M , Welling DB , Liberman MC , Maison SF . Chronic conductive hearing loss is associated with speech intelligibility deficits in patients with normal bone conduction thresholds. Ear Hear 41: 500–507, 2020. doi:10.1097/AUD.0000000000000787.
    Crossref | PubMed | ISI | Google Scholar
  • 16. Okada M , Parthasarathy A , Welling DB , Liberman MC , Maison SF . Idiopathic sudden sensorineural hearing loss speech intelligibility deficits following threshold recovery. Ear Hear 2020. In press. doi:10.1097/AUD.0000000000000987.
    Crossref | Google Scholar
  • 17. Rajan R , Cainer KE . Ageing without hearing loss or cognitive impairment causes a decrease in speech intelligibility only in informational maskers. Neuroscience 154: 784–795, 2008. doi:10.1016/j.neuroscience.2008.03.067.
    Crossref | PubMed | ISI | Google Scholar
  • 18. Sergeyenko Y , Lall K , Liberman MC , Kujawa SG . Age-related cochlear synaptopathy: an early-onset contributor to auditory functional decline. J Neurosci 33: 13686–13694, 2013. doi:10.1523/JNEUROSCI.1783-13.2013.
    Crossref | PubMed | ISI | Google Scholar
  • 19. Gorga MP , Kaminski JR , Beauchaine KA , Jesteadt W . Auditory brainstem responses to tone bursts in normally hearing subjects. J Speech Hear Res 31: 87–97, 1988. doi:10.1044/jshr.3101.87.
    Crossref | PubMed | Google Scholar
  • 20. Nikiforidis GC , Koutsojannis CM , Varakis JN , Goumas PD . Reduced variance in the latency and amplitude of the fifth wave of auditory brain stem response after normalization for head size. Ear Hear 14: 423–428, 1993. doi:10.1097/00003446-199312000-00008.
    Crossref | PubMed | ISI | Google Scholar
  • 21. Bharadwaj HM , Mai AR , Simpson JM , Choi I , Heinz MG , Shinn-Cunningham BG . Non-invasive assays of cochlear synaptopathy — candidates and considerations. Neuroscience 407: 53–66, 2019. doi:10.1016/j.neuroscience.2019.02.031.
    Crossref | PubMed | ISI | Google Scholar
  • 22. Shaheen LA , Valero MD , Liberman MC . Towards a diagnosis of cochlear neuropathy with envelope following responses. J Assoc Res Otolaryngol 16: 727–745, 2015. doi:10.1007/s10162-015-0539-3.
    Crossref | PubMed | ISI | Google Scholar
  • 23. Bharadwaj HM , Masud S , Mehraei G , Verhulst S , Shinn-Cunningham BG . Individual differences reveal correlates of hidden hearing deficits. J Neurosci 35: 2161–2172, 2015. doi:10.1523/JNEUROSCI.3915-14.2015.
    Crossref | PubMed | ISI | Google Scholar
  • 24. Encina-Llamas G , Harte JM , Dau T , Shinn-Cunningham B , Epp B . Investigating the effect of cochlear synaptopathy on envelope following responses using a model of the auditory nerve. J Assoc Res Otolaryngol 20: 363–382, 2019. doi:10.1007/s10162-019-00721-7.
    Crossref | PubMed | ISI | Google Scholar
  • 25. Grose JH , Buss E , Hall JW . Loud music exposure and cochlear synaptopathy in young adults: isolated auditory brainstem response effects but no perceptual consequences. Trends Hear 21: 2331216517737417, 2017. doi:10.1177/2331216517737417.
    Crossref | PubMed | ISI | Google Scholar
  • 26. Guest H , Munro KJ , Prendergast G , Millman RE , Plack CJ . 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, 2018. doi:10.1016/j.heares.2018.03.008.
    Crossref | PubMed | ISI | Google Scholar
  • 27. Vasilkov S , Garrett M , Mauermann M , Verhulst S . Enhancing the sensitivity of the envelope-following response for cochlear synaptopathy screening in humans: the role of stimulus envelope. Hear Res 400: 108132, 2021. doi:10.1016/j.heares.2020.108132.
    Crossref | PubMed | ISI | Google Scholar
  • 28. Verhulst S , Altoè A , Vasilkov V . Computational modeling of the human auditory periphery: Auditory-nerve responses, evoked potentials and hearing loss. Hear Res 360: 55–75, 2018. doi:10.1016/j.heares.2017.12.018.
    Crossref | PubMed | ISI | Google Scholar
  • 29. Dreyer A , Delgutte B . Phase locking of auditory-nerve fibers to the envelopes of high-frequency sounds: implications for sound localization. J Neurophysiol 96: 2327–2341, 2006. doi:10.1152/jn.00326.2006.
    Link | ISI | Google Scholar
  • 30. Parthasarathy A , Kujawa SG . Synaptopathy in the aging cochlea: characterizing early-neural deficits in auditory temporal envelope processing. J Neurosci 38: 7108–7119, 2018. doi:10.1523/JNEUROSCI.3240-17.2018.
    Crossref | PubMed | ISI | Google Scholar
  • 31. Noffsinger D , Wilson RH , Musiek FE . Department of veterans affairs compact disc recording for auditory perceptual assessment: background and introduction. J Am Acad Audiol 5: 231–235, 1994.
    PubMed | Google Scholar
  • 32. Burkard RF , Sims D . A comparison of the effects of broadband masking noise on the auditory brainstem response in young and older adults. Am J Audiol 11: 13–22, 2002. doi:10.1044/1059-0889(2002/004).
    Crossref | PubMed | Google Scholar
  • 33. Johannesen PT , Buzo BC , Lopez-Poveda EA . Evidence for age-related cochlear synaptopathy in humans unconnected to speech-in-noise intelligibility deficits. Hear Res 374: 35–48, 2019. doi:10.1016/j.heares.2019.01.017.
    Crossref | PubMed | ISI | Google Scholar
  • 34. Lee J , Dhar S , Abel R , Banakis R , Grolley E , Lee J , Zecker S , Siegel J . Behavioral hearing thresholds between 0.125 and 20 kHz using depth-compensated ear simulator calibration. Ear Hear 33: 315–329, 2012. doi:10.1097/AUD.0b013e31823d7917.
    Crossref | PubMed | ISI | Google Scholar
  • 35. Füllgrabe C , Moore BC , Stone MA . Age-group differences in speech identification despite matched audiometrically normal hearing: contributions from auditory temporal processing and cognition. Front Aging Neurosci 6: 347, 2015. doi:10.3389/fnagi.2014.00347.
    Crossref | PubMed | ISI | Google Scholar
  • 36. Kamerer AM , Kopun JG , Fultz SE , Neely ST , Rasetshwane DM . Reliability of measures intended to assess threshold-independent hearing disorders. Ear Hear 40: 1267–1279, 2019. doi:10.1097/AUD.0000000000000711.
    Crossref | PubMed | ISI | Google Scholar
  • 37. Hunter LL , Monson BB , Moore DR , Dhar S , Wright BA , Munro KJ , Zadeh LM , Blankenship CM , Stiepan SM , Siegel JH . Extended high frequency hearing and speech perception implications in adults and children. Hear Res 397: 107922, 2020. doi:10.1016/j.heares.2020.107922.
    Crossref | PubMed | ISI | Google Scholar
  • 38. Motlagh Zadeh L , Silbert NH , Sternasty K , Swanepoel W , Hunter LL , Moore DR . Extended high-frequency hearing enhances speech perception in noise. Proc Natl Acad Sci USA 116: 23753–23759, 2019. doi:10.1073/pnas.1903315116.
    Crossref | PubMed | ISI | Google Scholar
  • 39. Yeend I , Beach EF , Sharma M . Working memory and extended high-frequency hearing in adults: diagnostic predictors of speech-in-noise perception. Ear Hear 40: 458–467, 2019. doi:10.1097/AUD.0000000000000640.
    Crossref | PubMed | ISI | Google Scholar
  • 40. Coen RF , Robertson DA , Kenny RA , King-Kallimanis BL . Strengths and limitations of the MoCA for assessing cognitive functioning: findings from a large representative sample of Irish older adults. J Geriatr Psychiatry Neurol 29: 18–24, 2016. doi:10.1177/0891988715598236.
    Crossref | PubMed | ISI | Google Scholar
  • 41. Bramhall NF , McMillan GP , Mashburn AN . Subclinical auditory dysfunction: relationship between distortion product otoacoustic emissions and the audiogram. Am J Audiol 19: 1–16, 2021. doi:10.1044/2020_AJA-20-00056.
    Crossref | PubMed | Google Scholar
  • 42. Ortmann A , Guardia YC , Abdala C . Aging and Cochlear Nonlinearity as Measured with Distortion OAEs and Loudness Perception. Abstract of the 40th MidWinter meeting of the Association for Research in Otolaryngology. Baltimore, MD, 2017.
    Google Scholar
  • 43. Kuwada S , Anderson JS , Batra R , Fitzpatrick DC , Teissier N , D'Angelo WR . Sources of the scalp-recorded amplitude-modulation following response. J Am Acad Audiol 13: 188–204, 2002. doi:10.1055/s-0040-1715963.
    Crossref | PubMed | Google Scholar
  • 44. Joris PX , Schreiner CE , Rees A . Neural processing of amplitude-modulated sounds. Physiol Rev 84: 541–577, 2004. doi:10.1152/physrev.00029.2003.
    Link | ISI | Google Scholar
  • 45. Parthasarathy A , Bartlett E . Two-channel recording of auditory-evoked potentials to detect age-related deficits in temporal processing. Hear Res 289: 52–62, 2012. doi:10.1016/j.heares.2012.04.014.
    Crossref | PubMed | ISI | Google Scholar
  • 46. Pethe J , Von Specht H , Mühler R , Hocke T . Amplitude modulation following responses in awake and sleeping humansa comparison for 40 Hz and 80 Hz modulation frequency. Scand Audiol Suppl 30: 152–155, 2001. doi:10.1080/010503901300007371.
    Crossref | Google Scholar
  • 47. Kohlrausch A , Fassel R , Dau T . The influence of carrier level and frequency on modulation and beat-detection thresholds for sinusoidal carriers. J Acoust Soc Am 108: 723–734, 2000. doi:10.1121/1.429605.
    Crossref | PubMed | ISI | Google Scholar
  • 48. Ruggero MA , Rich NC , Recio A , Narayan SS , Robles L . Basilar-membrane responses to tones at the base of the chinchilla cochlea. J Acoust Soc Am 101: 2151–2163, 1997. doi:10.1121/1.418265.
    Crossref | PubMed | ISI | Google Scholar
  • 49. Wilson JL , Abrams KS , Henry KS . Effects of kainic acid-induced auditory nerve damage on envelope-following responses in the budgerigar (Melopsittacus undulates). J Assoc Res Otolaryngol 22: 33–49, 2021. doi:10.1007/s10162-020-00776-x.
    Crossref | PubMed | ISI | Google Scholar
  • 50. Charaziak KK , Dong W , Altoè A , Shera CA . Asymmetry and microstructure of temporal-suppression patterns in basilar-membrane responses to clicks: relation to tonal suppression and traveling-wave dispersion. J Assoc Res Otolaryngol 21: 151–170, 2020. doi:10.1007/s10162-020-00747-2.
    Crossref | PubMed | ISI | Google Scholar