Advertisement

Click-Evoked Auditory Efferent Activity: Rate and Level Effects

  • Sriram Boothalingam
  • Julianne Kurke
  • Sumitrajit Dhar
Research Article

Abstract

There currently are no standardized protocols to evaluate auditory efferent function in humans. Typical tests use broadband noise to activate the efferents, but only test the contralateral efferent pathway, risk activating the middle ear muscle reflex (MEMR), and are laborious for clinical use. In an attempt to develop a clinical test of bilateral auditory efferent function, we have designed a method that uses clicks to evoke efferent activity, obtain click-evoked otoacoustic emissions (CEOAEs), and monitor MEMR. This allows for near-simultaneous estimation of cochlear and efferent function. In the present study, we manipulated click level (60, 70, and 80 dB peak-equivalent sound pressure level [peSPL]) and rate (40, 50, and 62.5 Hz) to identify an optimal rate-level combination that evokes measurable efferent modulation of CEOAEs. Our findings (n = 58) demonstrate that almost all click levels and rates used caused significant inhibition of CEOAEs, with a significant interaction between level and rate effects. Predictably, bilateral activation produced greater inhibition compared to stimulating the efferents only in the ipsilateral or contralateral ear. In examining the click rate-level effects during bilateral activation in greater detail, we observed a 1-dB inhibition of CEOAE level for each 10-dB increase in click level, with rate held constant at 62.5 Hz. Similarly, a 10-Hz increase in rate produced a 0.74-dB reduction in CEOAE level, with click level held constant at 80 dB peSPL. The effect size (Cohen’s d) was small for either monaural condition and medium for bilateral, faster-rate, and higher-level conditions. We were also able to reliably extract CEOAEs from efferent eliciting clicks. We conclude that clicks can indeed be profitably employed to simultaneously evaluate cochlear health using CEOAEs as well as their efferent modulation. Furthermore, using bilateral clicks allows the evaluation of both the crossed and uncrossed elements of the auditory efferent nervous system, while yielding larger, more discernible, inhibition of the CEOAEs relative to either ipsilateral or contralateral condition.

Keywords

middle ear muscle reflex efferents CEOAE medial olivocochlear reflex 

Notes

Acknowledgments

This study was funded by American Speech-Language and Hearing Foundation New Investigator grant to SB and a Knowles Hearing Center grant to SD. The authors thank Prof. Donata Oertel for the stimulating discussions; Jen Birstler, Department of Biostatistics and Medical Informatics, University of Wisconsin–Madison for the assistance with statistics; and the two anonymous reviewers for the helpful comments.

References

  1. Abdala C, Mishra S, Garinis A (2013) Maturation of the human medial efferent reflex revisited. J Acoust Soc Am 133(2):938–950CrossRefGoogle Scholar
  2. Abdala C, Dhar S, Ahmadi M, Luo P (2014) Aging of the medial olivocochlear reflex and associations with speech perception. J Acoust Soc Am 135(2):755–765CrossRefGoogle Scholar
  3. Backus BC, Guinan JJ (2006) Time-course of the human medial olivocochlear reflex. J Acoust Soc Am 119(5):2889–2904CrossRefGoogle Scholar
  4. Benjamini Y, Hochberg Y (1995) Controlling the false discovery rate—a practical and powerful approach to multiple testing. J R Stat Soc Ser B-Methodol 57:289–300Google Scholar
  5. Berlin CI, Hood LJ, Wen H, Szabo P, Cecola RP, Rigby P, Jackson DF (1993) Contralateral suppression of non-linear click-evoked otoacoustic emissions. Hear Res 71:1):1–1)11CrossRefGoogle Scholar
  6. Berlin CI, Hood LJ, Hurley AE, Wen H, Kemp DT (1995) Binaural noise suppresses linear click-evoked otoacoustic emissions more than ipsilateral or contralateral noise. Hear Res 87(1):96–103CrossRefGoogle Scholar
  7. Bhatt I (2017) Increased medial olivocochlear reflex strength in normal-hearing, noise-exposed humans. PLoS One 12(9):e0184036–e0184018CrossRefGoogle Scholar
  8. de Boer J, Thornton ARD, Krumbholz K (2012) What is the role of the medial olivocochlear system in speech-in-noise processing? J Neurophysiol 107(5):1301–1312CrossRefGoogle Scholar
  9. Boothalingam S, Purcell DW (2015) Influence of the stimulus presentation rate on medial olivocochlear system assays. J Acoust Soc Am 137(2):724–732CrossRefGoogle Scholar
  10. Boothalingam S, Purcell D, Scollie S (2014) Influence of 100 Hz amplitude modulation on the human medial olivocochlear reflex. Neurosci Lett 580:56–61CrossRefGoogle Scholar
  11. Boothalingam S, Allan C, Allen P, Purcell D (2015) Cochlear delay and medial olivocochlear functioning in children with suspected auditory processing disorder. PLoS One 10(8):1–18CrossRefGoogle Scholar
  12. Boothalingam S, Macpherson E, Allan C, Allen P, Purcell D (2016) Localization-in-noise and binaural medial olivocochlear functioning in children and young adults. J Acoust Soc Am 139(1):247–262CrossRefGoogle Scholar
  13. Brashears SM, Morlet TG, Berlin CI, Hood LJ (2003) Olivocochlear efferent suppression in classical musicians. J Am Acad Audiol 14(6):314–324Google Scholar
  14. Brown MC, Kujawa SG, Duca ML (1998) Single olivocochlear neurons in the guinea pig. I. Binaural facilitation of responses to high-level noise. J Neurophysiol 79(6):3077–3087CrossRefGoogle Scholar
  15. Brown MC, de Venecia RK, Guinan JJ (2003) Responses of medial olivocochlear neurons. Exp Brain Res 153(4):491–498CrossRefGoogle Scholar
  16. Charaziak KK, Shera CA (2015) Measuring temporal suppression of clicked-evoked otoacoustic emissions at high frequencies. In Association for Research in Otolaryngology Mid-Winter Meeting Abs, p 308Google Scholar
  17. Collet L, Kemp DT, Veuillet E, Duclaux R, Moulin A, Morgon A (1990a) Effect of contralateral auditory stimuli on active cochlear micro-mechanical properties in human subjects. Hear Res 43(2–3):251–261CrossRefGoogle Scholar
  18. Collet L, Kemp DT, Veuillet E, Duclaux R, Moulin A, Morgon A (1990b) Effect of contralateral auditory-stimuli on active cochlear micromechanical properties in human-subjects. Hear Res 43:251–262CrossRefGoogle Scholar
  19. Deeter R, Abel R, Calandruccio L, Dhar S (2009) Contralateral acoustic stimulation alters the magnitude and phase of distortion product otoacoustic emissions. J Acoust Soc Am 126(5):2413–2424CrossRefGoogle Scholar
  20. Delano PH, Elgueda D, Hamame CM, Robles L (2007) Selective attention to visual stimuli reduces cochlear sensitivity in chinchillas. J Neurosci 27(15):41464153CrossRefGoogle Scholar
  21. Eggermont JJ, Spoor A (1973) Cochlear adaptation in guinea pigs. Quant Description Audiol 12(4):193–220Google Scholar
  22. Feeney MP, Keefe DH (1999) Acoustic reflex detection using wide-band acoustic reflectance, admittance, and power measurements. J Speech, Lang Hear Res 42(5):1029–1041CrossRefGoogle Scholar
  23. Ferragamo MJ, Golding NL, Oertel D (1998) Synaptic inputs to stellate cells in the ventral cochlear nucleus. J Neurophysiol 79(1):51–63CrossRefGoogle Scholar
  24. Fujino K, Oertel D (2001) Cholinergic modulation of stellate cells in the mammalian ventral cochlear nucleus. J Neurosci 21(18):7372–7383CrossRefGoogle Scholar
  25. Garinis AC, Glattke T, Cone-Wesson BK (2008) TEOAE suppression in adults with learning disabilities. Int J Audiol 47(10):607–614CrossRefGoogle Scholar
  26. Goodman S (2017) Auditory research lab audio software. University of Iowa, Iowa City https://github.com/myKungFu/ARLas Google Scholar
  27. Goodman SS, Fitzpatrick DF, Ellison JC, Jesteadt W, Keefe DH (2009) High-frequency click-evoked otoacoustic emissions and behavioral thresholds in humans. J Acoust Soc Am 125(2):1014–1032CrossRefGoogle Scholar
  28. Guinan JJ (2006) Olivocochlear efferents: anatomy, physiology, function, and the measurement of efferent effects in humans. Ear Hear 27(6):589–607CrossRefGoogle Scholar
  29. Guinan JJ (2014) Olivocochlear efferent function: issues regarding methods and the interpretation of results. Front Syst Neurosci 8:142CrossRefGoogle Scholar
  30. Guinan JJ, Backus BC, Lilaonitkul W, Aharonson V (2003) Medial olivocochlear efferent reflex in humans: otoacoustic emission (OAE) measurement issues and the advantages of stimulus frequency OAEs. J Assoc Res Otolaryngol 4(4):521–540CrossRefGoogle Scholar
  31. Hood LJ, Berlin CI, Bordelon J, Rose K (2003) Patients with auditory neuropathy/dys-synchrony lack efferent suppression of transient evoked otoacoustic emissions. J Am Acad Audiol 14(6):302–313Google Scholar
  32. Kiang N (1965) Discharge patterns of single fibers in the cat’s auditory nerve. MIT Press, Cambridge, MAGoogle Scholar
  33. Kim SH, Frisina DR, Frisina RD (2002) Effects of age on contralateral suppression of distortion product otoacoustic emissions in human listeners with normal hearing. Audiol Neurotol 7(6):348–357CrossRefGoogle Scholar
  34. Kumar A, Vanaja CS (2004) Functioning of olivocochlear bundle and speech perception in noise. Ear Hear 25(2):142–146CrossRefGoogle Scholar
  35. Liberman MC (1988) Response properties of cochlear efferent neurons: monaural vs. binaural stimulation and the effects of noise. J Neurophysiol 60(5):1779–1798CrossRefGoogle Scholar
  36. Liberman MC, Liberman LD, Maison SF (2014) Efferent feedback slows cochlear aging. J Neurosci 34(13):4599–4607CrossRefGoogle Scholar
  37. Lilaonitkul W, Guinan JJ (2009) Human medial olivocochlear reflex: effects as functions of contralateral, ipsilateral, and bilateral elicitor bandwidths. J Assoc Res Otolaryngol 10(3):459–470CrossRefGoogle Scholar
  38. Lilaonitkul W, Guinan JJ (2012) Frequency tuning of medial-olivocochlear-efferent acoustic reflexes in humans as functions of probe frequency. J Neurophysiol 107(6):1598–1611CrossRefGoogle Scholar
  39. Maison SF, Liberman MC (2000) Predicting vulnerability to acoustic injury with a noninvasive assay of olivocochlear reflex strength. J Neurosci 20(12):4701–4707CrossRefGoogle Scholar
  40. Maison SF, Usubuchi H, Liberman MC (2013) Efferent feedback minimizes cochlear neuropathy from moderate noise exposure. J Neurosci 33(13):5542–5552CrossRefGoogle Scholar
  41. Marks KL, Siegel JH (2017) Differentiating middle ear and medial olivocochlear effects on transient-evoked otoacoustic emissions. J Assoc Res Otolaryngol 121:1588–1514Google Scholar
  42. Mertes IB, Goodman SS (2015) Within- and across-subject variability of repeated measurements of medial olivocochlear-induced changes in transient-evoked otoacoustic emissions. Ear Hear 37(2): e72–e84Google Scholar
  43. Mishra SK, Lutman ME (2013) Repeatability of click-evoked otoacoustic emission-based medial olivocochlear efferent assay. Ear Hear 34(6):789–798CrossRefGoogle Scholar
  44. Mott JB, Norton SJ, Neely ST, Warr BW (1989) Changes in spontaneous otoacoustic emissions produced by acoustic stimulation of the contralateral ear. Hear Res 38(3):229–242CrossRefGoogle Scholar
  45. Muchnik C, Ari-Even-Roth D, Othman-Jebara R, Putter-Katz H, Shabtai EL, Hildesheimer M (2004) Reduced medial olivocochlear bundle system function in children with auditory processing disorders. Audiol Neurotol 9(2):107–114CrossRefGoogle Scholar
  46. Norton SJ, Gorga MP, Widen JE, Folsom RC, Sininger Y, Cone-Wesson BK, Vohr BR, Fletcher KA (2000) Identification of neonatal hearing impairment: summary and recommendations. Ear Hear 21(5):529–535CrossRefGoogle Scholar
  47. Oertel D, Wright S, Cao X-J, Ferragamo M, Bal R (2011) The multiple functions of T stellate/multipolar/chopper cells in the ventral cochlear nucleus. Hear Res 276(1–2):61–69CrossRefGoogle Scholar
  48. Peake WT, Goldstein MH Jr, Kiang NYS (1962) Responses of the auditory nerve to repetitive acoustic stimuli. J Acoust Soc Am 34(5):562–570CrossRefGoogle Scholar
  49. Perrot X, Collet L (2013) Function and plasticity of the medial olivocochlear system in musicians: a review. Hear Res 308:27–40CrossRefGoogle Scholar
  50. Pfeiffer RR, Kim DO (1972) Response patterns of single cochlear nerve fibers to click stimuli: descriptions for cat. J Acoust Soc Am 52(6B):1669–1677CrossRefGoogle Scholar
  51. R Core Team (2013) R: a language and environment for statistical computing. In: R Foundation for Statistical Computing, Vienna, Austria. http://www.R-project.org/ Google Scholar
  52. Rasmussen GL (1946) The olivary peduncle and other fiber projections of the superior olivary complex. J Comp Neurol 84(2):141–219CrossRefGoogle Scholar
  53. Robertson D, Gummer M (1985) Physiological and morphological characterization of efferent neurons in the guinea pig cochlea. Hear Res 20(1):63–77CrossRefGoogle Scholar
  54. Robles L, Ruggero MA (2001) Mechanics of the mammalian cochlea. Physiol Rev 81(3):1305–1352CrossRefGoogle Scholar
  55. Robles L, Ruggero MA, Rich NC (1986) Basilar membrane mechanics at the base of the chinchilla cochlea. I. Input–output functions, tuning curves, and response phases. J Acoust Soc Am 80(5):1364–1374CrossRefGoogle Scholar
  56. Rosnow RL, Rosenthal R (1996) Computing contrasts, effect sizes, and counternulls on other people’s published data: general procedures for research consumers. Psychol Methods 1(4):331–340 h CrossRefGoogle Scholar
  57. Ruggero MA (1992) Physiology and coding of sound in the auditory nerve. In popper, A. N. And fay, R. R., editors, The Mammalian Auditory pathway. Neurophysiology:34–93Google Scholar
  58. Shera CA, Guinan JJ (1999) Evoked otoacoustic emissions arise by two fundamentally different mechanisms: a taxonomy for mammalian OAEs. J Acoust Soc Am 105(2 Pt 1):782–798CrossRefGoogle Scholar
  59. Shera CA, Zweig G (1993) Noninvasive measurement of the cochlear traveling-wave ratio. J Acoust Soc Am 93(6):3333–3352CrossRefGoogle Scholar
  60. Smith PH, Rhode WS (1989) Structural and functional properties distinguish two types of multipolar cells in the ventral cochlear nucleus. J Comp Neurol 282(4):595–616CrossRefGoogle Scholar
  61. Thompson AM, Thompson GC (1991) Posteroventral cochlear nucleus projections to olivocochlear neurons. J Comp Neurol 303(2):267–285CrossRefGoogle Scholar
  62. de Venecia RK, Liberman MC, Guinan JJ, Brown MC (2005) Medial olivocochlear reflex interneurons are located in the posteroventral cochlear nucleus: a kainic acid lesion study in guinea pigs. J Comp Neurol 487(4):345–360CrossRefGoogle Scholar
  63. Veuillet E, Collet L, Duclaux R (1991) Effect of contralateral acoustic stimulation on active cochlear micromechanical properties in human subjects: dependence on stimulus variables. J Neurophysiol 65(3):724–735CrossRefGoogle Scholar
  64. Walsh KP, Pasanen EG, McFadden D (2015) Changes in otoacoustic emissions during selective auditory and visual attention. J Acoust Soc Am 137(5):2737–2757CrossRefGoogle Scholar
  65. Wilson US, Sadler KM, Hancock KE, Guinan JJ, Lichtenhan JT (2017) Efferent inhibition strength is a physiological correlate of hyperacusis in children with autism spectrum disorder. J Neurophysiol 118(2):1164–1172CrossRefGoogle Scholar
  66. Winslow RL, Sachs MB (1987) Effect of electrical stimulation of the crossed olivocochlear bundle on auditory nerve response to tones in noise. J Neurophysiol 57(4):1002–1021CrossRefGoogle Scholar
  67. Yoshie N (1968) Auditory nerve action potential responses to clicks in man. Laryngoscope 78(2):198–215CrossRefGoogle Scholar
  68. Zhao W, Dhar S (2012) Frequency tuning of the contralateral medial olivocochlear reflex in humans. J Neurophysiol 108(1):25–30CrossRefGoogle Scholar
  69. Zhao W, Dewey JB, Boothalingam S, Dhar S (2015) Efferent modulation of stimulus frequency otoacoustic emission fine structure. Front Syst Neurosci 9:168Google Scholar

Copyright information

© Association for Research in Otolaryngology 2018

Authors and Affiliations

  • Sriram Boothalingam
    • 1
  • Julianne Kurke
    • 2
  • Sumitrajit Dhar
    • 3
  1. 1.Department of Communication Sciences and Disorders, and The Waisman CenterUniversity of WisconsinMadisonUSA
  2. 2.Roxelyn and Richard Pepper Department of Communication Sciences and DisordersNorthwestern UniversityEvanstonUSA
  3. 3.Roxelyn and Richard Pepper Department of Communication Sciences and Disorders, and The Knowles Hearing CenterNorthwestern UniversityEvanstonUSA

Personalised recommendations