Abstract
>Human hearing is rather insensitive for very low frequencies (i.e. below 100 Hz). Despite this insensitivity, low-frequency sound can cause oscillating changes of cochlear gain in inner ear regions processing even much higher frequencies. These alterations outlast the duration of the low-frequency stimulation by several minutes, for which the term ‘bounce phenomenon’ has been coined. Previously, we have shown that the bounce can be traced by monitoring frequency and level changes of spontaneous otoacoustic emissions (SOAEs) over time. It has been suggested elsewhere that large receptor potentials elicited by low-frequency stimulation produce a net Ca2+ influx and associated gain decrease in outer hair cells. The bounce presumably reflects an underdamped, homeostatic readjustment of increased Ca2+ concentrations and related gain changes after low-frequency sound offset. Here, we test this hypothesis by activating the medial olivocochlear efferent system during presentation of the bounce-evoking low-frequency (LF) sound. The efferent system is known to modulate outer hair cell Ca2+ concentrations and receptor potentials, and therefore, it should modulate the characteristics of the bounce phenomenon. We show that simultaneous presentation of contralateral broadband noise (100 Hz–8 kHz, 65 and 70 dB SPL, 90 s, activating the efferent system) and ipsilateral low-frequency sound (30 Hz, 120 dB SPL, 90 s, inducing the bounce) affects the characteristics of bouncing SOAEs recorded after low-frequency sound offset. Specifically, the decay time constant of the SOAE level changes is shorter, and the transient SOAE suppression is less pronounced. Moreover, the number of new, transient SOAEs as they are seen during the bounce, are reduced. Taken together, activation of the medial olivocochlear system during induction of the bounce phenomenon with low-frequency sound results in changed characteristics of the bounce phenomenon. Thus, our data provide experimental support for the hypothesis that outer hair cell calcium homeostasis is the source of the bounce phenomenon.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Bian L, Scherrer NM (2007) Low-frequency modulation of distortion product otoacoustic emissions in humans. J Acoust Soc Am 122:1681
Boothroyd A, Cawkwell S (1970) Vibrotactile thresholds in pure tone audiometry. Acta Otolaryngol 69:381–387
Burns EM (2009) Long-term stability of spontaneous otoacoustic emissions. J Acoust Soc Am 125:3166–3176
Cheatham MA, Dallos P (2001) Inner hair cell response patterns: implications for low-frequency hearing. J Acoust Soc Am 110:2034–2044
Dallos P (1973) CHAPTER 3—the middle ear. In: The Auditory Periphery Biophysics and Physiology (Dallos P, ed), pp 83–126: Academic Press.
Day JE, Feeney MP (2008) The effect of the 226-Hz probe level on contralateral acoustic stapedius reflex thresholds. J Speech Lang Hear Res 51:1016–1025
Dobie RA, Wilson MJ (1996) A comparison of t test, F test, and coherence methods of detecting steady-state auditory-evoked potentials, distortion-product otoacoustic emissions, or other sinusoids. J Acoust Soc Am 100:2236–2246
Drexl M, Gurkov R, Krause E (2012) Low-frequency modulated quadratic and cubic distortion product otoacoustic emissions in humans. Hear Res 287:91–101
Drexl M, Uberfuhr M, Weddell TD, Lukashkin AN, Wiegrebe L, Krause E, Gurkov R (2014) Multiple indices of the ‘bounce’ phenomenon obtained from the same human ears. JARO 15:57–72
Fex J (1967) Efferent inhibition in the cochlea related to hair-cell dc activity: study of postsynaptic activity of the crossed olivocochlear fibres in the cat. J Acoust Soc Am 41:666–675
Fridberger A, Flock A, Ulfendahl M, Flock B (1998) Acoustic overstimulation increases outer hair cell Ca2+ concentrations and causes dynamic contractions of the hearing organ. Proc Natl Acad Sci U S A 95:7127–7132
Guinan JJ Jr (2006) Olivocochlear efferents: anatomy, physiology, function, and the measurement of efferent effects in humans. Ear Hear 27:589–607
Guinan JJ Jr (2010) Cochlear efferent innervation and function. Curr Opin Otolaryngol Head Neck Surg 18:447–453
Guinan JJ (2012) How are inner hair cells stimulated? Evidence for multiple mechanical drives. Hear Res 292:35–50
Hensel J, Scholz G, Hurttig U, Mrowinski D, Janssen T (2007) Impact of infrasound on the human cochlea. Hear Res 233:67–76
Hirsh I, Ward W (1952) Recovery of the auditory threshold after strong acoustic stimulation. J Acoust Soc Am 24:131
Jacob S, Johansson C, Fridberger A (2013) Noise-induced alterations in cochlear mechanics, electromotility, and cochlear amplification. Pflugers Arch - Eur J Physiol 465:907–917
Johnson SL, Beurg M, Marcotti W, Fettiplace R (2011) Prestin-driven cochlear amplification is not limited by the outer hair cell membrane time constant. Neuron 70:1143–1154
Kemp DT (1986) Otoacoustic emissions, travelling waves and cochlear mechanisms. Hear Res 22:95–104
Kemp DT, Brill OJ (2009) Slow oscillatory cochlear adaptation to brief overstimulation: cochlear homeostasis dynamics. In: Cooper NP, Kemp DT (eds) Concepts and challenges in the biophysics of hearing. World Scientific Publ Co Pte Ltd., Singapore, pp 168–174
Kevanishvili Z, Hofmann G, Burdzgla I, Pietsch M, Gamgebeli Z, Yarin Y, Tushishvili M, Zahnert T (2006) Behavior of evoked otoacoustic emission under low-frequency tone exposure: objective study of the bounce phenomenon in humans. Hear Res 222:62–69
Kirk DL, Patuzzi RB (1997) Transient changes in cochlear potentials and DPOAEs after low-frequency tones: the ‘two-minute bounce’ revisited. Hear Res 112:49–68
Kirk DL, Moleirinho A, Patuzzi RB (1997) Microphonic and DPOAE measurements suggest a micromechanical mechanism for the ‘bounce’ phenomenon following low-frequency tones. Hear Res 112:69–86
Kugler K, Wiegrebe L, Grothe B, Kössl M, Gürkov R, Krause E, Drexl M (2014) Low-frequency sound affects active micromechanics in the human inner ear. Royal Society Open Science 1
Larsen E, Liberman MC (2009) Slow build-up of cochlear suppression during sustained contralateral noise: central modulation of olivocochlear efferents? Hear Res 256:1–10
Le Prell CG, Dell S, Hensley B, Hall JW 3rd, Campbell KC, Antonelli PJ, Green GE, Miller JM, Guire K (2012) Digital music exposure reliably induces temporary threshold shift in normal-hearing human subjects. Ear Hear 33:e44–58
Møller AR (1984) 1 - Neurophysiological basis of the acoustic middle-ear reflex. In: The Acoustic Reflex (Silman S, ed), pp 1–34: Academic Press.
Nowotny M, Gummer AW (2006) Nanomechanics of the subtectorial space caused by electromechanics of cochlear outer hair cells. Proc Natl Acad Sci U S A 103:2120–2125
O’Beirne GA, Patuzzi RB (2007) Mathematical model of outer hair cell regulation including ion transport and cell motility. Hear Res 234:29–51
Patuzzi R (2011) Ion flow in cochlear hair cells and the regulation of hearing sensitivity. Hear Res 280:3–20
Patuzzi R, Wareing N (2002) Generation of transient tinnitus in humans using low-frequency tones and its mechanism. In: Patuzzi R (ed) Proceedings of the Seventh International Tinnitus Seminar. The University of Western Australia, Crawley, pp 16–24
Rabbitt RD, Brownell WE (2011) Efferent modulation of hair cell function. Curr Opin Otolaryngol Head Neck Surg 19:376–381
Rabbitt RD, Clifford S, Breneman KD, Farrell B, Brownell WE (2009) Power efficiency of outer hair cell somatic electromotility. PLoS Comput Biol 5, e1000444
Relkin EM, Sterns A, Azeredo W, Prieve BA, Woods CI (2005) Physiological mechanisms of onset adaptation and contralateral suppression of DPOAEs in the rat. J Assoc Res Otolaryngol 6:119–135
Salt AN (2004) Acute endolymphatic hydrops generated by exposure of the ear to nontraumatic low-frequency tones. J Assoc Res Otolaryngol : JARO 5:203–214
Salt AN, Lichtenhan JT, Gill RM, Hartsock JJ (2013) Large endolymphatic potentials from low-frequency and infrasonic tones in the guinea pig. J Acoust Soc Am 133:1561–1571
Scholz G, Hirschfelder A, Marquardt T, Hensel J, Mrowinski D (1999) Low-frequency modulation of the 2f1-f2 distortion product otoacoustic emissions in the human ear. Hear Res 130:189–196
Sridhar TS, Brown MC, Sewell WF (1997) Unique postsynaptic signaling at the hair cell efferent synapse permits calcium to evoke changes on two time scales. J Neurosci 17:428–437
Warr WB, Guinan JJ, White JS (1986) Organization of the efferent fibers: the lateral and medial olivocochlear systems. In: Altschuler RA, Hoffman DW, Bobbin RP (eds) Neurobiology of hearing: cochlea. Raven Press, New York, pp 333–348
Wilson RH, Shanks JE, Lilly DJ (1984) 10—acoustic-reflex adaptation. In: The Acoustic Reflex (Silman S, ed), pp 329–386: Academic Press.
Zhao W, Dhar S (2010) The effect of contralateral acoustic stimulation on spontaneous otoacoustic emissions. JARO 11:53–67
Zhao W, Dhar S (2011) Fast and slow effects of medial olivocochlear efferent activity in humans. PLoS One 6, e18725
Acknowledgments
This work was funded by a grant (01EO1401) from the German Ministry of Science and Education to the German Center for Vertigo and Balance Disorders (IFB), project TR-F9 to K.K., R.G., E.K. and M.D., and a grant from the BCCN Munich, TP7, B3 Wiegrebe to L.W. The authors wish to acknowledge the contributions of David Laubender, who was involved in carrying out some of the experimental procedures.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Kugler, K., Wiegrebe, L., Gürkov, R. et al. Concurrent Acoustic Activation of the Medial Olivocochlear System Modifies the After-Effects of Intense Low-Frequency Sound on the Human Inner Ear. JARO 16, 713–725 (2015). https://doi.org/10.1007/s10162-015-0538-4
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10162-015-0538-4