Kugler, et al Royal Society, Low Frequency Sound Affects Active Micromechanics in the Human Inner Ear


August 18, 2014

Kathrin Kugler1,3, Lutz Wiegrebe3, Benedikt Grothe3, Manfred Kössl4, Robert Gürkov1,2, Eike Krause1,2 and Markus Drexl1,2

1 German Center for Vertigo and Balance Disorders (IFB), and
2 Department of Otorhinolaryngology, Head and Neck Surgery, Grosshadern Medical Centre, University of Munich, 81377 Munich, Germany
3 Department Biology II, University of Munich, 82152 Martinsried, Germany
4 Institute for Cell Biology and Neuroscience, Johann Wolfgang Goethe University, 60438 Frankfurt/ Main, Germany


 1. Summary

Noise-induced hearing loss is one of the most common auditory pathologies, resulting from overstimulation of the human cochlea, an exquisitely sensitive micromechanical device. At very low frequencies (less than 250 Hz), however, the sensitivity of human hearing, and therefore the perceived loudness is poor. The perceived loudness is mediated by the inner hair cells of the cochlea which are driven very inadequately at low frequencies. To assess the impact of low-frequency (LF) sound, we exploited a by-product of the active amplification of sound outer hair cells (OHCs) perform, so-called spontaneous otoacoustic emissions. These are faint sounds produced by the inner ear that can be used to detect changes of cochlear physiology. We show that a short exposure to perceptually unobtrusive, LF sounds significantly affects OHCs: a 90 s, 80 dB(A) LF sound induced slow, concordant and positively correlated frequency and level oscillations of spontaneous otoacoustic emissions that lasted for about 2 min after LF sound offset. LF sounds, contrary to their unobtrusive perception, strongly stimulate the human cochlea and affect amplification processes in the most sensitive and important frequency range of human hearing.

2. Introduction

For decades, low-frequency (LF) sound, i.e. sound with frequencies lower than 250 Hz, has been considered to largely bypass the inner ear even at intense levels, simply because human hearing thresholds for frequencies below 250 Hz are relatively high. Recent evidence from animal models shows that physiological cochlear responses can be elicited with very LF and infrasound, where hearing in most mammals is poor or non-existent. No data for human subjects are available, but, considering the higher sensitivity of humans for LF sounds compared with most mammals, similar results can be expected.

Perceptual thresholds essentially reflect the sensitivity of inner hair cells (IHCs), one class of cochlear sensory cells on the basilar membrane, which are functionally coupled to inner ear fluids. IHCs are therefore sensitive to the velocity of sound-driven basilar-membrane movements, which decreases with decreasing frequency of the sound stimulus. Outer hair cells (OHCs), by contrast, are mechanically linked to both the basilar membrane and the overlying tectorial membrane, and are responsible for active cochlear amplification of sound.

OHCs are sensitive to the sound-driven displacement of the basilar membrane, which does not decrease with decreasing frequency. Thus, OHCs are more sensitive to LF sound than IHCs. In addition, at LFs, the transfer characteristics of the middle ear and shunting at the helicotrema, a small opening connecting scala media and scala vestibuli of the cochlea, attenuate input to both IHCs and OHCs.

While IHCs are contacted by afferent terminals of the auditory nerve and convey acoustic information to the auditory brain, the OHCs’ main task is to detect and mechanically amplify sound waves by fast changes of the length of their cell body. This so-called cochlear amplifier actively generates mechanical energy which is fed back into the cochlear travelling wave and ensures the exquisite sensitivity and wide dynamic range of mammalian hearing. Active cochlear amplification leads, as a by-product, to the formation of otoacoustic emissions, sounds generated in the inner ear which can be recorded in the ear canal. In humans, non-invasive recordings of different classes of sound-evoked otoacoustic emissions (EOAEs) allow indirect access to OHC function. While EOAE measurements following LF sound stimulation indicate LF-induced changes in cochlear and especially OHC physiology, they cannot probe the cochlea in its original state, as the external sound stimulation required already changes cochlear properties. Spontaneous otoacoustic emissions (SOAEs) are narrowband acoustic signals which are spontaneously emitted by the inner ear in the absence of acoustic stimulation and can be recorded in the ear canal with a sensitive microphone. They are a by-product of active biophysical amplification by OHCs in the cochlea. In humans, they persist over years and are relatively stable in both frequency and level under normal physiological conditions. Two main theories about the mechanisms generating SOAEs exist and while fundamentally different in their reasoning, they both share active OHCs as necessary elements. Therefore, and because they do not require external stimulation, SOAEs allow for the most direct, non-invasive access to OHC function. A single study reports changes of two SOAEs after LF exposure. Here, we use SOAE measurements for a comprehensive characterization of LF-induced changes of cochlear physiology and active sound amplification. Specifically, we monitored the sound level and frequency of SOAEs before and after the exposure to a 90 s LF sinusoid with 30 Hz and a level of 80 dB(A). Both the sound level and especially the exposure duration used in this study are well below the limits for noise exposures in normal working environments.

6. Conclusion

The results of this study clearly indicate that there is a pronounced discrepancy between the unobtrusive perception of LF sound, reflected in their low sensation levels and the physiological responses of the cochlea following the LF sound exposure. To the best of our knowledge, perception has been the only measure available in humans to assess inner ear responses to very LF sound, but, as the current data show, severely underestimates cochlear and, especially OHC, sensitivity. Direct quantifications of inner ear active amplification, as measured in this study, are much better suited to assess the risk potential of LF sound.

Ethics statement. The ethics committee of the University Hospital of the Ludwig-Maximilians University Munich, Germany, in agreement with the Code of Ethics of the World Medical Association (Declaration of Helsinki) for experiments involving humans, approved the procedures and all subjects gave their written informed consent.

Data accessibility. The raw data supporting this study can be accessed under doi:10.6084/m9.figshare.1136017.

Funding statement. This work was supported by a grant from the German Ministry of Science and Education to the German Center for Vertigo and Balance Disorders (IFB), project TR-F9 to R.G., E.K. and M.D., and a grant from the BCCN Munich, TP7, B3 Wiegrebe to L.W.

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Original Research Paper available here: http://rsos.royalsocietypublishing.org/content/1/2/140166