Elsevier

Hearing Research

Volume 140, Issues 1–2, February 2000, Pages 189-201
Hearing Research

Middle ear influence on otoacoustic emissions. I: Noninvasive investigation of the human transmission apparatus and comparison with model results

https://doi.org/10.1016/S0378-5955(99)00201-4Get rights and content

Abstract

Evoked otoacoustic emissions (EOAEs) are generated within the cochlea in response to external sounds, and they can be acoustically detected in the external auditory meatus after backward propagation through the middle ear. In addition to being used to probe the cochlear mechanisms, they are expected to be sensitive to minute changes in middle ear impedance. Systematic measurements of the changes in the vectorial components of EOAEs were carried out after various manipulations of the human middle ear in order to characterize the influence of stiffness and inertia of the stapes and tympanic-membrane systems. For this purpose, stapedius muscle contractions were elicited by high-level contralateral sound, controlled changes in middle ear pressure (range ±100 daPa) were produced and the tympanic membrane was loaded with water droplets. A computer model of the middle ear network was implemented using a standard lumped-element electric analog of the middle ear (Zwislocki’s model). Forward and backward transmission changes were simulated and model predictions were compared to experimental data. Apart from the case of positive middle ear pressures, a close qualitative correspondence was found between model and real-ear results. Each of the effects was characterized by a unique pattern of phase and magnitude changes as a function of frequency, in relation to the mechanical characteristics of the involved subsystem (i.e. stapes stiffness, tympanic-membrane stiffness or mass) and its resonance properties. Owing to their high sensitivity, EOAEs could be helpful for an accurate individual multifrequency analysis of middle ear impedance by comparisons under rest and test conditions.

Introduction

Evoked otoacoustic emissions (EOAEs) have widespread laboratory and clinical interest as noninvasive probes of cochlear function. Transient-evoked otoacoustic emissions (TEOAEs) are generated by brief stimuli (Kemp, 1978), whereas distortion-product otoacoustic emissions (DPOAEs; Kemp, 1979a) are observed when the cochlea is stimulated by a pair of pure tones at frequencies f1 and f2: combination tones, e.g. at 2f1−f2, appear as a result of cochlear nonlinearities. For EOAEs to be found in the external ear canal, the cellular mechanisms ensuring high sensitivity and tuning must be operating (Brownell, 1990). In addition, sound conduction through the middle ear has to be close to normal, both in the forward direction for the stimuli to reach the cochlea, and in the reverse direction for the cochlear responses to be detected in the ear canal. It is well-acknowledged that EOAEs can hardly be detected if significant conductive hearing loss is present (Owens et al., 1992, Amedee, 1995). Physiological transmission changes may also alter EOAE characteristics even though hearing sensitivity remains within normal limits (posture: Wilson, 1980, Antonelli and Grandori, 1986; pressure gradient at the tympanic membrane: Veuillet et al., 1992, Naeve et al., 1992, Hauser et al., 1993, Osterhammel et al., 1993, Trine et al., 1993, Plinkert et al., 1994, Richter et al., 1994 in man, Zhang and Abbas, 1997 in guinea pig; middle ear muscle contractions: Whitehead et al., 1991, Burns et al., 1993 in man; mass of tympanic membrane: Wiederhold, 1990 in cat).

As the influence of middle ear characteristics can be confounding in experiments involving measurements of the fine structure of otoacoustic emissions, it would be very important to find unambiguous criteria for separating middle from inner ear effects. This requires full characterization of the influence of the middle ear upon EOAEs. A stiffness increase is expected to bear a typical signature, with the induced change being maximum below the resonance frequency of the involved system, i.e. in the frequency interval where it is stiffness-driven, whereas it tends to disappear above resonance frequency, in contrast with mass effects which should be dominant at higher frequencies. The trends reported by Hauser et al. (1993) for tympanic-membrane stiffness in man, and Wiederhold (1990) for tympanic-membrane mass in cat, are consistent with the previous contention. However, no systematic attempt has been made so far to fit EOAE experimental data with theoretical models of the middle ear. Lumped-element models of the middle ear (Zwislocki, 1962, Lutman and Martin, 1979, Kringlebotn, 1988, Shera and Zweig, 1992) are thought to be reliable as long as sound propagation can be neglected, i.e. at frequencies below 3–4 kHz. They can be applied to computing EOAE changes after modifications of the various middle ear structures.

The goal of the present work was to use noninvasive EOAE measurements in man to document the effects of several middle ear parameters varying within their physiological range. Reflex contractions of the stapedius muscle were induced by high-level noise in the contralateral ear (20 dB above reflex threshold). Variations of air pressure in the middle ear (range ±100 daPa) served to alter tympanic-membrane stiffness. Last, the tympanic membrane was weighted with a 20 μl droplet of water in order to contrast inertia vs. stiffness influences on EOAEs. Because they can be freely sampled over a broad interval by varying f2 and f1, DPOAEs were preferred to TEOAEs to monitor the changes of middle ear impedance. The level and phase shifts of DPOAEs with respect to control conditions were measured between 0.5 and 3–4 kHz. The model of Zwislocki, modified by Lutman and Martin (1979), was implemented in a simple program to compute the forward and reverse middle ear transfer functions under control and test conditions, with the first-order approximation that the cochlear sources of DPOAEs remained unaltered (model of Kemp, 1980). The computed shifts were plotted against frequency using average parameter values, then, attempts were made to optimize their fit with the experimental data. The companion work (Büki et al., 2000) applied the same methods to human subjects submitted to posture changes, in order to analyze the complex changes in sound transmission that occur with body tilt and identify their mechanisms.

Section snippets

Subjects

Healthy adults, aged from 24 to 39 years, were tested in the course of a routine ENT visit. They had no history of ear disease and their otoscopy, pure-tone audiogram (octave frequencies from 0.125 to 8 kHz) and tympanometry were normal. In particular, all hearing thresholds were better than 15 dB HL. Eight subjects were included for all tests and six additional subjects participated in test 4.2 only (see Section 4). One ear per subject was taken into account, that with the largest DPOAE

Control DPOAE recordings

The DPOAE levels were between 0 and 15 dB SPL for primary frequencies below 1.5 kHz and between 10 and −5 dB for higher frequencies, with a mean noise floor between −7 and −15 dB SPL below 1.5 kHz, and less than −15 dB SPL above 1.5 kHz. The required signal-to-noise ratio of 12 dB was reached in all subjects for at least 90% of the frequency samples. The slopes S of DPOAE growth functions, for primary levels around 60 and 70 dB, ranged between 0.3 and 0.9, depending on the ear and the test

Discussion

The effects of conductive hearing impairment on otoacoustic emissions are well-acknowledged (Owens et al., 1992, Amedee, 1995). Even when the middle ear departs only slightly from its optimal transmission, in the absence of any detectable conductive hearing loss, otoacoustic emissions can reflect middle ear impedance changes. It is important to document these changes with regard to the clinical implications of a possible interaction of middle ear status with inner ear energy release. For

Perspectives

Another factor that may influence middle ear transmission has been pinpointed recently using otoacoustic emissions. Büki et al. (1996) reported systematic frequency-dependent effects of posture (in normal subjects) and intracranial pressure (in neurosurgical patients) on the phase of TEOAEs. This issue bears important clinical applications, since most available methods to monitor intracranial pressure in neurosurgical patients are invasive, except the tympanic-membrane displacement technique of

Acknowledgements

This work was funded by grant 99023 from Apape (PAI Balaton) to P.A. and B.B., and grants INSERM/NWO 1994 and OTKA T022194. The comments of John Rosowski are gratefully acknowledged.

References (47)

  • M.L. Whitehead et al.

    Effects of the crossed acoustic reflex on distortion-product otoacoustic emissions in awake rabbits

    Hear. Res.

    (1991)
  • J.P. Wilson

    Evidence for a cochlear origin for acoustic re-emissions, threshold fine structure and tonal tinnitus

    Hear. Res.

    (1980)
  • E. Zwicker

    On the influence of acoustical probe impedance on evoked otoacoustic emissions

    Hear. Res.

    (1990)
  • Allen, J.B., 1990. Cubedis user manual, Bell...
  • R.G. Amedee

    The effects of chronic otitis media with effusion on the measurements of transiently evoked otoacoustic emissions

    Laryngoscope

    (1995)
  • A. Antonelli et al.

    Long term stability, influence of the head position and modelling considerations for evoked otoacoustic emissions

    Scand. Audiol. Suppl.

    (1986)
  • E. Borg

    A quantitative study of the effect of the acoustic stapedius reflex on sound transmission through the middle ear of man

    Acta Otolaryngol. (Stockh.)

    (1968)
  • Borg, E., Counter, S.A., Rosler, G., 1984. Theories of middle ear muscle function. In: Silman, S. (Ed.), The Acoustic...
  • W.E. Brownell

    Outer hair cell electromotility and otoacoustic emissions

    Ear Hear.

    (1990)
  • L. Collet et al.

    Effect of contralateral auditory stimuli on active cochlear micro-mechanical properties in human subjects

    Hear. Res.

    (1990)
  • Guinan, J.J., Jr., 1996. Physiology of olivocochlear efferents. In: Dallos, P., Popper, A.N., Fay, R.R. (Eds.), The...
  • K.B. Hüttenbrink

    The mechanics of the middle ear at static air pressures

    Acta Otolaryngol. (Stockh.) Suppl.

    (1988)
  • D.T. Kemp

    Stimulated acoustic emissions from within the human auditory system

    J. Acoust. Soc. Am.

    (1978)
  • Cited by (64)

    • Wideband tympanometry patterns in relation to intracranial pressure

      2021, Hearing Research
      Citation Excerpt :

      A second answer stems from graphs of aEA. The effect of an isolated increase in annular-ligament stiffness due to increased ICP should be a reduction in aEA in the frequency interval where stiffness dominates the mechanical responses, thus below 1 kHz (Avan et al., 2000; Lutman and Martin, 1979). Such an effect was visible in some ears (Fig. 1a and b) but not all (Fig. 1c and d).

    • Abnormal fast fluctuations of electrocochleography and otoacoustic emissions in Menière's disease

      2015, Hearing Research
      Citation Excerpt :

      In normal ears, body tilt induces a moderate phase shift of the 2f1-f2 DPOAE, about 10° on average (Avan et al., 2011). In supine posture, the mildly increased intracranial pressure in reference to the upright position gets transmitted to cochlear fluids through the cochlear aqueduct and pushes on the stapes footplate, thus increasing the mechanical stiffness of the interface between middle and inner ear, which accounts for the phase shift (Avan et al., 2000). Invasive manipulations of intracranial pressure in neurosurgical environments confirm a 10° OAE phase shift at low frequencies for a 60-mm water pressure increase (Büki et al., 1996), a reasonable estimate of what body tilt might produce.

    View all citing articles on Scopus
    1

    Current address: Academic Medical Centre, University of Amsterdam, The Netherlands.

    View full text