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Sinusoidal amplitude modulation alters contralateral noise suppression of evoked otoacoustic emissions in humans
Pergamon PII:
Neuroscience Vol. 91, No. 1, pp. 133–138, 1999 Copyright 䉷 1999 IBRO. Published by Elsevier Science Ltd Printed in Great Britain. All rights reserved 0306-4522/99 $20.00+0.00 S0306-4522(98)00608-3
SINUSOIDAL AMPLITUDE MODULATION ALTERS CONTRALATERAL NOISE SUPPRESSION OF EVOKED OTOACOUSTIC EMISSIONS IN HUMANS S. MAISON,*† C. MICHEYL*‡ and L. COLLET* *Universite´ Claude Bernard Lyon 1, Laboratoire “Neurosciences and Syste`mes Sensoriels”, UPRESA CNRS 5020, Lyon, France ‡Applied Psychology Unit, Medical Research Council and Department of Experimental Psychology, University of Cambridge, Cambridge, U.K.
Abstract—It is well established that low-level broad band noise can elicit an amplitude decrease in evoked otoacoustic emissions recorded in the opposite ear. However, the influence of the temporal characteristics of the contralateral stimulus on this effect remains largely unknown. In the present study, otoacoustic emissions evoked by 60 dB SPL clicks were recorded in 19 normal-hearing subjects using the Otodynamics ILO88, successively in absence and presence of a contralateral noise that was either steady or modulated sinusoidally in amplitude at different depths (from 25% to 100% in 25 point steps) and rates (from 50 Hz to 800 Hz in half-octave steps). The energy was kept constant whatever the modulation depth. The results showed that the evoked otoacoustic-emission attenuation effect induced by contralateral stimulation varied depending on the modulation depth and frequency of the contralateral amplitudemodulated noise. The largest suppression effect was observed at the 100 Hz modulation frequency and the 100% modulation depth. The 50 Hz modulation resulted in less suppression than with unmodulated noise. An interpretation of these results in terms of the influence of temporal amplitude fluctuations falling within a certain range on medial olivocochlear bundle activity is discussed. 䉷 1999 IBRO. Published by Elsevier Science Ltd. Key words: medial olivocochlear system, outer hair cells, cochlear micromechanics, amplitude modulation, human.
Since Rasmussen’s description 26 of the cochlear efferent system in 1946, anterograde transport techniques using radioactively labelled amino acids have distinguished two populations of olivocochlear efferent fibres. 33 Firstly, the lateral olivocochlear neurons which project mainly ipsilaterally on to cochlear afferent neuron dendrites close to the inner hair cells, and, secondly, the medial olivocochlear neurons originating from the medial nuclei of the superior olivary complex, and projecting mainly on to the contralateral organ of Corti, where they synapse at the base of the outer hair cells (OHCs). Electrophysiological studies have sought to demonstrate involvement of the medial olivocochlear bundle (MOCB) in the suppression of the auditory nerve response to acoustic stimulation, obtained by electrical stimulation to the floor of the fourth ventricle. 10 Similar suppressions have †To whom correspondence should be addressed. Abbreviations: AM, amplitude modulation or amplitude modulated; CAP, compound action potential; CAS, contralateral acoustic stimulation; EOAE, evoked otoacoustic emission; MD, modulation depth; MF, modulation frequency; MOCB, medial olivocochlear bundle; OAE, otoacoustic emission; OHC, outer hair cell. 133
been shown for endocochlear potential and for the discharge rate of cochlear afferents. 6,12,13 It has been shown that acoustic stimulation of the contralateral ear can activate the MOCB 4,6 and modify ipsilateral activity in auditory fibres in response to acoustic stimulation. In particular, Folsom and Owsley 7 demonstrated that contralateral sound stimulation could induce a decrease in compound action potential (CAP) amplitude in humans. The MOCB establishes basolateral synapses with cochlear OHCs. It has been shown that contralateral acoustic stimulation (CAS) can, via MOCB fibres, modify the sounds generated by fast OHC contractions, known as otoacoustic emissions (OAEs). Mountain 23 and Siegel and Kim 27 stimulated efferent fibres and observed a simultaneous decrease in distortion product OAE amplitude. Puel and Rebillard 25 showed the same effect, using a contralateral broad band noise in guinea-pigs, and found suppression of the effect after section of the floor of the fourth ventricle. Likewise, in humans, numerous studies 1,5,30,31 have demonstrated a decrease in evoked OAE (EOAE) amplitude, using contralateral broad band noises, narrow band noises or clicks at low contralateral stimulus intensity (30 dB SL). Because this contralateral EOAE
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amplitude attenuation effect is already significant at such low contralateral stimulus intensity, it cannot be explained by acoustic crosstalk. Moreover, although a possible involvement of the middle ear cannot be completely excluded at such levels, the contralateral suppression effect cannot be entirely due to a middle ear modification because it is still found in subjects with unilateral loss of the stapedial reflex. 31 Moreover, the middle ear could not explain the frequency specificity found in the contralateral stimulation effect. 17 More recently, it has been demonstrated that the effect is absent or dramatically reduced in patients whose MOCB had been sectioned during vestibular neurectomy 11 as the olivocochlear bundle exits the brain with the vestibular division of the vestibulo-cochlear nerve. 26 Studies performed so far have indicated that, while a significant contralateral EOAE amplitude suppression effect can be observed with intensities as low as 30 dB SL when the CAS consists of broad band noises or narrow band noises, no significant contralateral EOAE suppression is obtained below about 60 dB SL for a pure-tone CAS. 1,18,30 However, at such a high stimulus intensity, mechanisms other than MOCB action, such as those mentioned above, may well be responsible for the effect. In that case, pure tones would appear to be less effective, or even not effective at all, in inducing MOCB-mediated contralateral EOAE attenuation. These effects of contralateral tones on EOAEs contrast with the effects observed on CAP which reveal substantial amounts of suppression at frequencies below about 1.5 kHz using contralateral pure tones of relatively low level, around 25–30 dB SPL. 17 The exact reason for the lesser contralateral EOAE suppression effectiveness of pure tones as compared to noises of the same sensation level, implying that other CAS characteristics than sound level are determinant in the contralateral EOAE attenuation effect, remains unclear at present. One possible factor in this difference has been recently revealed by the finding that significant contralateral EOAE attenuation can be elicited by low-intensity tones when these are amplitude modulated 18 or frequency modulated. 19 This result suggests that rapid temporal fluctuations which are naturally present in noises but absent in steady tones contribute to enhance the contralateral attenuation effect, thereby explaining why this effect is larger with the former than with the latter. However, because amplitude modulation alters the spectrum of tones as well as their temporal envelope, it remains unclear whether the effect of amplitude modulation observed in this study is due to amplitude fluctuations in the temporal envelope of the contralateral stimulus per se or whether it is due to the presence of side bands surrounding the carrierfrequency peak in the spectrum. In other words, the question as to whether temporal amplitude fluctuations are a factor in the contralateral EOAE attenuation effect still remains unanswered. To further test
the hypothesis that amplitude modulation plays a role per se in the contralateral attenuation effect via temporal mechanisms, through the fluctuations it induces in the contralateral stimulus envelope, the present study compared contralateral EOAE attenuation effects elicited by modulated vs unmodulated white noise. In this study, as in many others, 3,24,32 advantage was taken of the fact that the long-term power spectrum of white noise, contrary to that of tones, is unaffected by temporal amplitude modulation. EXPERIMENTAL PROCEDURES
Subjects The present study involved 19 subjects (nine males, 10 females; 22–39 years old; mean age 28 years, S.D. 7) with no history of auditory pathology and normal audiometric functions [thresholds of 10 dB hearing level (HL) or better between 250 Hz and 8 000 Hz at octave intervals on pure tone audiogram]. Tonal audiometry and tympanometry were conducted in a soundproof room using a Madsen DA III audiometer and an Amplaid 702 impedancemeter, respectively. Evoked otoacoustic emission recording EOAEs were recorded and analysed according to the methodology proposed by Bray and Kemp. 2 Stimulus was presented with a BP 1712 earphone and EOAEs were recorded with a Knowles 1843 microphone, both embedded in a plastic ear plug. Stimulus presentation, data recording and averaging were carried out using the Otodynamics ILO88 software and hardware. The stimulus was a 1 kHz tone pip (one cycle rise-and-fall, two cycles plateau). The stimulus presentation rate was 50 Hz. The linear cochlear echo method, with a combination of four acoustic impulses identical in size and polarity, was used: meatal and middle ear echoes are not self-cancelling in this condition, and their durations increase with stimulus level; such ringing components were eliminated by using low intrameatal stimulation. The stimulus level was 60 ^ 3 dB SPL, measured in the ear canal. To minimize stimulus artifact, EOAE analysis was windowed so as to truncate the first 6 ms of the response to zero. The analysis window was 20 ms; 512 responses were averaged. A pass band of 500–6 000 Hz was employed. EOAE amplitude was computed from the whole response in a time window of 6–20 ms. Contralateral acoustic stimulation The CAS was either an unmodulated noise or an amplitude modulated (AM) noise, generated using a 16-bit digital-to-analogue (D/A) converter at a sampling rate of 44.1 kHz and delivered through a TDH 39 earphone (bandwidth: 50–8000 Hz). The D/A card was installed on a IBMcompatible computer. The formula used for the generation of the modulated stimulus was: s t k:1 ⫹ m:cos 2pfm t:c t; where c(t) represents a white noise carrier, m and fm are, respectively, the modulation depth—between 0 and 1—and frequency (in Hz), and k is a correction factor applied to maintain the energy of the modulated noise equal to that of the unmodulated noise; this correction factor was given by: p k 1= 1 ⫹ m2 =2: In each subject, the level of the contralateral noise was set at 40 dB SL, i.e. 40 dB above the absolute threshold of this
Medial olivocochlear system activated by AM noise
noise measured beforehand in this subject. The mean absolute threshold across listeners was 6.6 dB SPL—overall level—(S.D. 4.0 dB). Procedure AM noise effect on EOAEs was studied according to two parameters: modulation depth (MD) and modulation frequency (MF). Effect of modulation depth. Subjects received a contralateral noise (broad band noise: 0–20,000 Hz) modulated at 100 Hz and with depth varying between 0 (unmodulated) and 100% by 25 point steps. Contralateral intensity level was 40 dB SL (i.e. 46.6 ^ 4.0 dB SPL). Effect of modulation frequency. Subjects followed the above procedure with a contralateral noise modulated with a depth of 100% and with frequency varying between 50 and 800 Hz by half-octave steps. Statistics Statistical analysis was performed using Sigmastat 䉸 software (version 1.02) and included analysis of variance for repeated measures (RMANOVA) in their non-parametric version (i.e. Friedman RMANOVA) and multiple comparisons tests (Student’s Newman–Keuls method). RESULTS
Figure 1 shows EOAE amplitudes recorded from one representative subject without and with contralateral stimulations described in Experimental Procedures. It should first be noted that all the contralateral noises (unmodulated and modulated) used in this experiment induced a statistically significant suppression of EOAE amplitude compared to that found without contralateral stimulation (paired ttest, P ⬍ 0.001). The main result of the present study is presented in Fig. 2. While an unmodulated noise (i.e. 0% MD) induced a significant EOAE amplitude suppression, an AM noise of the same energy induced a significantly greater EOAE amplitude suppression: P 0.006, for unmodulated and 100%-modulated noise. For MD, ANOVA for repeated measures showed a statistically significant effect (Friedman RMANOVA: x 2 11.0, P 0.027). In spite of a regular increase in EOAE amplitude suppression with MD (i.e. EOAE amplitude suppression: 0% ⫺ 0.85 ^ 0.12, 25% ⫺ 0.88 ^ 0.15, 50% ⫺ 0.92 ^ 0.1, 75% ⫺ 0.91 ^ 0.15 and 100% ⫺ 1.11 ^ 0.14), the 100%-MD AM noise was the only contralateral stimulus to induce a significantly greater suppression of EOAE amplitude compared with unmodulated noise (pairwise multiple comparison, P ⬍ 0.05). The data shown in Fig. 3 describe the variation in attenuation as a function of contralateral MF. Friedman RMANOVA showed a statistically significant MF effect from 50 to 800 Hz by half-octave steps (x 2 22.7, P 0.004). EOAE amplitude was reduced significantly for MFs ranging in half-octave
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steps from 50 to 800 Hz for an MD of 100%. For this MD, the greatest increase in contralateral EOAE-amplitude suppression was obtained for the 100 Hz MF. The contralateral EOAE suppression effect obtained in presence of a 100 Hz, 100% AM noise proved significantly different (pairwise multiple comparison, P ⬍ 0.05) from the EOAE suppression elicited by any of the other contralateral stimuli used in this study. At the 50 Hz MF, significantly less suppression than with unmodulated noise was observed (paired t-test, P 0.015). DISCUSSION
The results of the present study indicate that larger contralateral EOAE amplitude attenuation effects can be obtained with modulated rather than with unmodulated noise as contralateral stimulus under a given range of modulation conditions, the contralateral EOAE attenuation effect elicited by AM noise being dependent on the AM parameters. Regarding the first parameter, AM rate or frequency, the largest suppression effect was obtained with a contralateral noise modulated at a frequency of 100 Hz. Only at this modulation rate did the AM noise elicit a contralateral EOAE attenuation effect larger than that produced by unmodulated noise. This finding of 100 Hz as a preferential modulation rate for the contralateral EOAE attenuation effect is in agreement with the results of a previous study in which the largest contralateral EOAE attenuation effects were elicited by AM tones at a MF of 100 Hz. 18 However, the tuning to amplitude-modulation rate observed in our previous study was broader than the tuning observed in the present study in the sense that, at least at the largest modulation depths, several modulation rates in the 50–400 Hz range other than 100 Hz also elicited larger contralateral EOAE suppression than in the unmodulated condition. This difference between the two studies is most probably due to a difference in the carrier waveform. Whereas the steady broadband noise used in the present study elicited contralateral suppression, the pure tones used in the earlier study did not. Therefore, it is conceivable that the effects of amplitude modulation on contralateral suppression are larger when the steady contralateral stimulus used as a reference produces none than when this stimulus already elicits a substantial amount of baseline suppression. Assuming that the contralateral EOAE-amplitude suppression effects are underlaid by activation of the MOCB, as is strongly suggested by data reviewed in the Introduction, the origin of the selectivity to AM rate observed in the present and our previous studies may be sought in the physiology of MOCB neurons. Interestingly, the only results available in the literature on the coding
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Fig. 1. Examples of differences in EOAE traces induced by contralateral noises with different modulation depths and rates in one subject (female, 25 years old). The top panel shows the EOAE trace recorded without contralateral stimulation. The left-hand column shows the differences in EOAE traces induced by contralateral noise amplitude modulated at a rate of 100 Hz and at different depths, as computed by subtracting the EOAE trace recorded in presence of the noise from the reference EOAE trace shown at the top. The right-hand column shows the differences in EOAE trace induced by contralateral noise amplitude modulated at a depth of 100% and at different rates.
of AM by MOCB neurons 14 indicate two main types of efferent neurons: one—most units—exhibiting modulation-transfer functions with a peak around 100 Hz, and a second—24% of the units—showing a broad low-frequency peak. These data are grossly consistent with our findings but further information on the coding of AM by MOCB neurons is required before the neurophysiological mechanisms underlying these findings can be discussed in more detail. An intriguing result of the present study lies in the fact that the 50 Hz AM noise elicited
less suppression than unmodulated noise. An interpretation of this observation is that, owing to bandpass filtering by the cochlea, the peripheral auditory filter outputs in response to the unmodulated noise already exhibited some degree of AM at rates around 100 Hz—as determined by the 3 dB bandwidth of filters having their center frequencies around 1 kHz—and that these fluctuations, which are the most efficient in eliciting contralateral suppression, were disrupted by the superimposition of an extrinsic AM at a lower rate such as 50 Hz.
Medial olivocochlear system activated by AM noise
Fig. 2. EOAE amplitude suppression as a function of contralateral MD. EOAEs were elicited by a 1 kHz tone pip set at 60 dB SPL. EOAEs were recorded in 19 subjects without (EOAE relative amplitude 0 dB) and with a broad band noise modulated at a frequency of 100 Hz with a depth varying from 0% (unmodulated) to 100% by 25 point steps. Bars indicate standard errors of the EOAEs.
Fig. 3. EOAE amplitude suppression as a function of contralateral MF. EOAEs were elicited by a 1 kHz tone pip set at 60 dB SPL. EOAEs were recorded in 19 subjects without (EOAE relative amplitude 0 dB) and with a broad band noise modulated at a depth of 100% with a frequency varying from 50 Hz to 800 Hz by half-octave steps. Bars indicate standard errors of the EOAEs.
Considering the second AM parameter, namely, AM depth, the results indicate that the deeper the AM applied, the larger the contralateral EOAE attenuation. However, although an increase in EOAE amplitude suppression was found for 25, 50 and 75% MDs, only the 100% MD elicited an EOAE attenuation effect significantly larger than did 0% modulation. In our previous study using AM tones, 18 significant contralateral EOAE attenuation was obtained from modulation of about 37%. Once again, however, a possible reason for the fact that only the largest MD proved significant is that the broad band noises used as contralateral stimuli already exerted a suppression effect, even when unmodulated.
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Because the noises used in this study had very broad bandwidths, the difference observed between the EOAE attenuation effects elicited by modulated and unmodulated stimuli cannot be imputed to alterations in the long-term spectrum of these stimuli. Moreover, because the energy of the contralateral stimulus was held constant independently of the depth of modulation, and was thus equal in unmodulated and modulated conditions, the observed difference cannot be imputed to differences in the overall energy of the contralateral stimulus. The possibility that the observed difference between modulated and unmodulated stimuli is due to the larger maximum instantaneous amplitude in the modulated stimulus cannot be completely ruled out on the basis of the present results. However, several arguments argue against this interpretation. Firstly, the results of previous studies show that whilst steady tones start to elicit significant contralateral suppression at levels around 60 dB SL, 31 AM tones already do so at levels as low as 30 dB SL. 18 A simple calculation indicates that the maximum increase in peak level produced by applying the AM together with the correction factor was about 4 dB. Consequently, even if one assumes that the increase in peak level produced by the modulation is equivalent to an increase in overall level, the observed necessity of raising the level of an unmodulated contralateral stimulus by more than 20 dB in order for it to have a similar suppressive effect than an unmodulated stimulus cannot be accounted for. This, however, might hold only for pure tones, not for noise. Given the incompleteness of neurophysiological events, the present results do not allow us to determine the exact mechanisms by which temporal amplitude fluctuations can elicit variations in contralateral EOAE suppression. According to arguments raised in previous studies, 5,30 MOCB rather than middle ear functioning is the main mechanism of contralateral suppression effects. However, so far, strong arguments against middle ear effects have been obtained using unmodulated stimuli only and it therefore cannot be excluded that the suppressive effects observed more recently with AM stimuli involve middle-ear reflexes. CONCLUSIONS
Sounds in the natural environment are rarely steady. Biological signals such as animal or human vocalizations present temporal amplitude and frequency fluctuations. 28 The results of the present study, indicating variations in MOCB activity in response to temporal amplitude fluctuations with rates lying within the periodicity-pitch range, with a maximum around the human-voice fundamentalfrequency, suggest the possibility of an involvement of this efferent system in the processing of ecological signals. 14 From this point of view, these
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results add a new dimension to the notion of the role of the auditory efferents in hearing suggested in recent studies in both animals 15,16,20,34 and humans. 21,22
Acknowledgements—The authors are grateful to Professor John D. Durrant and to an anonymous reviewer for their very helpful comments and suggestions on earlier versions of this manuscript.
REFERENCES
1. Berlin C. I., Hood L. J., Szabo P., Cecola R. P., Rigby P. and Jackson D. F. (1993) Contralateral suppression of non-linear click-evoked otoacoustic emissions. Hear. Res. 71, 1–11. 2. Bray P. and Kemp D. T. (1987) An advanced cochlear echo technique suitable for infant screening. Br. J. Audiol. 21, 191–204. 3. Burns E. M. and Viemeister N. F. (1976) Nonspectral pitch. J. Acoust. Soc. Am. 60, 863–868. 4. Cody A. R. and Johnstone B. M. (1982) Acoustically evoked activity of single efferent neurons in the guinea pig cochlea. J. Acoust. Soc. Am. 72, 280–282. 5. Collet L., Kemp D. T., Veuillet E., Duclaux R., Moulin A. and Morgon A. (1990) Effects of contralateral auditory stimuli on active cochlear micromechanical properties in human subjects. Hear. Res. 43, 251–262. 6. Fex J. (1962) Auditory nerve activity in centrifugal and centripetal cochlear fibers in cat. A study of a feedback system. Acta physiol. scand. 55, Suppl. 189, 1–72. 7. Folsom R. L. and Owsley R. M. (1985) N1 action potentials in humans: influence of simultaneous contralateral stimulation. Acta otolar. 421, Suppl. 77–85. 10. Galambos R. (1956) Suppression of auditory nerve activity by stimulation of efferent fibers to cochlea. J. Neurophysiol. 19, 424–437. 11. Giraud A. L., Collet L., Che´ry-Croze S., Magnan J. and Chays A. (1995) Evidence of a medial olivocochlear involvement in contralateral suppression of otoacoustic emissions in humans. Brain Res. 705, 15–23. 12. Guinan J. J. and Gifford M. L. (1988) Effects of electrical stimulation of efferent olivocochlear neurons on cat auditory-nerve fibers. I. Rate-level functions. Hear. Res. 33, 97–114. 13. Guinan J. J. and Gifford M. L. (1988) Effects of electrical stimulation of efferent olivocochlear neurons on cat auditory-nerve fibers. II. Spontaneous rate. Hear. Res. 33, 115–128. 14. Gummer M., Yates G. K. and Johnstone B. M. (1988) Modulation transfer function of efferent neurons in the guinea pig cochlea. Hear. Res. 36, 41–52. 15. Kawase T. and Liberman M. C. (1993) Antimasking effects of the olivocochlear reflex. I. Enhancement of compound action potentials to masked tones. J. Neurophysiol. 70, 2519–2532. 16. Liberman M. C. (1988) Responses properties of cochlear efferent neurons: monaural vs. binaural stimulation and the effects of noise. J. Neurophysiol. 60, 1779–1798. 17. Liberman M. C. (1989) Rapid assessment of sound-evoked olivocochlear feedback: suppression of compound action potentials by contralateral sound. Hear. Res. 39, 47–56. 18. Maison S., Micheyl C. and Collet L. (1997) Medial olivocochlear efferent system in humans studied with amplitude modulated tones. J. Neurophysiol. 77, 1759–1768. 19. Maison S., Micheyl C. and Collet L. (1998) Contralateral frequency-modulated tones suppress transient evoked otoacoustic emissions in humans. Hear. Res. 117, 114–118. 20. May B. J. and McQuone S. J. (1995) Effects of bilateral olivocochlear lesions on pure-tone intensity discrimination in cats. Audit. Neurosci. 1, 385–400. 21. Micheyl C. and Collet L. (1996) Involvement of the olivocochlear bundle in the detection of tones in noise. J. Acoust. Soc. Am. 3, 1604–1610. 22. Micheyl C., Khalfa S., Perrot X. and Collet L. (1997) Difference in auditory efferent activity between musicians and nonmusicians. NeuroReport (in press). 23. Mountain D. C. (1980) Changes in endolymphatic potential and crossed olivocochlear bundle stimulation alter cochlear mechanics. Science 210, 71–72. 24. Patterson R. D., Johnson D. D. and Milroy R. (1978) Amplitude modulated noise: the detection of modulation versus the detection of modulation rate. J. Acoust. Soc. Am. 52, 1904–1911. 25. Puel J. L. and Rebillard G. (1990) Effect of contralateral sound stimulation on the distortion product 2F1-F2: evidence that the medial efferent system is involved. J. Acoust. Soc. Am. 87, 1630–1635. 26. Rasmussen G. (1946) The olivary peduncle and other fibre projections of the superior olivary complex. J. comp. Neurol. 84, 141–219. 27. Siegel J. H. and Kim D. O. (1982) Efferent control of cochlear mechanics. Olivocochlear bundle stimulation affects cochlear biomechanical non-linearity. Hear. Res. 6, 172–182. 28. Stevens K. N. and House A. S. (1972) Speech perception. In Foundations of Modern Auditory Theory (ed. Tobias J. V.), Vol. II. Academic, New York. 30. Veuillet E., Collet L. and Duclaux R. (1991) Effect of contralateral auditory stimulation on active cochlear micromechanical properties in human subjects: dependence on stimulus variables. J. Neurophysiol. 65, 724–735. 31. Veuillet E., Collet L. and Morgon A. (1992) Differential effects of ear-canal pressure and contralateral acoustic stimulation on evoked otoacoustic emissions in humans. Hear. Res. 61, 47–55. 32. Viemeister N. F. (1979) Temporal modulation transfer functions based upon modulation thresholds. J. Acoust. Soc. Am. 66, 1364–1380. 33. Warr W. B., Guinan J. J. Jr and White J. S. (1986) Organization of the efferent fibers: the lateral and medial olivocochlear systems. In Neurobiology of Hearing. The Cochlea (eds Altschuler R. A., Hoffman D. W. and Bobbin R. P.), pp. 333–348. Raven, New York. 34. Winslow R. L. and Sachs M. B. (1988) Single tone intensity discrimination based on auditory nerve rate responses in backgrounds of quiet, noise and with stimulation of the crossed olivocochlear bundle. Hear. Res. 35, 165–190. (Accepted 2 October 1998)
Neuroscience Vol. 91, No. 1, pp. 133–138, 1999 Copyright 䉷 1999 IBRO. Published by Elsevier Science Ltd Printed in Great Britain. All rights reserved 0306-4522/99 $20.00+0.00 S0306-4522(98)00608-3
SINUSOIDAL AMPLITUDE MODULATION ALTERS CONTRALATERAL NOISE SUPPRESSION OF EVOKED OTOACOUSTIC EMISSIONS IN HUMANS S. MAISON,*† C. MICHEYL*‡ and L. COLLET* *Universite´ Claude Bernard Lyon 1, Laboratoire “Neurosciences and Syste`mes Sensoriels”, UPRESA CNRS 5020, Lyon, France ‡Applied Psychology Unit, Medical Research Council and Department of Experimental Psychology, University of Cambridge, Cambridge, U.K.
Abstract—It is well established that low-level broad band noise can elicit an amplitude decrease in evoked otoacoustic emissions recorded in the opposite ear. However, the influence of the temporal characteristics of the contralateral stimulus on this effect remains largely unknown. In the present study, otoacoustic emissions evoked by 60 dB SPL clicks were recorded in 19 normal-hearing subjects using the Otodynamics ILO88, successively in absence and presence of a contralateral noise that was either steady or modulated sinusoidally in amplitude at different depths (from 25% to 100% in 25 point steps) and rates (from 50 Hz to 800 Hz in half-octave steps). The energy was kept constant whatever the modulation depth. The results showed that the evoked otoacoustic-emission attenuation effect induced by contralateral stimulation varied depending on the modulation depth and frequency of the contralateral amplitudemodulated noise. The largest suppression effect was observed at the 100 Hz modulation frequency and the 100% modulation depth. The 50 Hz modulation resulted in less suppression than with unmodulated noise. An interpretation of these results in terms of the influence of temporal amplitude fluctuations falling within a certain range on medial olivocochlear bundle activity is discussed. 䉷 1999 IBRO. Published by Elsevier Science Ltd. Key words: medial olivocochlear system, outer hair cells, cochlear micromechanics, amplitude modulation, human.
Since Rasmussen’s description 26 of the cochlear efferent system in 1946, anterograde transport techniques using radioactively labelled amino acids have distinguished two populations of olivocochlear efferent fibres. 33 Firstly, the lateral olivocochlear neurons which project mainly ipsilaterally on to cochlear afferent neuron dendrites close to the inner hair cells, and, secondly, the medial olivocochlear neurons originating from the medial nuclei of the superior olivary complex, and projecting mainly on to the contralateral organ of Corti, where they synapse at the base of the outer hair cells (OHCs). Electrophysiological studies have sought to demonstrate involvement of the medial olivocochlear bundle (MOCB) in the suppression of the auditory nerve response to acoustic stimulation, obtained by electrical stimulation to the floor of the fourth ventricle. 10 Similar suppressions have †To whom correspondence should be addressed. Abbreviations: AM, amplitude modulation or amplitude modulated; CAP, compound action potential; CAS, contralateral acoustic stimulation; EOAE, evoked otoacoustic emission; MD, modulation depth; MF, modulation frequency; MOCB, medial olivocochlear bundle; OAE, otoacoustic emission; OHC, outer hair cell. 133
been shown for endocochlear potential and for the discharge rate of cochlear afferents. 6,12,13 It has been shown that acoustic stimulation of the contralateral ear can activate the MOCB 4,6 and modify ipsilateral activity in auditory fibres in response to acoustic stimulation. In particular, Folsom and Owsley 7 demonstrated that contralateral sound stimulation could induce a decrease in compound action potential (CAP) amplitude in humans. The MOCB establishes basolateral synapses with cochlear OHCs. It has been shown that contralateral acoustic stimulation (CAS) can, via MOCB fibres, modify the sounds generated by fast OHC contractions, known as otoacoustic emissions (OAEs). Mountain 23 and Siegel and Kim 27 stimulated efferent fibres and observed a simultaneous decrease in distortion product OAE amplitude. Puel and Rebillard 25 showed the same effect, using a contralateral broad band noise in guinea-pigs, and found suppression of the effect after section of the floor of the fourth ventricle. Likewise, in humans, numerous studies 1,5,30,31 have demonstrated a decrease in evoked OAE (EOAE) amplitude, using contralateral broad band noises, narrow band noises or clicks at low contralateral stimulus intensity (30 dB SL). Because this contralateral EOAE
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amplitude attenuation effect is already significant at such low contralateral stimulus intensity, it cannot be explained by acoustic crosstalk. Moreover, although a possible involvement of the middle ear cannot be completely excluded at such levels, the contralateral suppression effect cannot be entirely due to a middle ear modification because it is still found in subjects with unilateral loss of the stapedial reflex. 31 Moreover, the middle ear could not explain the frequency specificity found in the contralateral stimulation effect. 17 More recently, it has been demonstrated that the effect is absent or dramatically reduced in patients whose MOCB had been sectioned during vestibular neurectomy 11 as the olivocochlear bundle exits the brain with the vestibular division of the vestibulo-cochlear nerve. 26 Studies performed so far have indicated that, while a significant contralateral EOAE amplitude suppression effect can be observed with intensities as low as 30 dB SL when the CAS consists of broad band noises or narrow band noises, no significant contralateral EOAE suppression is obtained below about 60 dB SL for a pure-tone CAS. 1,18,30 However, at such a high stimulus intensity, mechanisms other than MOCB action, such as those mentioned above, may well be responsible for the effect. In that case, pure tones would appear to be less effective, or even not effective at all, in inducing MOCB-mediated contralateral EOAE attenuation. These effects of contralateral tones on EOAEs contrast with the effects observed on CAP which reveal substantial amounts of suppression at frequencies below about 1.5 kHz using contralateral pure tones of relatively low level, around 25–30 dB SPL. 17 The exact reason for the lesser contralateral EOAE suppression effectiveness of pure tones as compared to noises of the same sensation level, implying that other CAS characteristics than sound level are determinant in the contralateral EOAE attenuation effect, remains unclear at present. One possible factor in this difference has been recently revealed by the finding that significant contralateral EOAE attenuation can be elicited by low-intensity tones when these are amplitude modulated 18 or frequency modulated. 19 This result suggests that rapid temporal fluctuations which are naturally present in noises but absent in steady tones contribute to enhance the contralateral attenuation effect, thereby explaining why this effect is larger with the former than with the latter. However, because amplitude modulation alters the spectrum of tones as well as their temporal envelope, it remains unclear whether the effect of amplitude modulation observed in this study is due to amplitude fluctuations in the temporal envelope of the contralateral stimulus per se or whether it is due to the presence of side bands surrounding the carrierfrequency peak in the spectrum. In other words, the question as to whether temporal amplitude fluctuations are a factor in the contralateral EOAE attenuation effect still remains unanswered. To further test
the hypothesis that amplitude modulation plays a role per se in the contralateral attenuation effect via temporal mechanisms, through the fluctuations it induces in the contralateral stimulus envelope, the present study compared contralateral EOAE attenuation effects elicited by modulated vs unmodulated white noise. In this study, as in many others, 3,24,32 advantage was taken of the fact that the long-term power spectrum of white noise, contrary to that of tones, is unaffected by temporal amplitude modulation. EXPERIMENTAL PROCEDURES
Subjects The present study involved 19 subjects (nine males, 10 females; 22–39 years old; mean age 28 years, S.D. 7) with no history of auditory pathology and normal audiometric functions [thresholds of 10 dB hearing level (HL) or better between 250 Hz and 8 000 Hz at octave intervals on pure tone audiogram]. Tonal audiometry and tympanometry were conducted in a soundproof room using a Madsen DA III audiometer and an Amplaid 702 impedancemeter, respectively. Evoked otoacoustic emission recording EOAEs were recorded and analysed according to the methodology proposed by Bray and Kemp. 2 Stimulus was presented with a BP 1712 earphone and EOAEs were recorded with a Knowles 1843 microphone, both embedded in a plastic ear plug. Stimulus presentation, data recording and averaging were carried out using the Otodynamics ILO88 software and hardware. The stimulus was a 1 kHz tone pip (one cycle rise-and-fall, two cycles plateau). The stimulus presentation rate was 50 Hz. The linear cochlear echo method, with a combination of four acoustic impulses identical in size and polarity, was used: meatal and middle ear echoes are not self-cancelling in this condition, and their durations increase with stimulus level; such ringing components were eliminated by using low intrameatal stimulation. The stimulus level was 60 ^ 3 dB SPL, measured in the ear canal. To minimize stimulus artifact, EOAE analysis was windowed so as to truncate the first 6 ms of the response to zero. The analysis window was 20 ms; 512 responses were averaged. A pass band of 500–6 000 Hz was employed. EOAE amplitude was computed from the whole response in a time window of 6–20 ms. Contralateral acoustic stimulation The CAS was either an unmodulated noise or an amplitude modulated (AM) noise, generated using a 16-bit digital-to-analogue (D/A) converter at a sampling rate of 44.1 kHz and delivered through a TDH 39 earphone (bandwidth: 50–8000 Hz). The D/A card was installed on a IBMcompatible computer. The formula used for the generation of the modulated stimulus was: s t k:1 ⫹ m:cos 2pfm t:c t; where c(t) represents a white noise carrier, m and fm are, respectively, the modulation depth—between 0 and 1—and frequency (in Hz), and k is a correction factor applied to maintain the energy of the modulated noise equal to that of the unmodulated noise; this correction factor was given by: p k 1= 1 ⫹ m2 =2: In each subject, the level of the contralateral noise was set at 40 dB SL, i.e. 40 dB above the absolute threshold of this
Medial olivocochlear system activated by AM noise
noise measured beforehand in this subject. The mean absolute threshold across listeners was 6.6 dB SPL—overall level—(S.D. 4.0 dB). Procedure AM noise effect on EOAEs was studied according to two parameters: modulation depth (MD) and modulation frequency (MF). Effect of modulation depth. Subjects received a contralateral noise (broad band noise: 0–20,000 Hz) modulated at 100 Hz and with depth varying between 0 (unmodulated) and 100% by 25 point steps. Contralateral intensity level was 40 dB SL (i.e. 46.6 ^ 4.0 dB SPL). Effect of modulation frequency. Subjects followed the above procedure with a contralateral noise modulated with a depth of 100% and with frequency varying between 50 and 800 Hz by half-octave steps. Statistics Statistical analysis was performed using Sigmastat 䉸 software (version 1.02) and included analysis of variance for repeated measures (RMANOVA) in their non-parametric version (i.e. Friedman RMANOVA) and multiple comparisons tests (Student’s Newman–Keuls method). RESULTS
Figure 1 shows EOAE amplitudes recorded from one representative subject without and with contralateral stimulations described in Experimental Procedures. It should first be noted that all the contralateral noises (unmodulated and modulated) used in this experiment induced a statistically significant suppression of EOAE amplitude compared to that found without contralateral stimulation (paired ttest, P ⬍ 0.001). The main result of the present study is presented in Fig. 2. While an unmodulated noise (i.e. 0% MD) induced a significant EOAE amplitude suppression, an AM noise of the same energy induced a significantly greater EOAE amplitude suppression: P 0.006, for unmodulated and 100%-modulated noise. For MD, ANOVA for repeated measures showed a statistically significant effect (Friedman RMANOVA: x 2 11.0, P 0.027). In spite of a regular increase in EOAE amplitude suppression with MD (i.e. EOAE amplitude suppression: 0% ⫺ 0.85 ^ 0.12, 25% ⫺ 0.88 ^ 0.15, 50% ⫺ 0.92 ^ 0.1, 75% ⫺ 0.91 ^ 0.15 and 100% ⫺ 1.11 ^ 0.14), the 100%-MD AM noise was the only contralateral stimulus to induce a significantly greater suppression of EOAE amplitude compared with unmodulated noise (pairwise multiple comparison, P ⬍ 0.05). The data shown in Fig. 3 describe the variation in attenuation as a function of contralateral MF. Friedman RMANOVA showed a statistically significant MF effect from 50 to 800 Hz by half-octave steps (x 2 22.7, P 0.004). EOAE amplitude was reduced significantly for MFs ranging in half-octave
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steps from 50 to 800 Hz for an MD of 100%. For this MD, the greatest increase in contralateral EOAE-amplitude suppression was obtained for the 100 Hz MF. The contralateral EOAE suppression effect obtained in presence of a 100 Hz, 100% AM noise proved significantly different (pairwise multiple comparison, P ⬍ 0.05) from the EOAE suppression elicited by any of the other contralateral stimuli used in this study. At the 50 Hz MF, significantly less suppression than with unmodulated noise was observed (paired t-test, P 0.015). DISCUSSION
The results of the present study indicate that larger contralateral EOAE amplitude attenuation effects can be obtained with modulated rather than with unmodulated noise as contralateral stimulus under a given range of modulation conditions, the contralateral EOAE attenuation effect elicited by AM noise being dependent on the AM parameters. Regarding the first parameter, AM rate or frequency, the largest suppression effect was obtained with a contralateral noise modulated at a frequency of 100 Hz. Only at this modulation rate did the AM noise elicit a contralateral EOAE attenuation effect larger than that produced by unmodulated noise. This finding of 100 Hz as a preferential modulation rate for the contralateral EOAE attenuation effect is in agreement with the results of a previous study in which the largest contralateral EOAE attenuation effects were elicited by AM tones at a MF of 100 Hz. 18 However, the tuning to amplitude-modulation rate observed in our previous study was broader than the tuning observed in the present study in the sense that, at least at the largest modulation depths, several modulation rates in the 50–400 Hz range other than 100 Hz also elicited larger contralateral EOAE suppression than in the unmodulated condition. This difference between the two studies is most probably due to a difference in the carrier waveform. Whereas the steady broadband noise used in the present study elicited contralateral suppression, the pure tones used in the earlier study did not. Therefore, it is conceivable that the effects of amplitude modulation on contralateral suppression are larger when the steady contralateral stimulus used as a reference produces none than when this stimulus already elicits a substantial amount of baseline suppression. Assuming that the contralateral EOAE-amplitude suppression effects are underlaid by activation of the MOCB, as is strongly suggested by data reviewed in the Introduction, the origin of the selectivity to AM rate observed in the present and our previous studies may be sought in the physiology of MOCB neurons. Interestingly, the only results available in the literature on the coding
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Fig. 1. Examples of differences in EOAE traces induced by contralateral noises with different modulation depths and rates in one subject (female, 25 years old). The top panel shows the EOAE trace recorded without contralateral stimulation. The left-hand column shows the differences in EOAE traces induced by contralateral noise amplitude modulated at a rate of 100 Hz and at different depths, as computed by subtracting the EOAE trace recorded in presence of the noise from the reference EOAE trace shown at the top. The right-hand column shows the differences in EOAE trace induced by contralateral noise amplitude modulated at a depth of 100% and at different rates.
of AM by MOCB neurons 14 indicate two main types of efferent neurons: one—most units—exhibiting modulation-transfer functions with a peak around 100 Hz, and a second—24% of the units—showing a broad low-frequency peak. These data are grossly consistent with our findings but further information on the coding of AM by MOCB neurons is required before the neurophysiological mechanisms underlying these findings can be discussed in more detail. An intriguing result of the present study lies in the fact that the 50 Hz AM noise elicited
less suppression than unmodulated noise. An interpretation of this observation is that, owing to bandpass filtering by the cochlea, the peripheral auditory filter outputs in response to the unmodulated noise already exhibited some degree of AM at rates around 100 Hz—as determined by the 3 dB bandwidth of filters having their center frequencies around 1 kHz—and that these fluctuations, which are the most efficient in eliciting contralateral suppression, were disrupted by the superimposition of an extrinsic AM at a lower rate such as 50 Hz.
Medial olivocochlear system activated by AM noise
Fig. 2. EOAE amplitude suppression as a function of contralateral MD. EOAEs were elicited by a 1 kHz tone pip set at 60 dB SPL. EOAEs were recorded in 19 subjects without (EOAE relative amplitude 0 dB) and with a broad band noise modulated at a frequency of 100 Hz with a depth varying from 0% (unmodulated) to 100% by 25 point steps. Bars indicate standard errors of the EOAEs.
Fig. 3. EOAE amplitude suppression as a function of contralateral MF. EOAEs were elicited by a 1 kHz tone pip set at 60 dB SPL. EOAEs were recorded in 19 subjects without (EOAE relative amplitude 0 dB) and with a broad band noise modulated at a depth of 100% with a frequency varying from 50 Hz to 800 Hz by half-octave steps. Bars indicate standard errors of the EOAEs.
Considering the second AM parameter, namely, AM depth, the results indicate that the deeper the AM applied, the larger the contralateral EOAE attenuation. However, although an increase in EOAE amplitude suppression was found for 25, 50 and 75% MDs, only the 100% MD elicited an EOAE attenuation effect significantly larger than did 0% modulation. In our previous study using AM tones, 18 significant contralateral EOAE attenuation was obtained from modulation of about 37%. Once again, however, a possible reason for the fact that only the largest MD proved significant is that the broad band noises used as contralateral stimuli already exerted a suppression effect, even when unmodulated.
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Because the noises used in this study had very broad bandwidths, the difference observed between the EOAE attenuation effects elicited by modulated and unmodulated stimuli cannot be imputed to alterations in the long-term spectrum of these stimuli. Moreover, because the energy of the contralateral stimulus was held constant independently of the depth of modulation, and was thus equal in unmodulated and modulated conditions, the observed difference cannot be imputed to differences in the overall energy of the contralateral stimulus. The possibility that the observed difference between modulated and unmodulated stimuli is due to the larger maximum instantaneous amplitude in the modulated stimulus cannot be completely ruled out on the basis of the present results. However, several arguments argue against this interpretation. Firstly, the results of previous studies show that whilst steady tones start to elicit significant contralateral suppression at levels around 60 dB SL, 31 AM tones already do so at levels as low as 30 dB SL. 18 A simple calculation indicates that the maximum increase in peak level produced by applying the AM together with the correction factor was about 4 dB. Consequently, even if one assumes that the increase in peak level produced by the modulation is equivalent to an increase in overall level, the observed necessity of raising the level of an unmodulated contralateral stimulus by more than 20 dB in order for it to have a similar suppressive effect than an unmodulated stimulus cannot be accounted for. This, however, might hold only for pure tones, not for noise. Given the incompleteness of neurophysiological events, the present results do not allow us to determine the exact mechanisms by which temporal amplitude fluctuations can elicit variations in contralateral EOAE suppression. According to arguments raised in previous studies, 5,30 MOCB rather than middle ear functioning is the main mechanism of contralateral suppression effects. However, so far, strong arguments against middle ear effects have been obtained using unmodulated stimuli only and it therefore cannot be excluded that the suppressive effects observed more recently with AM stimuli involve middle-ear reflexes. CONCLUSIONS
Sounds in the natural environment are rarely steady. Biological signals such as animal or human vocalizations present temporal amplitude and frequency fluctuations. 28 The results of the present study, indicating variations in MOCB activity in response to temporal amplitude fluctuations with rates lying within the periodicity-pitch range, with a maximum around the human-voice fundamentalfrequency, suggest the possibility of an involvement of this efferent system in the processing of ecological signals. 14 From this point of view, these
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results add a new dimension to the notion of the role of the auditory efferents in hearing suggested in recent studies in both animals 15,16,20,34 and humans. 21,22
Acknowledgements—The authors are grateful to Professor John D. Durrant and to an anonymous reviewer for their very helpful comments and suggestions on earlier versions of this manuscript.
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