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Contralateral frequency-modulated tones suppress transient-evoked otoacoustic emissions in humans
Hearing Research 117 (1998) 114^118
Contralateral frequency-modulated tones suppress transient-evoked otoacoustic emissions in humans Steèphane Maison *, Christophe Micheyl, Lionel Collet Universiteè Claude Bernard Lyon 1, Laboratoire `Neurosciences et Systeémes Sensoriels', UPRESA CNRS 5020, Hoêpital E. Herriot^Pavillon U, 3 place d'Arsonval, 69437 Lyon cedex 03, France Received 11 September 1997; revised 4 December 1997; accepted 10 December 1997
Abstract In order to test the sensitivity of the human medial olivocochlear bundle (MOCB) to stimulus frequency fluctuations, changes in transient-evoked otoacoustic emission (TEOAE) amplitude induced by frequency modulated (FM) tones were measured in 18 normal-hearing subjects. The results revealed that TEOAE amplitude was reduced by contralateral FM tones at 40 dB above puretone threshold, with significant influences of both modulation rate (MR) and modulation depth (MD). This finding is discussed in the light of other recent results indicating amplitude fluctuation and frequency bandwidth effects in MOCB activation in humans. z 1998 Published by Elsevier Science B.V. Key words: Medial olivocochlear system; Cochlear micromechanism; Otoacoustic emission; Human; Frequency modulation
1. Introduction The mammalian auditory system comprises a neural e¡erent pathway originating in the vicinity of the medial superior olivary complex and projecting mainly onto the contralateral cochlea (Warr et al., 1986), where it establishes synaptic contact with the outer hair cells (OHCs) of the organ of Corti. This medial olivocochlear bundle (MOCB) forms part of an interaural pathway whereby acoustic stimulation in one ear elicits e¡erent activity in the opposite ear (Bunìo, 1978; Liberman, 1989). The role in hearing played by this re£exlike e¡erent activation remains a matter of controversy. While some studies suggest that it might contribute to protecting the inner ear against overstimulation (Rajan, 1988 ; Reiter and Liberman, 1995), or enhancing the encoding of signals in noise in animals (Winslow and Sachs, 1988; Kawase and Liberman, 1993; May and McQuone, 1995) and humans (Micheyl and Collet, 1996 ; Micheyl et al., 1997; Maison et al., 1997b), others fail to ¢nd any change after olivocochlear bundle * Corresponding author. Tel.: +33 (472) 11 05 03; Fax: +33 (472) 11 05 04; E-mail: [email protected]
(OCB) section whether in animals (Trahiotis and Elliott, 1968; Igirashi et al., 1979) or humans (Scharf et al., 1994, Scharf et al., 1997). One solution to this apparent contradiction may be that the OCB requires speci¢c stimulation conditions in order to reach a signi¢cant level of activity, conditions which may not be met in some experimental studies involving basic stimuli. From this point of view, determining the stimulus characteristics that lead to signi¢cant OCB activation would be an important prerequisite for understanding the function of this system. Studies addressing the question of the stimulus characteristics required for MOCB activation are scarce in the literature. This question was bypassed in the earliest studies, that used electrical stimulation of OCB neurons at the level of the fourth ventricle (Galambos, 1956; Wiederhold and Kiang, 1970 ; Gi¡ord and Guinan, 1987), and only studies involving acoustic stimulation provide relevant information. One such study, in particular, revealed that contralateral noises were more ef¢cient than contralateral tones in inducing OCB activity (Liberman, 1988). In humans, one way of studying MOCB activity induced by contralateral acoustic stimulation is to measure the contralateral suppression of
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transient-evoked otoacoustic emission (TEOAE) amplitude (Collet et al., 1990). This measure is based on the ¢nding that the amplitude of TEOAEs, which are sound vibrations recorded in the external auditory meatus in response to an auditory stimulus, is reduced by a stimulus in the opposite ear. Because several studies suggest that TEOAEs result from OHC fast motility (Brownell, 1990 ; Murata et al., 1991) and that the MOCB, which projects onto these cells, can be excited by contralateral acoustic stimulation (e.g., Bunìo, 1978 ; Liberman, 1989), the contralateral attenuation of the TEOAE has been interpreted as re£ecting an inhibitory MOCB action on OHC motility (Collet et al., 1990; Veuillet et al., 1991; Norman and Thorton, 1993; Berlin et al., 1993, Berlin et al., 1995; Giraud et al., 1995). So far, most studies of the attenuation of TEOAE amplitude have used steady tones or steady noises as contralateral stimuli. Signi¢cant suppression has been reported with contralateral sounds as low as 20 dB SL when the contralateral stimulus consists of broadband or narrowband noise; when it consists of a pure tone, no signi¢cant contralateral TEOAE suppression has been found from 20 to 60 dB HL (Berlin et al., 1993). Pure tones appear to be less e¡ective than noises in inducing e¡erent activation. However, more recent data reveal large suppressive e¡ects with amplitudemodulated (AM) tones, which may mean a speci¢c sensitivity of the MOCB to temporally £uctuating stimuli (Maison et al., 1997a). The present study tested whether £uctuations in stimulus frequency would, like £uctuations in stimulus amplitude, induce MOCB activation in humans, and how such activation might depend on frequency-modulation parameters. Accordingly, TEOAE amplitude was measured in the absence and in the presence of contralateral tones, which were frequency modulated (FM) at various depths and rates. 2. Methods
115
lyzed according to the method proposed by Bray and Kemp (1987). Stimulus presentation, data recording and averaging were carried out using the Otodynamics ILO88 software and hardware. The probe comprised a Knowles 1843 microphone and a BP 1712 earphone transducer, both embedded in a plastic earplug. The stimulus was a 1-kHz tone pip of 4 ms (1 cycle rise, 2 cycles plateau, 1 cycle fall); the intrameatal intensity, i.e., the level of the stimulus as measured in the ear canal, was 60 þ 3 dB SPL peak. The stimulus presentation rate was at 50 Hz. Responses were acquired over the 20 ms separating successive stimulus onsets. The averaging process stopped when 512 responses had been obtained. In order to remove stimulus artifacts, only the last 14 ms of response were taken into account in the analysis, the ¢rst 6 ms being cancelled. Subjects reclined in a sound-proof room. 2.3. Frequency-modulated stimuli The contralateral acoustic stimulus was a frequencymodulated (FM) tone, the waveform of which was de¢ned by the following formula: s t AWsin 2Zfc t fd =fc Wcos 2Zfm t where fc is the carrier frequency, fm is the modulation rate (MR), and fd is the modulation depth (MD). The carrier frequency was held constant at 1 kHz. Modulation frequencies of 10, 50, 100, 200, and 400 Hz, and modulation depths between 10 and 640 Hz, at octaves, were used. The level of the contralateral stimulus was set at 40 dB above absolute threshold for a steady tone at the carrier frequency ; this corresponded to a mean SPL of 46.7 þ 2.6 dB. The waveform of the stimulus was computed digitally and passed through a 16-bit digital-to-analog (D/A) converter at a sampling rate of 44.1 kHz before being delivered to the subject's left ear via a TDH 39 earphone. 2.4. Statistics
2.1. Subjects The study involved 18 subjects (11 male and 7 female ; mean age = 21 þ 3 yr) who had no history of auditory pathology and whose hearing levels were no higher than 10 dB HL between 250 Hz and 8000 Hz at octave intervals on a pure-tone audiogram. As assessed using an Amplaid 702 impedance meter, all the subjects showed middle ear acoustic re£ex in response to contralateral white noise stimuli (threshold mean = 87 dB SL; S.D. = 2 dB). 2.2. TEOAE recordings and analysis TEOAEs from the right ear were recorded and ana-
The results were analyzed by means of one- or twoway repeated-measure analysis of variances (ANOVAs) using as dependent variable the contralateral EOAE amplitude variation ^ computed by subtracting the EOAE amplitude measured in absence of contralateral stimulus from that obtained in presence of a contralateral stimulus, respectively ^ and as factors the rate and/or depth of frequency modulation. Further information as to the di¡erences in EOAE attenuation e¡ect elicited by various conditions was obtained using Student's t-test; in order to account for the fact that several such pairwise comparisons were performed over the same set of data, Bonferroni correction was applied.
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Fig. 1. Combined e¡ect of contralateral modulation rate and modulation depth on TEOAE amplitude. EAOEs were elicited by a 1-kHz tone pip set at 60 þ 3 dB SPL. Contralateral stimulation was FM tones at 40 dB SL. TEOAEs were recorded without and with a 1-kHz FM tone with MRs varying from 10 to 400 Hz (see top of each graph) and MDs varying from 10 to 640 Hz (X axis). Ordinate gives the relative TEOAE amplitude. Bars give the standard error (S.E.) of the TEOAEs. Single asterisk: P 6 0.05. Double asterisk: P 6 0.01. Triple asterisk: P 6 0.001.
3. Results Fig. 1 shows TEOAE amplitude attenuation as a function of the modulation depth (MD) of the contralateral FM tones at the various modulation rates (MRs) tested. Overall, the graphs indicate that suppression increases with increasing MD and MR. The results of a two-way repeated-measures ANOVA revealed highly signi¢cant e¡ects of both MD (F = 13.1, P 6 0.001) and MR (F = 4.1, P = 0.003) on amplitude attenuation. No signi¢cant interaction between the two factors was found. One-way ANOVAs further disclosed a highly signi¢cant e¡ect of MD at each MR (P 6 0.005). However, MR had a signi¢cant e¡ect on contralateral amplitude attenuation only at MDs of 80 and 160 Hz, not at the other MDs. Multiple pairwise comparisons, using Student's t-tests with Bonferoni's correction, revealed that TEOAE amplitude attenuation became signi¢cant at smaller MDs as MR increased: it became signi¢cant at 160 Hz when the MR was 10 Hz, at 80 Hz when the MR was 50 Hz, at 40 Hz when the MR was 100 Hz, at 20 Hz when the MR was 200 Hz and ¢nally at 10 Hz when the MR was 400 Hz. 4. Discussion The results of the present study indicate that TEOAE amplitude can be signi¢cantly attenuated by contralateral FM tones, and that the amount of attenuation depends on the depth and on the rate of frequency modulation. The fact that contralateral TEOAE amplitude suppression increased with the depth of frequency modulation, which de¢nes the width of the frequency
sweep, suggests that the frequency range spanned by the contralateral stimulus is an important factor in the suppression. This interpretation is supported by the results of a recent study in which TEOAE attenuation was measured as a function of contralateral noise bandwidth, and which revealed increasing attenuation with increasing bandwidth (Maison et al., personal communication; Norman and Thorton, 1993). It is consistent with the observation made in previous studies that pure tones do not elicit signi¢cant attenuation at SLs or SPLs at which broadband noises do elicit signi¢cant attenuation (Collet et al., 1990; Veuillet et al., 1991; Ryan et al., 1991; Berlin et al., 1993; Norman and Thorton, 1993). The sigmoid-like shape of the functions relating TEOAE suppression to MD observed for MRs of 50, 100 and 200 Hz suggests the underlying operation of a threshold-and-saturation mechanism whereby MDs which are too small will fail to induce variations in TEOAE amplitude ^ as with an unmodulated tone ^ whilst too large MDs do not elicit further changes in TEOAE amplitude once a certain maximum has been reached. Interestingly, at all MRs except 400 Hz, the critical MD at which TEOAE amplitude stopped increasing corresponded to a frequency sweep of 80 or 160 Hz, which compares well with the equivalent rectangular bandwidth of the auditory ¢lter centered on the carrier frequency of 1 kHz (Moore and Glasberg, 1987). Stimulus energy is known to be integrated by the auditory system within the bandwidth of peripheral auditory ¢lters (Fletcher, 1940). It might be that this phenomenon played a role in the present study, limiting the e¡ect of frequency sweeps exceeding the bandwidth of the auditory ¢lter centered on the carrier frequency.
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Another possible factor in the observed increase in contralateral TEOAE attenuation with increasing FM depth, besides stimulus bandwidth, is the amount of amplitude £uctuation at the output of auditory ¢lters. Because of bandpass ¢ltering at the cochlear stage, FM stimuli are likely to become AM in the auditory periphery (Saberi and Hafter, 1995). Other ¢ndings have recently demonstrated that AM tones elicit more contralateral TEOAE amplitude suppression than unmodulated tones of the same energy (Maison et al., 1997a). This notion of FM-induced AM signals in the auditory system may mean that the contralateral attenuation e¡ects with FM tones in the present study might ultimately re£ect AM sensitivity of MOCB activation. From this point of view, it is interesting to note that the largest contralateral TEOAE attenuation effects were observed for FM depths ranging between 50 and 200 Hz, which is consistent with the ¢nding, in our previous study, that AM rates between 100 and 200 Hz produced the largest TEOAE attenuation e¡ects. The comparison between the EOAE attenuation effects measured in this study using FM tones and those obtained in a previous study using AM tones suggests that, at the same SL and carrier frequency, FM tones elicit overall larger contralateral EOAE suppression than AM tones: whereas the largest EOAE variations measured in the present study were on average around 31.5 dB, at a modulation rate of 200 Hz and a depth of 160 Hz, those found earlier with AM tones were around 30.5, at a modulation rate of 100 Hz and a depth of 100% (Maison et al., 1997a). The e¡ects produced by FM tones are comparable to those measured in other studies using wide- or broadband noises using the same levels of contralateral and ipsilateral stimulation and same type of ipsilateral stimulus as used here: namely, using 50-dB SPL narrow-band noises (1-kHz centre frequency, 1/3rd-octave passbands) Veuillet et al. (1991) recorded EOAE variations slightly larger than 1 dB. Similar e¡ects were obtained using narrow- and broadband noises in a more recent study (Maison et al., personal communication). Therefore, overall noises and FM tones appear to be more e¤cient contralateral suppressors than AM tones. Together with recent results indicating a speci¢c sensitivity of MOCB activation to amplitude modulation (Maison et al., 1997a), the present ¢nding of substantial MOCB activation by frequency modulation suggests overall that the MOCB is liable to be strongly activated in listening situations involving stimuli with envelope or frequency £uctuations in the 50^200-Hz range. Because most ecologically relevant sounds, such as vocalization, contain such amplitude and frequency £uctuations, these results point to an e¡ective involvement of the MOCB in natural listening conditions in humans.
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Acknowledgments The authors are grateful to Professor Bertram Scharf for helpful comments on the manuscript. We gratefully acknowledge the other anonymous reviewers.
References Berlin, C.I., Hood, L.J., Hurley, A.E., Wen, H., Kemp, D.T., 1995. Binaural noise suppresses linear click-evoked otoacoustic emissions more than ipsilateral or contralateral noise. Hear. Res. 87, 96^103. Berlin, C.I., Hood, L.J., Wen, H., Szabo, P., Cecola, R.P., Rigby, P., Jackson, D.F., 1993. Contralateral suppression of non-linear clickevoked otoacoustic emissions. Hear. Res. 71, 1^11. Bray, P., Kemp, D.T., 1987. An advanced cochlear echo technique suitable for infant screening. Br. J. Audiol. 21, 191^204. Brownell, W.E., 1990. Outer hair cell electromotility and otoacoustic emissions. Ear Hear. 11, 82^92. Bunìo, W., 1978. Auditory nerve activity in£uenced by contralateral ear sound stimulation. Exp. Neurol. 59, 62^74. Collet, L., Kemp, D.T., Veuillet, E., Duclaux, R., Moulin, A., Morgon, A., 1990. E¡ects of contralateral auditory stimuli on active cochlear micromechanical properties in human subjects. Hear. Res. 43, 251^262. Fletcher, H., 1940. Auditory patterns. Rev. Mod. Phys. 12, 47^65. Galambos, R., 1956. Suppression of auditory-nerve activity by stimulation of e¡erent ¢bers to the cochlea. J. Neurophysiol. 19, 424^ 437. Gi¡ord, M.L., Guinan, J.J., 1987. E¡ects of electrical stimulation medial olivocochlear neurons on ipsilateral and contralateral cochlear responses. Hear. Res. 29, 179^194. Giraud, A.L., Collet, L., Cheèry-Croze, S., Magnan, J., Chays, A., 1995. Evidence of a medial olivocochlear involvement in contralateral suppression of otoacoustic emissions in humans. Brain Res. 705, 15^23. Igirashi, M., Cranford, J.L., Allen, E.A., Alford, B.R., 1979. Behavioural auditory function after transection of crossed olivocochlear bundle in the cat. I. Pure-tone intensity discrimination. Acta Otolaryngol. (Stockh.) 87, 429^433. Kawase, T., Liberman, M.C., 1993. Antimasking e¡ects of the olivocochlear re£ex. I. Enhancement of compound action potentials to masked tones. J. Neurophysiol. 70, 2519^2532. Liberman, M.C., 1988. Response properties of cochlear e¡erent neurons: monaural vs. binaural stimulation and the e¡ects of noise. J. Neurophysiol. 60, 1779^1798. Liberman, M.C., 1989. Rapid assessment of sound-evoked olivocochlear feedback: suppression of compound action potential by contralateral sound. Hear. Res. 38, 47^56. Maison, S., Micheyl, C., Collet, L., 1997a. Medial olivocochlear e¡erent system in humans studied with amplitude-modulated tones. J. Neurophysiol. 77, 1759^1768. Maison, S., Micheyl, C., Chays, A., Collet, L., 1997b. Medial olivocochlear system stabilizes active cochlear micromechanical properties. Hear. Res. 113, 89^98. Maison, S., Micheyl, C., Andeèol, G., Galleègo, S., Collet, L., submitted. What does activate medial olivocochlear e¡erent system in humans? Spectral aspects. May, B.J., McQuone, S.J., 1995. E¡ects of bilateral olivocochlear lesions on pure-tone intensity discrimination in noise. Audit. Neurosci. 1, 385^400. Micheyl, C., Collet, L., 1996. Involvement of the olivocochlear bundle in the detection of tones in noise. J. Acoust. Soc. Am. 99, 1604^ 1610.
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Micheyl, C., Perrot, X., Collet, L., 1997. Relationship between auditory intensity discrimination in noise and olivocochlear e¡erent system activity in humans. Behav. Neurosci. 111, 801^807. Moore, B.C.J., Glasberg, B.R., 1987. Formulae describing frequency selectivity as a function of frequency and level and their use in calculating excitation patterns. Hear. Res. 28, 209^225. Murata, K., Moriyama, T., Hosokawa, Y., Minami, S., 1991. Alternating current induced otoacoustic emissions in the guinea pig. Hear. Res. 55, 201^214. Norman, M., Thorton, A.R.D., 1993. Frequency analysis of the contralateral suppression of evoked otoacoustic emissions by narrowband noise. Br. J. Audiol. 27, 281^289. Rajan, R., 1988. E¡ect of electrical stimulation of the crossed olivocochlear bundle on temporary threshold shifts in auditory sensitivity. I. Dependence on electrical stimulation parameters. J. Neurophysiol. 60, 549^568. Reiter, E.R., Liberman, M.C., 1995. E¡erent-mediated protection from acoustic overexposure: relation to `slow e¡ects' of olivocochlear stimulation. J. Neurophysiol. 73, 506^514. Ryan, S., Kemp, D.T., Hinchcli¡e, R., 1991. The in£uence of contralateral stimulation on otoacoustic emission responses in humans. Br. J. Audiol. 25, 391^397. Saberi, K., Hafter, E.R., 1995. A common neural code for frequencyand amplitude-modulated sounds. Nature 374, 537^539. Scharf, B., Magnan, J., Chays, A., 1997. On the role of the olivo-
cochlear bundle in hearing: 16 case studies. Hear. Res. 103, 101^ 122. Scharf, B., Magnan, J., Collet, L., Ulmer, E., Chays, A., 1994. On the role of the olivocochlear bundle in hearing: a case study. Hear. Res. 75, 11^26. Trahiotis, C., Elliott, D.N., 1968. Behavioral investigation of some possible e¡ects of sectioning the crossed olivocochlear bundle. J. Acoust. Soc. Am. 47, 592^596. Veuillet, E., Collet, L., Duclaux, R., 1991. E¡ect of contralateral auditory stimulation on active cochlear micomechanical properties in human subjects: Dependence on stimulus variables. J. Neurophysiol. 65, 724^735. Warr, W.B., Guinan, J.J. Jr., White, J.S., 1986. Organization of the e¡erent ¢bers: the lateral and medial olivocochlear systems. In: Neurobiology of Hearing: The Cochlea (Altschuler, R.A., Ho¡man, D.W., Bobbin, R.P., Eds.) pp. 333^348, Raven Press, New York. Wiederhold, M.L., Kiang, N.Y.S., 1970. E¡ects of electrical stimulation of the crossed olivocochlear bundle on single auditory-nerve ¢bers in cat. J. Acoust. Soc. Am. 48, 950^965. Winslow, R.L., 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.
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Contralateral frequency-modulated tones suppress transient-evoked otoacoustic emissions in humans Steèphane Maison *, Christophe Micheyl, Lionel Collet Universiteè Claude Bernard Lyon 1, Laboratoire `Neurosciences et Systeémes Sensoriels', UPRESA CNRS 5020, Hoêpital E. Herriot^Pavillon U, 3 place d'Arsonval, 69437 Lyon cedex 03, France Received 11 September 1997; revised 4 December 1997; accepted 10 December 1997
Abstract In order to test the sensitivity of the human medial olivocochlear bundle (MOCB) to stimulus frequency fluctuations, changes in transient-evoked otoacoustic emission (TEOAE) amplitude induced by frequency modulated (FM) tones were measured in 18 normal-hearing subjects. The results revealed that TEOAE amplitude was reduced by contralateral FM tones at 40 dB above puretone threshold, with significant influences of both modulation rate (MR) and modulation depth (MD). This finding is discussed in the light of other recent results indicating amplitude fluctuation and frequency bandwidth effects in MOCB activation in humans. z 1998 Published by Elsevier Science B.V. Key words: Medial olivocochlear system; Cochlear micromechanism; Otoacoustic emission; Human; Frequency modulation
1. Introduction The mammalian auditory system comprises a neural e¡erent pathway originating in the vicinity of the medial superior olivary complex and projecting mainly onto the contralateral cochlea (Warr et al., 1986), where it establishes synaptic contact with the outer hair cells (OHCs) of the organ of Corti. This medial olivocochlear bundle (MOCB) forms part of an interaural pathway whereby acoustic stimulation in one ear elicits e¡erent activity in the opposite ear (Bunìo, 1978; Liberman, 1989). The role in hearing played by this re£exlike e¡erent activation remains a matter of controversy. While some studies suggest that it might contribute to protecting the inner ear against overstimulation (Rajan, 1988 ; Reiter and Liberman, 1995), or enhancing the encoding of signals in noise in animals (Winslow and Sachs, 1988; Kawase and Liberman, 1993; May and McQuone, 1995) and humans (Micheyl and Collet, 1996 ; Micheyl et al., 1997; Maison et al., 1997b), others fail to ¢nd any change after olivocochlear bundle * Corresponding author. Tel.: +33 (472) 11 05 03; Fax: +33 (472) 11 05 04; E-mail: [email protected]
(OCB) section whether in animals (Trahiotis and Elliott, 1968; Igirashi et al., 1979) or humans (Scharf et al., 1994, Scharf et al., 1997). One solution to this apparent contradiction may be that the OCB requires speci¢c stimulation conditions in order to reach a signi¢cant level of activity, conditions which may not be met in some experimental studies involving basic stimuli. From this point of view, determining the stimulus characteristics that lead to signi¢cant OCB activation would be an important prerequisite for understanding the function of this system. Studies addressing the question of the stimulus characteristics required for MOCB activation are scarce in the literature. This question was bypassed in the earliest studies, that used electrical stimulation of OCB neurons at the level of the fourth ventricle (Galambos, 1956; Wiederhold and Kiang, 1970 ; Gi¡ord and Guinan, 1987), and only studies involving acoustic stimulation provide relevant information. One such study, in particular, revealed that contralateral noises were more ef¢cient than contralateral tones in inducing OCB activity (Liberman, 1988). In humans, one way of studying MOCB activity induced by contralateral acoustic stimulation is to measure the contralateral suppression of
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transient-evoked otoacoustic emission (TEOAE) amplitude (Collet et al., 1990). This measure is based on the ¢nding that the amplitude of TEOAEs, which are sound vibrations recorded in the external auditory meatus in response to an auditory stimulus, is reduced by a stimulus in the opposite ear. Because several studies suggest that TEOAEs result from OHC fast motility (Brownell, 1990 ; Murata et al., 1991) and that the MOCB, which projects onto these cells, can be excited by contralateral acoustic stimulation (e.g., Bunìo, 1978 ; Liberman, 1989), the contralateral attenuation of the TEOAE has been interpreted as re£ecting an inhibitory MOCB action on OHC motility (Collet et al., 1990; Veuillet et al., 1991; Norman and Thorton, 1993; Berlin et al., 1993, Berlin et al., 1995; Giraud et al., 1995). So far, most studies of the attenuation of TEOAE amplitude have used steady tones or steady noises as contralateral stimuli. Signi¢cant suppression has been reported with contralateral sounds as low as 20 dB SL when the contralateral stimulus consists of broadband or narrowband noise; when it consists of a pure tone, no signi¢cant contralateral TEOAE suppression has been found from 20 to 60 dB HL (Berlin et al., 1993). Pure tones appear to be less e¡ective than noises in inducing e¡erent activation. However, more recent data reveal large suppressive e¡ects with amplitudemodulated (AM) tones, which may mean a speci¢c sensitivity of the MOCB to temporally £uctuating stimuli (Maison et al., 1997a). The present study tested whether £uctuations in stimulus frequency would, like £uctuations in stimulus amplitude, induce MOCB activation in humans, and how such activation might depend on frequency-modulation parameters. Accordingly, TEOAE amplitude was measured in the absence and in the presence of contralateral tones, which were frequency modulated (FM) at various depths and rates. 2. Methods
115
lyzed according to the method proposed by Bray and Kemp (1987). Stimulus presentation, data recording and averaging were carried out using the Otodynamics ILO88 software and hardware. The probe comprised a Knowles 1843 microphone and a BP 1712 earphone transducer, both embedded in a plastic earplug. The stimulus was a 1-kHz tone pip of 4 ms (1 cycle rise, 2 cycles plateau, 1 cycle fall); the intrameatal intensity, i.e., the level of the stimulus as measured in the ear canal, was 60 þ 3 dB SPL peak. The stimulus presentation rate was at 50 Hz. Responses were acquired over the 20 ms separating successive stimulus onsets. The averaging process stopped when 512 responses had been obtained. In order to remove stimulus artifacts, only the last 14 ms of response were taken into account in the analysis, the ¢rst 6 ms being cancelled. Subjects reclined in a sound-proof room. 2.3. Frequency-modulated stimuli The contralateral acoustic stimulus was a frequencymodulated (FM) tone, the waveform of which was de¢ned by the following formula: s t AWsin 2Zfc t fd =fc Wcos 2Zfm t where fc is the carrier frequency, fm is the modulation rate (MR), and fd is the modulation depth (MD). The carrier frequency was held constant at 1 kHz. Modulation frequencies of 10, 50, 100, 200, and 400 Hz, and modulation depths between 10 and 640 Hz, at octaves, were used. The level of the contralateral stimulus was set at 40 dB above absolute threshold for a steady tone at the carrier frequency ; this corresponded to a mean SPL of 46.7 þ 2.6 dB. The waveform of the stimulus was computed digitally and passed through a 16-bit digital-to-analog (D/A) converter at a sampling rate of 44.1 kHz before being delivered to the subject's left ear via a TDH 39 earphone. 2.4. Statistics
2.1. Subjects The study involved 18 subjects (11 male and 7 female ; mean age = 21 þ 3 yr) who had no history of auditory pathology and whose hearing levels were no higher than 10 dB HL between 250 Hz and 8000 Hz at octave intervals on a pure-tone audiogram. As assessed using an Amplaid 702 impedance meter, all the subjects showed middle ear acoustic re£ex in response to contralateral white noise stimuli (threshold mean = 87 dB SL; S.D. = 2 dB). 2.2. TEOAE recordings and analysis TEOAEs from the right ear were recorded and ana-
The results were analyzed by means of one- or twoway repeated-measure analysis of variances (ANOVAs) using as dependent variable the contralateral EOAE amplitude variation ^ computed by subtracting the EOAE amplitude measured in absence of contralateral stimulus from that obtained in presence of a contralateral stimulus, respectively ^ and as factors the rate and/or depth of frequency modulation. Further information as to the di¡erences in EOAE attenuation e¡ect elicited by various conditions was obtained using Student's t-test; in order to account for the fact that several such pairwise comparisons were performed over the same set of data, Bonferroni correction was applied.
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Fig. 1. Combined e¡ect of contralateral modulation rate and modulation depth on TEOAE amplitude. EAOEs were elicited by a 1-kHz tone pip set at 60 þ 3 dB SPL. Contralateral stimulation was FM tones at 40 dB SL. TEOAEs were recorded without and with a 1-kHz FM tone with MRs varying from 10 to 400 Hz (see top of each graph) and MDs varying from 10 to 640 Hz (X axis). Ordinate gives the relative TEOAE amplitude. Bars give the standard error (S.E.) of the TEOAEs. Single asterisk: P 6 0.05. Double asterisk: P 6 0.01. Triple asterisk: P 6 0.001.
3. Results Fig. 1 shows TEOAE amplitude attenuation as a function of the modulation depth (MD) of the contralateral FM tones at the various modulation rates (MRs) tested. Overall, the graphs indicate that suppression increases with increasing MD and MR. The results of a two-way repeated-measures ANOVA revealed highly signi¢cant e¡ects of both MD (F = 13.1, P 6 0.001) and MR (F = 4.1, P = 0.003) on amplitude attenuation. No signi¢cant interaction between the two factors was found. One-way ANOVAs further disclosed a highly signi¢cant e¡ect of MD at each MR (P 6 0.005). However, MR had a signi¢cant e¡ect on contralateral amplitude attenuation only at MDs of 80 and 160 Hz, not at the other MDs. Multiple pairwise comparisons, using Student's t-tests with Bonferoni's correction, revealed that TEOAE amplitude attenuation became signi¢cant at smaller MDs as MR increased: it became signi¢cant at 160 Hz when the MR was 10 Hz, at 80 Hz when the MR was 50 Hz, at 40 Hz when the MR was 100 Hz, at 20 Hz when the MR was 200 Hz and ¢nally at 10 Hz when the MR was 400 Hz. 4. Discussion The results of the present study indicate that TEOAE amplitude can be signi¢cantly attenuated by contralateral FM tones, and that the amount of attenuation depends on the depth and on the rate of frequency modulation. The fact that contralateral TEOAE amplitude suppression increased with the depth of frequency modulation, which de¢nes the width of the frequency
sweep, suggests that the frequency range spanned by the contralateral stimulus is an important factor in the suppression. This interpretation is supported by the results of a recent study in which TEOAE attenuation was measured as a function of contralateral noise bandwidth, and which revealed increasing attenuation with increasing bandwidth (Maison et al., personal communication; Norman and Thorton, 1993). It is consistent with the observation made in previous studies that pure tones do not elicit signi¢cant attenuation at SLs or SPLs at which broadband noises do elicit signi¢cant attenuation (Collet et al., 1990; Veuillet et al., 1991; Ryan et al., 1991; Berlin et al., 1993; Norman and Thorton, 1993). The sigmoid-like shape of the functions relating TEOAE suppression to MD observed for MRs of 50, 100 and 200 Hz suggests the underlying operation of a threshold-and-saturation mechanism whereby MDs which are too small will fail to induce variations in TEOAE amplitude ^ as with an unmodulated tone ^ whilst too large MDs do not elicit further changes in TEOAE amplitude once a certain maximum has been reached. Interestingly, at all MRs except 400 Hz, the critical MD at which TEOAE amplitude stopped increasing corresponded to a frequency sweep of 80 or 160 Hz, which compares well with the equivalent rectangular bandwidth of the auditory ¢lter centered on the carrier frequency of 1 kHz (Moore and Glasberg, 1987). Stimulus energy is known to be integrated by the auditory system within the bandwidth of peripheral auditory ¢lters (Fletcher, 1940). It might be that this phenomenon played a role in the present study, limiting the e¡ect of frequency sweeps exceeding the bandwidth of the auditory ¢lter centered on the carrier frequency.
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Another possible factor in the observed increase in contralateral TEOAE attenuation with increasing FM depth, besides stimulus bandwidth, is the amount of amplitude £uctuation at the output of auditory ¢lters. Because of bandpass ¢ltering at the cochlear stage, FM stimuli are likely to become AM in the auditory periphery (Saberi and Hafter, 1995). Other ¢ndings have recently demonstrated that AM tones elicit more contralateral TEOAE amplitude suppression than unmodulated tones of the same energy (Maison et al., 1997a). This notion of FM-induced AM signals in the auditory system may mean that the contralateral attenuation e¡ects with FM tones in the present study might ultimately re£ect AM sensitivity of MOCB activation. From this point of view, it is interesting to note that the largest contralateral TEOAE attenuation effects were observed for FM depths ranging between 50 and 200 Hz, which is consistent with the ¢nding, in our previous study, that AM rates between 100 and 200 Hz produced the largest TEOAE attenuation e¡ects. The comparison between the EOAE attenuation effects measured in this study using FM tones and those obtained in a previous study using AM tones suggests that, at the same SL and carrier frequency, FM tones elicit overall larger contralateral EOAE suppression than AM tones: whereas the largest EOAE variations measured in the present study were on average around 31.5 dB, at a modulation rate of 200 Hz and a depth of 160 Hz, those found earlier with AM tones were around 30.5, at a modulation rate of 100 Hz and a depth of 100% (Maison et al., 1997a). The e¡ects produced by FM tones are comparable to those measured in other studies using wide- or broadband noises using the same levels of contralateral and ipsilateral stimulation and same type of ipsilateral stimulus as used here: namely, using 50-dB SPL narrow-band noises (1-kHz centre frequency, 1/3rd-octave passbands) Veuillet et al. (1991) recorded EOAE variations slightly larger than 1 dB. Similar e¡ects were obtained using narrow- and broadband noises in a more recent study (Maison et al., personal communication). Therefore, overall noises and FM tones appear to be more e¤cient contralateral suppressors than AM tones. Together with recent results indicating a speci¢c sensitivity of MOCB activation to amplitude modulation (Maison et al., 1997a), the present ¢nding of substantial MOCB activation by frequency modulation suggests overall that the MOCB is liable to be strongly activated in listening situations involving stimuli with envelope or frequency £uctuations in the 50^200-Hz range. Because most ecologically relevant sounds, such as vocalization, contain such amplitude and frequency £uctuations, these results point to an e¡ective involvement of the MOCB in natural listening conditions in humans.
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Acknowledgments The authors are grateful to Professor Bertram Scharf for helpful comments on the manuscript. We gratefully acknowledge the other anonymous reviewers.
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