!,( E L S E V I E R Hearing Research 82 (1995) 59-64

Effects of acoustic overstimulation on 2fl-f2 distortion product in the cochlear microphonics

Masafumi Yoshida *, Mitsuyoshi Aoyagi, Kazumi Makishima Department of Otorhinolaryngology, University of Occupational and Environmental Health, School of Medicine, Yahata-nishiku,

lO'takyushu 807, Japan

Received 16 April 1994; revised 6 September 1994; accepted 18 October 1994

Abstract

The cochlear microphonics (CM) in response to two-tone stimuli as well as the threshold of compound action potential (CAP) were measured before and after exposure to 4 kHz pure tone at 100 dB SPL for 10 min. Although the loss of CM output at the primary frequencies was limited to around 2 dB, the 2fl-f2 distortion products in the CM (CM-DPs) were markedly reduced immediately after the exposure, especially at low primary levels (i.e. less than 65 dB). The low level CM-DPs recovered gradually near the initial level within 7 days from the exposure. The elevation of CAP threshold closely paralleled with the reduction of CM-DPs in not only the acute phase but also in the recovery phase from the exposure. These results show that the active transduction process in the cochlea was affected by acoustic overstimulation. This impairment of the active transduction was postulated to play an important role in developing the noise induced temporary threshold shift.

Keywords: Acoustic overstimulation; Cochlear microphonics; 2fl-f2 distortion product; Active process

1. Introduction

The inter-modulation distortion products (DPs) in the cochlear microphonics (CM) response to two-tone stimulation have long been recognized (Wever et al., 1940; Dallos, 1969). Kemp and Brown studied the propert ies of the DPs in the CM during bitonal stimu- lation, and made a comparison with the DPs measured acoustically in the external ear canal (Kemp and Brown, 1984; Brown and Kemp, 1985). They concluded that both electrical (CM) DPs and acoustic DPs were di- rectly related to the physiological process associated with the transduction activity of the cochlear outer hair cell (OHC), especially with its nonlinear property. This nonlinear and active transduction process in the cochlea was proposed to play a role in amplifying low-level acoustic stimuli (cochlear amplifier; Davis, 1983), and was thought to be bidirectional, consisting of a forward (mechano-electrical) and reverse (electro-mechanical) transduction process (Mountain, 1986; Kim, 1986).

* Corresponding author.

0378-5955/95/$09.50 © 1995 Elsevier Science B.V. All rights reserved SSDI 0 3 7 8 - 5 9 5 5 ( 9 4 ) 0 0 1 6 5 - 0

Among the numerous studies performed on the effects of acoustic overstimulation (see Saunders et al., 1985; 1991; Schmiedt, 1984 for review), there have been several reports suggesting the effect of acoustic overstimulation on the cochlear transduction mecha- nism. From the fact that blockade of afferent transmit- ter receptors did not reduce the effect of acoustic trauma, Puel et al. (1988) concluded that the cochlear transduction mechanisms were affected by intense sound exposure earlier than the postsynaptic struc- tures. Patuzzi et al. (1989) demonstrated a high corre- lation between the neural threshold elevation and the decrease in the low-frequency CM amplitude, and sug- gested that the temporary loss of neural sensitivity following loud sound was due to a simple inactivation of the mechano-electrical transduction channels at the apex of the OHC. Intracellular recording studies by Cody and Russell (1991) revealed that exposure of the cochlea to loud sound reduced the nonlinear proper- ties of the hair cells and resulted in a linearization of the hair cell response to acoustic stimuli. The results of all these investigations seem to indicate that acoustic overstimulation affects the transduction activity of the cochlear hair cells.

60 M. Yoshida et al. / Hearing Research 82 (1995) 59-64

The purpose of the present study was to investigate the effects of acoustic overstimulation on the cochlear transduction activity. We monitored the CM response to two-tone stimuli together with the compound action potential (CAP) before and after loud sound exposure in the guinea pig, and observed the correlation be- tween the alterations in the CAP threshold and the output of the distortion product in cochlear micro- phonics (CM-DP).

2. Materials and methods

2.1. Subjects Experiments were performed on 42 albino guinea

pigs with normal pinna reflex, weighing 250-450 g. The animals were anesthetized with 35 m g / k g of Pentobar- bital sodium administrated intraperitoneally. Each ani- mal was placed in a supine position with its head held stationary by a head holder. Body temperatures were controlled at approximately 38°C by a heating pad. The care and use of the animals reported in this study were performed in accordance with the guidelines of the Declaration of Helsinki.

Acoustic stimuli and exposure sounds were deliv- ered using the closed sound system through a hollow earbar of the headholder. Calibrations of the sound intensity were made previously with a B & K 4182 probe microphone in a dummy ear, and were confirmed in the ear canal near the tympanic membrane of each animal at the end of the measurement.

2.2. Noise exposure and period of measurement The guinea pigs with spontaneous respiration were

exposed to 4 KHz pure tone at an intensity of 100 dB SPL for 10 rain.

The animals exposed to the sound were divided into four groups as the intervals between the sound expo- sure and the electrophysiological measurement de- scribed below. In one group (day 0, N = 5), the mea- surements were performed immediately after the expo- sure. In the other three groups, the measurements were done 24 h (day 1, N = 9), 72 h (day 3, N = 7), and 168 h (day 7, N = 8) after the exposure.

In 13 animals without sound exposure, the identical electrophysiological measurement was obtained as a control.

2.3. Electrophysiological measurement A tracheostomy was performed, and ventilation was

maintained artificially with a ventilator. Each animal was immobilized with an intramuscular injection of 6 m g / k g of tubocurarine chloride. The left tympanic bulla of each animal was opened through a ventral approach, and bony cochlea was exposed. A tiny fenes- tration (about 150 microns in diameter) was made in

the bony wall over the scala tympani near the round window. An enamel insulated platinum electrode, with an exposed tip and having a diameter of 100 microns, was inserted into the scala tympani through the surgi- cal fenestration. An identical reference electrode was placed over the surface of the bulla. The recordings referenced to a ground Ag/AgC1 disc electrode placed on the neck muscle were amplified (WPI DMA-80) differentially with a gain of one thousand.

Acoustic stimuli used to obtain CAP thresholds were 2, 2.8, 4, 5, 6.3, 8, 10, 12 kHz tone bursts (1 ms rise/fall , 10 ms duration) arranged in a train with 60 ms inter-burst intervals. These signals produced by an external signal generator (made in our laboratory), were transduced and delivered to the left ear canal of each animal. Electrical responses to the tone burst trains were filtered with a bandpass of 8 to 1500 Hz (24 dB/oc tave roll-off) and averaged over 32 samples, and then displayed as a train of the CAPs. The threshold was defined as the lowest stimulus intensity at which the following two criteria could be met: a) an averaged N1-P1 amplitude of > 10 micro volt and b) increased amplitude with the next stimulus increment.

The CM-DP was elicited by equal-intensity 'pr imary ' stimuli at 4.62 kHz (f~) and 6 kHz (f2), yielding an f z / f l ration of 1.3. Pure tone signals were generated by two digital synthesizers (NF 1930A) phase-locked triggered by external signals, and routed through atten- uators and amplifiers to transducers (Koss Pro-4AA). The acoustic output from these transducers with an intensity ranging from 45 to 75 dB SPL were delivered to the left ear canal. Electrical responses to this bitonal stimulation were amplified and directed to a signal analyzer (RION SA-74A). The responses were aver- aged over 32 samples and the averaged response was submitted to Fast Fourier Transform (FFT) analysis and stored on a disk.

3. Results

3.1. Compound action potentials Fig. 1 demonstrates the mean and standard devia-

tion of the CAP threshold at the frequencies from 2 to 12 kHz in control and day 0 animals. The CAP thresh- olds in the control animals were obtained at the stimu- lus intensities of approximately 30 dB SPL for all frequencies tested. In day 0 animals, the CAP thresh- old was elevated at the frequencies of around and above 4 kHz with the maximum change at 5 kHz. The magnitudes of the elevation were 23.4 _+ 6.7 dB for 4 kHz, 27.9 _+ 4.5 dB for 5 kHz, and 26.0 +_ 4.2 dB for 6.3 kHz (mean _+ S.D.).

Fig. 2 reveals the CAP threshold in all five groups as individual values as well as the mean and standard deviation for each group at the frequencies of 4, 5 and

M. Yoshida et aL / Hearing Research 82 (1995) 59-64 61

- J a . ¢n

S 0 .1- ¢1) i l l

. l - p . Q.

6

20

40

60

80 - - o - - CONTROL = Day 0

m , • • | | | I

100 2 4 6 10

FREQUENCY (kHz)

Fig. 1. Threshold (mean + S.D.) of the CAP before (open circle) and immediately after (closed circle) the exposure of 4 kHz pure tone at 100 dB SPL for 10 rain.

- - e -- CONTROL

~, 100 - -e -- Day 0

o

E 10 LLI O k--

a .

<

0.1 ( _ )

I I I I I I I

40 45 50 55 60 65 70 75 80

PRIMARY LEVEL (dB SPL)

Fig. 3. Outputs of the CM response to two-tone stimulation ( f l = 4.62 kHz; f2 = 6 kHz, equal intensity) at the frequency of ]'2 (dashed line) and 2 f l - f 2 (3.24 kHz, solid line). Open and closed circles indicate before and immediately after the exposure, respectively.

6.3 kHz, where the maximum threshold elevation was observed immediately after the exposure. The mean CAP thresholds in day 1 group returned about half way to their control levels, and those in day 3 and 7 group recovered almost completely in all three frequencies. However, distributions of the CAP threshold in day 1, 3 and 7 groups were twice as wide as those of the control and day 0 animals for all frequencies.

i I I I I

2 0 • ~i

, o

60 4 kHz 7 0 I

i

20 o

q 4o ~ so

60 s ~ 7o T I . I ! I

60 6.3 kHz ~ 7 0 I I I I I

CONTROL day 0 day 1 day 3 day 7

Fig. 2. Threshold of the CAP at 4, 5 and 6.3 kHz before and at various periods after the exposure. Small symbols indicate the indi- vidual value, and large open squares indicate their means and standard deviations.

3.2. Bitonal cochlear microphonics Outputs of the bitonal CM at the f~,~quency of 6

knz (rE) and 3.24 kHz (2fl-f2 DP) t~" ~'control and day 0 groups are demonstrated in x 3. After the exposure, the CM output at 2f1%~~,~M-DP) was diminished more as the stimulus levo ~ecreased, and lowered down to noise level (0.05 miC~ °! V) at the level of 55 dB and below. In contrast, ,the input-output function of the CM at f2, which closel'¢ paralleled with that at fl , demonstrated a lateral shift with a sensitivity loss limited to around 2.0 dB. The differences in the CM output between the control and day 0 group were

" O

o

m t~

-10

-15

-20

-25

- 3 0

-35

- 4 0

- 4 5

-50 40

control

-

I I I I I I I

45 50 55 6 0 65 70 75 8 0

PRIMARY LEVEL (dB SPL)

Fig. 4. Output of 2f]-f2 CM-DP presented by distortion ratio before (open circle) and immediately after (closed circle) the expo- sure. The distortion ratio was obtained by the following numerical expression:

distortion ratio (dB) = 10Logl0{(2fl-f2 o u t p u t ) / ( f I output) 2

+ (f2 output) 2}

Asterisk (*) indicates a statistically significant difference from the controls (P < 0.01).

62 M. Yoshida et al. / Hearing Research 82 (1995) 59-64

not statistically significant for both f~ and f2 at all stimulus levels (P > 0.2, t-test).

For the convenience of comparison with the CAP threshold shift, the output of CM-DP, measured in micro volts, was transformed into a distortion ratio (dB) with the following numerical expression:

distortion ratio (dB)

(2 f i - f 2 output) = = 1 0 L o g l0

( f l °utput) 2 + (f= °utput) 2

The mean and standard deviation of the distortion ratio are indicated as a function of the stimulus intensi- ties for the control and day 0 animals in Fig. 4. Al- though no significant difference in the distortion ratio between the two groups was observed at the primary level of 75 dB SPL, the decrease in the distortion ratio at the primary intensities below 65 dB SPL was statisti- cally significant by the t-test (P < 0.01).

Fig. 5 reveals the individual values and their means of distortion ratio in each group at the primary level of 60 dB SPL. The mean distortion ratio, being -29.3 + 2.5 dB in the ce~ .~ l group, fell down to -48 .5 + 5.4 dB in day 0. And t nean distortion ratio in day 1, 3 and 7 groups showC,,-1, gradual recovery, indicating the val- ues of -41 .7 : ~ . 4 , -34 .8 + 8.6 and -33.1 + 4.9 dB, respectively. ~:._

3.3. Correlationc/between the changes in CAP threshold and distortion ratio

Fig. 6 illust~tes scatter plots for loss in the distor- tion ratio at tli[ primary intensity of 60 dB SPL plotted against the mean of CAP threshold shifts at 4, 5 and 6.3 kHz. The }gss in distortion ratio was obtained by subtracting the ratio in individual animals exposed to 4 kHz pure tone from the mean value in the control

-20

-25

-30

o -3s

~ -40

~ -4g

~ -50 o

-55

-60

I I I I

•

I I I I I I

cd~I'ROL day0 day 1 day3 day7

Fig. 5. Distorthz~ ratio at 60 dB SPL primary level before and at various periods ltfte~the exposure. Small symbols indicate individual value, anu la:v ~ squares indicate their means and standard devia- tions.

.-. 25 n n '?3 v

20

O ~ 15

I-

z o_ S I--

0 ~- 0 a

-5 -20

' ' ' ' 1 ' ' ' ' 1 ' ' ' ' 1 . . . . I ' ' ' ' 1 ' ' ' '

• Day 0 • 0 1 1

• Day 1 • • Day3 =&e.-" • • Day 7

I / •

O i i s

• I l l s /

t •*" i i i I , • l , l i , l . , , , l , . . , l i l l l l i i

-10 0 10 20 30 40

CAP THRESHOLD SHIFT (dB)

Fig. 6. Scatter plot of the loss in distortion ratio at 60 dB SPL primary level in individual animals plotted against the CAP threshold shift. The regression line between them was Y = 4.1 + 0.47X, and the correlation coefficient was 0.85 (P < 0.001).

animals. The distortion ratio loss tended to increase in linear manner as the CAP threshold elevated. The regression line between them was Y = 4.1 + 0.47X, and the correlation coefficient was 0.85 (N = 29, P < 0.001).

4. Discussion

The recording from single auditory neurons in the spiral ganglion of the guinea pig revealed a sensitivity loss of the tuning curves at and above the characteristic frequency in the initial phase of continuous pure tone exposures at the intensity of 100 dB SPL (Cody and Johnstone, 1980). The CAP near the threshold was shown to reflect the activity of a small group of neu- rons tuned to a single frequency (Dallos and Cheatham, 1976). Electro-cochleogram with CAP in the guinea pig was considered to satisfy the conditions required for it to reflect a single unit threshold, except for the most basal units (Johnstone et al., 1979). In the present study with the exposure to 4 kHz pure tone at 100 dB SPL for 10 min, the CAP thresholds demonstrated an elevation of around 30 dB at and above 4 kHz immedi- ately after the exposure. These observations agreed with the data reported on the single unit tuning curves (Cody and Johnstone, 1980), and also coincided with the noise induced temporary threshold shift measured psychoacoustically in humans (Ward, 1963).

Because DPs are considered to originate at the cochlear sites tuned to the frequencies of the primary tones (Robles et al., 1991), and the CAP threshold elevation was maximum at 5 kHz and second at 6.3 kHz in the present study, the CM was monitored with a bitonal stimulation consisting of 4.62 and 6 kHz pure tones. Reductions of the CM output at the primary

M. Yoshida et al. / Hearing Research 82 (1995) 59-64 63

frequencies (fl or f2) remained around 2 dB in all stimulus intensities even immediately after the sound exposure. The OHCs were embedded in the electro- mechanical feedback loop, which acted as a cochlear amplifier and partially or wholly canceled viscous damping within the organ of Corti (Patuzzi et al., 1989). A comparatively small change in the efficiency of OHCs, which transduced the basilar membrane movements, was considered to reduce the sensitivity of primary afferent nerve fibers greatly. Moreover, be- cause the CM recorded in the scala tympani of the basal turn with a single electrode is the arithmetic sum of responses from the OHCs distributed in the turn, the reduction of the OHC efficiency in the restricted region may be larger than the gross CM loss. Thus a small loss in the gross CM output, which was not statistically significant in this study, may not be in contradiction with the CAP threshold elevation up to 30 dB observed immediately after the sound exposure.

In contrast, the 2f1-f2 DPs in the CM at the primary intensities below 65 dB SPL were substantially reduced immediately after the sound exposure, while the DPs at the intensity of 75 dB remained at approxi- mately the same level as that in control animals. These results indicated that the CM at primary frequencies and the CM-DP showed different behavior toward acoustic overstimulation, when the primary intensity level was mild to moderate (i.e. below 65 dB SPL).

The tone-on-tone masking experiment on the cochlear potentials by Cheatham (1985) revealed that the slope of suppression growth functions for the cubic difference tone (2fl-f2) were three times steeper than that of the CM for its primaries in the guinea pig. She concluded that the data were consistent with the no- tion that suppression was brought by attenuating the input to the CM generator, and were compatible with the idea that suppression originates in cochlear me- chanics. The mechanical origin of the two-tone sup- pression was demonstrated by the measurement of the basilar-membrane vibration with the Mossbauer tech- nique and laser-velocimetry (Ruggero et al., 1992). According to these, our data seem to indicate that the residual effect of acoustic overstimulation produces a mechanical attenuation of the input to the CM genera- tor in similar manner to that of a simultaneous (tone- on-tone) masking.

Similar dissociation between the gross CM and the low level CM-DP were also described in the study by Kujawa et al. (1992), where intracochlear application of salicylate was performed in the guinea pig. From that finding, they concluded that salicylate acted on the OHCs and compromised active cochlear transduction processes selectively. Stypulkowski (1990) demon- strated a salicylate mediated increase in the membrane conductance of the OHCs in cats. He stated that this change in the OHCs interfered with the reverse trans-

duction process, and then reduced a gain of the cochlear amplifier, resulting in a loss of neural sensitiv- ity to low level stimuli. His data on single unit record- ings also demonstrated parallels between salicylate in- toxication and noise trauma. An attenuation of the input to the CM generator after acoustic overstimula- tion, which was suggested in this study, may also be produced by an inactivation of the transduction process in the cochlear OHCs.

In gentamicin-treated animals, Brown et al. (1989) reported that an early involvement of OHC was indi- cated only by an elimination of the low-intensity por- tion of the acoustic DP growth function. Norton et al. (1991) found that acoustic DPs to lower-level primaries were attenuated to the level of the noise floor within several minutes after cessation of normal cardiac activ- ity, while responses to high-level stimuli persisted for up to 3 h. In our investigation on the CM-DP with anoxia, the distortion ratio at primary intensities below 65 dB SPL decreased markedly immediately after the cessation of artificial ventilation, although the ratio at 75 dB remained at the control levels (unpublished data). The distortion products response to bitonal stim- ulation only at low intensity probably reflected the integrity of the active, physiologically vulnerable cochlear process. Thus, reduction in the CM-DPs to low level primaries observed in this study, which sug- gested a decrease of the cochlear nonlinearity, was assumed to indicate the effect of acoustic overstimula- tion on the cochlear active transduction system.

The decrease in DP-OAE level after acoustic over- stimulation has been reported to correlate significantly with the shift in the CAP growth function in the cat (Wiederhold et al., 1986). The present study using the guinea pig demonstrated that the reduction in the CM-DP and the elevation of CAP threshold correlated closely to each other not only in day 0 animals but also in animals from day 1 to day 7. Both neural sensitivity and active transduction mechanism in the cochlea ap- peared to be affected by the acoustic overstimulation, and then to recover in a similar manner. Therefore, alteration in the cochlear active transduction process is considered one of the mechanisms underlying the noise induced temporary threshold shift.

In the mammalian cochlea transduction system, both the passive and active process formed a feedback loop, which generated a negative damping against a positive frictional damping (Mountain, 1986). From this study, the question regarding which part in the transduction process was principally affected by acoustic overstimu- lation remained still unanswered. However, from close parallels seen between the CAP and the low-level CM-DP after acoustic overstimulation, the alteration of the active transduction process was proposed to play an important role in producing the noise induced tem- porary threshold shift.

64 M. Yoshida et aL / Hearing Research 82 (1995) 59-64

Acknowledgements

We wish to thank Mr. Shinichi Oishi for his sugges- tions in preparation of the manuscript, and Dr. Toshi- aki Takagi for his technical assistance in developing the signal generator used in this study.

References

Brown, A.M. and Kemp, D.T. (1985) Intermodulation distortion in the cochlea: could basal vibration be the major cause of round window CM distortion? Hear. Res. 19, 191-198.

Brown, A.M., McDoweU, B. and Forge, A. (1989) Acoustic distortion products can be used to monitor the effects of chronic gentamicin treatment. Hear. Res. 42, 143-156.

Davis, H. (1983) An active process in cochlear mechanics. Hear. Res. 9, 79-90.

Cheatham, M.A. (1985) Growth of suppression in the cochlear potentials. Hear. Res. 18, 291-294.

Cody, A.R. and Johnstone, B.M. (1980) Single auditory neuron response during acute acoustic trauma. Hear. Res. 3, 3-16.

Cody, A.L. and Russell l.J. (1991) Effects of Intense acoustic stimu- lation on the nonlinear properties of mammalian hair cells. In: A.L. Dancer, D. Henderson, R.J. Salvi and R.P. Hamernik (Eds.), Noise-Induced Hearing Loss, Mosby-year Book, St. Louis, MO, pp. 11-27.

Dallos, P. (1969) Combination tone 2f~-]" 2 in microphonic poten- tials. J. Acoust. Soc. Am. 46, 1437-1444.

DaUos, P. and Cheatham, M.A. (1976) Compound action potential (AP) tuning curves. J. Acoust. Soc. Am. 59, 591-597.

Johnstone, J.R., Alder, V.A., Johnstone, B.M., Robertson, D. and Yates, G.Y. (1979) Cochlear action potential threshold and single unit thresholds. J. Acoust. Soc. Am. 65, 254-257.

Kemp, D.T. and Brown, A.M. (1984) Ear canal acoustic and round window electrical correlates of 2f l - f2 distortion generated in the cochlea. Hear. Res. 13, 39-46.

Kim, D.O. (1986) Active and nonlinear cochlear biomechanics and the role of outer-hair-cell subsystem in the mammalian auditory system. Hear. Res. 22, 105-114.

Kujawa, S.G., Fallon, M. and Bobbin R.P. (1992) Intracochlear salicylate reduces low-intensity acoustic and cochlear micro- phonic distortion products. Hear. Res. 64, 73-80.

Mountain, D.C. (1986) Electromechanical properties of hair cells. In: R.A. Altschuler, D.W. Hoffman and R.P. Bobbin (Eds.), Neuro- biology of Hearing: The Cochlea. Raven Press, New York, pp. 77-90.

Norton, S.J., Bargones, J.Y. and Rubel, E.W. (1991) Development of otoacoustic emissions in gerbil: Evidence for micromechanical changes underlying development of the place code. Hear. Res. 51, 73-92.

Patuzzi, R.B., Yates, G.K. and Johnstone B.M. (1989) Changes in cochlear microphonic and neural sensitivity produced by acoustic trauma. Hear. Res. 39, 189-202.

Puel, J.L., Bobbin, R.P. and Fallon, M. (1988) The active process is affected first by intense sound exposure. Hear. Res. 37, 53-64.

Robles, L., Ruggero, M.A. and Rich, N.C. (1991) Two-tone distor- tion in the basilar membrane of the cochlea. Nature 349, 413-414.

Ruggero, M.A., Robles, L. and Rich, N.C. (1992) Basilar membrane responses to two-tone and broadband stimuli. J. Neurophysiol. 68, 1087-1099.

Saunders, J.C., Dear, S.P. and Schneider M.E. (1985) The anatomi- cal consequences of acoustic injury: A review and tutorial. J. Acoust. Soc. Am. 78, 833-860.

Saunders, J.C., Cohen, Y.E. and Szymko, Y.M. (1991) The structural and functional consequences of acoustic injury in the cochlea and peripheral auditory system: A five year update. J. Acoust. Soc. Am. 90, 136-146.

Schmiedt, R.A. (1984) The effects of noise on the physiology of hearing: A review and tutorial. J. Acoust. Soc. Am. 76, 1293-1317.

Stypulkowski, P.H. (1990) Mechanisms of salicylate ototoxicity. Hear. Res. 46, 113-146.

Ward, W.D. (1963) Auditory fatigue and masking. In:J. Jerger (Eds), Modern Developments in Audiology. Academic Press, New York, pp. 241-286.

Wever, E.G., Bray, C.W. and Lawrence, M. (1940) The interference of tones in the cochlea. J. Acoust. Soc. Am. 12, 268-280.

Wiederhold, M.L., Mahoney, J.W. and Kellogg, D.L. (1986) Acoustic overstimulation reduces 2f l - f2 cochlear emissions at all levels in the cat. In: J.B. Allen, J.L. Hall, A. Hubbard, S.T. Neely and A. Tubis (Eds.), Peripheral Auditory Mechanisms. Springer-Verlag, Berlin, pp. 322-329.