Medial olivocochlear system stabilizes active cochlear micromechanical properties in humans

Hearing Research 113 (1997) 89^98

Medial olivocochlear system stabilizes active cochlear micromechanical properties in humans Steèphane Maison a *, Christophe Micheyl a , Andreè Chays b , Lionel Collet ;

a

a

è Claude Bernard Lyon 1, Laboratoire Neurosciences et Syste é mes Sensoriels, Pavillon U, CNRS UPRESA 5020, Ho ê pital E. Herriot, Universite 3 place d'Arsonval, 69437 Lyon, France

b

ê pital Nord, Marseille, France Service d'O.R.L. et de Chirurgie Cervico-Faciale, Ho

Received 5 September 1996; revised 9 July 1997; accepted 16 July 1997

Abstract

To investigate the involvement of the medial olivocochlear system (MOCS) in outer hair cell (OHC) motility stabilization, evoked otoacoustic emissions (EOAEs) were recorded in 20 normal-hearing subjects and in eight vestibular-neurotomized subjects, successively in the presence and absence of low-intensity contralateral acoustic stimulation. Intrasubject EOAE amplitude variability was assessed as the standard deviation computed over several successive recordings. In normal-hearing subjects, a significantly lower EOAE amplitude variability with contralateral acoustic stimulation (CAS) was observed in subjects in whom the CAS induced the greatest EOAE amplitude reduction. This result could not be attributed to the EOAE amplitude reduction itself, since variability was otherwise found to increase when EOAE amplitude decreased. Moreover, statistically significant correlations between EOAE amplitude attenuation and EOAE amplitude variability under CAS were observed. In the eight subjects operated for vestibular neurotomy, no such effect was found. Being sectioned in vestibular-neurotomized subjects, the MOCS can no longer exert its effects. These results strongly support the notion that MOCS activity, as induced by CAS, elicits a reduction in EOAE amplitude variability in normal-hearing subjects. This finding and some of its possible implications for understanding the role of the MOCS in hearing in humans are discussed. Medial olivocochlear system; Human; Active cochlear micromechanism; Vestibular neurotomy; Outer hair cell; Otoacoustic emission Keywords :

1. Introduction

The cochlear organ of Corti receives e¡erent innervation via the olivocochlear bundle, described by Rasmussen (1946). Two anatomical e¡erent systems have been distinguished by means of anterograde labeling (Guinan et al., 1983, 1984; Warr and Guinan, 1979) : the mainly ipsilateral lateral olivocochlear bundle, which synapses with a¡erent neuron dendrites near to the inner hair cells (IHCs) on the one hand, and the medial olivocochlear bundle, the cell bodies of which are situated on the medial nuclei of the superior olivary

* Corresponding author. Tel.: (33) 472 11 05 03; Fax: (33) 472 11 05 04; E-mail: [email protected]

complex, on the other. Most medial olivocochlear system (MOCS) ¢bers cross at the £oor of the fourth ventricle (Warr et al., 1986; Warr, 1975) and synapse with the outer hair cells (OHCs) of the contralateral cochlea. Numerous electrophysiological studies have shown an inhibitory e¡ect of MOCS stimulation upon the auditory periphery. In particular, electrical stimulation to the fourth ventricle inhibits the action potential recorded at the round window (Galambos, 1956) in response to acoustic clicks, the discharge rate of auditory nerve neurons and the endocochlear potential, and enhances cochlear microphonics (Wiederhold and Kiang, 1970 ; Fex, 1959). The inhibitory e¡ects described and attributed to the MOCS are blocked by strychnine (Fex, 1962 ; Desmedt and Monaco, 1961). Guinan and Gi¡ord (1988) have shown a decrease in a¡erent dis-

0378-5955 / 97 / $17.00 ß 1997 Elsevier Science B.V. All rights reserved PII S 0 3 7 8 - 5 9 5 5 ( 9 7 ) 0 0 1 3 6 - 6

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S. Maison et al. / Hearing Research 113 (1997) 89^98

90

charge after electrical stimulation to the fourth ven-

hearing thresholds after intravenous infusion of atro-

tricle.

pine, thought to block OHC cholinergic receptors. Be-

Several authors have used acoustic stimulation, as

sides these physiological data, the literature indicates

being closer to natural stimulation, to investigate the

that the variability in perception thresholds for detec-

olivocochlear

tion of tones in noise decreases in presence of contra-

bundle.

Fex

(1962)

showed

that

the

MOCS could be activated by acoustic stimulation and Bun ì o (1978) observed changes in the spontaneous auditory

nerve

activity

with

low-intensity

contralateral

lateral noise. Is EOAE amplitude variability modi¢ed by contralateral acoustic stimulation ? Is EOAE amplitude varia-

Johnstone

bility linked to individual variability in MOCS activa-

(1988) showed that CAS had similar e¡ects to those

tion ? The present study aimed, by means of EOAE

observed during electrical stimulation of the MOCS.

recordings in presence or absence of contralateral noise,

Folsom and Owsley (1987) showed, in humans, a sub-

to test whether EOAE amplitude variability depends on

stantial amplitude decrease in compound action poten-

MOCS activity.

acoustic

stimulation

(CAS).

Rajan

and

tial with CAS, an e¡ect which was abolished, in animals, by MOCS section (Liberman, 1989). Others have suggested that MOCS stimulation could modify the

2. Methods

acoustic distortion products which are now thought to re£ect OHC active micromechanical properties (Siegel

2.1. Subjects

and Kim, 1982 ; Mountain, 1980). More

recently,

various

studies

have

addressed

The study involved 31 subjects, of whom 20 were

MOCS functioning in humans. It has been demon-

healthy

strated that evoked otoacoustic emission (EOAE) am-

(mean þ S.D.)) with no history of auditory pathology

plitude can be reduced by CAS in humans (Maison et

and with normal audiometric functions (i.e. less than

al., 1997 ; Berlin et al., 1993 ; Ryan et al., 1991 ; Veuillet

10 dB loss between 250 Hz and 8000 Hz per octave

et al., 1991, 1992 ; Collet et al., 1990, 1992). Observed at

on pure tone audiogram). The other 11 subjects were

low contralateral stimulus intensities, this EOAE at-

patients who had been operated for vestibular neuro-

tenuation e¡ect cannot be explained exclusively in terms

(14

male,

6

female ;

age :

27.5 þ 6.6

years

tomy (n = 8 ; 3 male, 5 female ; age : 43.7 þ 12.6 years

of acoustic crosstalk or middle-ear re£ex. The most

(mean þ S.D.)) or for hemifacial spasm (n = 3 ; 2 male,

likely explanation of the e¡ect is that an acoustic stim-

1 female ; 30, 40 and 56 years old). The neurotomized

ulus in the contralateral ear activates MOCS projecting

patients had been operated for incapacitating vestibular

onto OHCs in the ipsilateral cochlea and that this acti-

disorders. Since the olivocochlear bundle exits the brain

vation alters OHC functioning, thought to be the gen-

with the vestibular division of the vestibulo-cochlear

erating mechanism for EOAEs.

nerve

In all previous studies of the e¡ect of CAS on

(Amesen,

1984 ;

Rasmussen,

1946),

vestibular

neurotomy is presumed to result in the sectioning of

EOAEs, the focus has been on the decrease in EOAE

olivocochlear

amplitude. However, careful inspection of the reported

Therefore, such patients provide a human model of

results indicates that, besides the reported EOAE am-

hearing without e¡erents to the cochlea. Hemifacial

plitude shift, there appears a decrease in EOAE ampli-

spasm patients are surgical control subjects. All of the

tude variability with CAS. Indeed, a previous study,

patients included in this study had recovered normal

which sought to show MOCS involvement in the con-

hearing, i.e. normal audiometry and normal tympanom-

tralateral suppression e¡ect, found greater EOAE am-

etry. Middle ear re£exes were present in both ears. No

plitude variability in the healthy ear of total unilateral

vertigo persisted after surgical intervention and the uni-

hearing loss subjects than in the normal-hearing group

lateral peripheral vestibular disorder was con¢rmed by

(Collet et al., 1990). The authors suggested that the

nystagmographic recordings using the Ulmer Videonys-

absence of OHC motility modulation during CAS by

tagmoscope apparatus (Collin ORL), including exami-

e¡erent ¢bers could explain the greater variability ob-

nation of spontaneous horizontal optokinetic nystag-

served in the unilateral deafness group. Another study,

mus and of responses to the bithermal caloric test.

where showed

EOAEs that

were

EOAE

recorded amplitude

at

six

time

variability

e¡erent

¢bers

(Williams

et

al.,

1993).

intervals, decreased

2.2. Retrosigmoid approach

under CAS (Collet et al., 1992). Although standard deviations were computed, no statistical test of EOAE

All patients had been referred to the Otolaryngolog-

amplitude variability was performed, whereas a signi¢-

ical Department of the North Hospital of Marseille

cant amplitude decrease with CAS was observed. An-

(France) for surgical intervention. The surgical tech-

other previous study (Quaranta and Salonna, 1990),

nique used, for vestibular neurotomy and for hemifacial

using

tests,

spasm, was the retrosigmoid approach on a recumbent

showed a systematic increase in standard deviation of

patient, consisting of craniotomy limited to a 1.5 cm

EOAEs

and

cochlear

psychoacoustic

HEARES 2891 28-11-97

S. Maison et al. / Hearing Research 113 (1997) 89^98

91

trepanation behind the sigmoid sinus. The cerebellum

livered through a TDH 39 left earphone. The absolute

fell away spontaneously. In the case of vestibular neu-

threshold was measured preliminarily to enable stimu-

rotomy, the acoustic and vestibular nerves were sepa-

lus intensity setting at 30 dB SL.

rated and the vestibular division was sectioned (Magnan et al., 1991). In the case of hemifacial spasm, an

2.6. Procedure

endoscope allowed the irritative vascular contact to be distinguished from the normal arterial loop. The artery

2.6.1. EOAE amplitude variability

was carefully mobilized with the help of a microscope

EOAEs were recorded in the right ear for the healthy

and held away from the nerve with a te£on foam pad

control subjects, at an intrameatal stimulus intensity of

(Magnan et al., 1994).

60 þ 3 dB SPL. Three sets of EOAE recordings were made, with the following procedure : 10 recordings in

2.3. Audiometry and tympanometry

the the

Tonal audiometry was conducted in a sound-proof room

using

thresholds

a

Madsen

were

OB

measured

828 at

audiometer.

250,

500,

Hearing

1000,

2000,

4000 and 8000 Hz (according to ISO standards). Tympanometry was conducted in a sound-proof room using

absence

of

presence

CAS

of

(`PRE'),

then

contralateral

10

BBN

recordings

at

30

dB

in SL

(`CAS'), and ¢nally 10 recordings again in the absence of CAS (`POST'). For each set of recordings, the standard

deviation

(S.D.)

of

EOAE

amplitude

was

com-

puted. For all patients, the above protocol was applied in both ears. The ear in which EOAEs were recorded is

an Amplaid 702 impedancemeter.

hereafter called `ipsilateral'. The opposite ear, in which

2.4. Recording and analysis of the EOAEs

the BBN was presented, is called `contralateral'. Moreover, in patients, one ear was designated `healthy' and

EOAEs were recorded and analyzed according to the methodology Stimulus

proposed

presentation,

by

Bray

data

and

recording

Kemp and

the other `operated'.

(1987).

averaging

2.6.2. EOAE amplitude variability and reduction

were carried out using the Otodynamics ILO88 soft-

The quanti¢cation of EOAE amplitude attenuation

ware and hardware. The probe comprised a Knowles

during CAS was in terms of the `equivalent attenuation'

1843 microphone and a BP 1712 transmitter, both em-

èry-Croze et (EA) used by Veuillet et al. (1991) and Che

bedded in a plastic ear plug. Stimulus was an un¢ltered

al. (1994). EA is de¢ned as the mean reduction in stim-

click of 80

duration. The stimulus presentation rate

ulus amplitude required to elicit the same reduction in

was 50 Hz. The analysis time was 20 ms. 512 responses

EOAE amplitude as obtained with the 30 dB SL con-

were averaged.

tralateral noise. Five stimulus intensities (from 60 to 72

The

Ws

linear

di¡erential

cochlear

echo

method

was

dB SPL in 3 dB steps) gave ¢ve pairs (with and without

employed. This technique uses a combination of four

CAS)

acoustic impulses of the same amplitude and the same

order of presence/absence of contralateral noise were

of

EOAE

amplitudes.

Stimulus

intensities

and

polarity. In this condition, the meatal and middle ear

randomized.

in-

Two subgroups were de¢ned according to EA value :

crease with stimulus level. Therefore, a low intrameatal

group A, subjects with EA less than the median EA :

stimulus level (60 þ 3 dB SPL) was used and the ¢rst

n = 10

(6 male, 4 female ; age : 28.5 þ 6.6 years), mean

2.5 ms or the ¢rst 8 ms of the response were excluded.

EA =

0.54 þ 0.36 dB ; group B, subjects with EA great-

The

er than the median EA :

echoes

are

not

self-canceling

intensity of

and

the maximum

their

durations

pressure excursion of

the stimulus waveform, expressed in dB SPL, was meas-

3

n = 10

26.4 þ 6.8 years), mean EA =

3

(8 male, 2 female ; age :

1.38 þ 0.24 dB.

ured in the outer ear canal (intrameatally). For spec-

The di¡erences between S.D. (PRE) and S.D. (CAS)

trum analysis, a pass band of 500^6000 Hz was em-

and that between S.D. (POST) and S.D. (CAS) were

ployed.

calculated in order to test for a relationship between

In all normal-hearing subjects, EOAEs were recorded

these values and those of EA in control subjects.

in the right, `ipsilateral', ear. In patients operated with the retrosigmoid approach, EOAEs were recorded in both ears. For all the subjects, EOAE amplitude was computed from the whole response (i.e. 2.5^20 or 8^20

2.6.3. E¡ect of ipsilateral stimulus intensity on EOAE variability This experiment aimed to determine the e¡ect of ipsilateral stimulus intensity on EOAE variability. It in-

ms).

volved 15 subjects (8 male, 7 female ; 28.7 þ 8.0 years

2.5. Contralateral acoustic stimulation

old). 10 EOAE recordings were performed at 3 intrameatal stimulus intensities : 60, 63 and 66 dB SPL. For

The

CAS

consisted

of

a

broad-band

noise

(BBN)

generated using a Madsen OB 828 audiometer and de-

each stimulus intensity, EOAE amplitude SD was calculated.

HEARES 2891 28-11-97

S. Maison et al. / Hearing Research 113 (1997) 89^98

92

3.1.1. Group A : EA less than control median

2.6.4. In£uence of the `middle-ear echo'

The in£uence of the middle-ear was studied using a

(

time window analysis of 8^20 ms. The same protocol as described in Section 2.6.1 was performed once again.

6

2.5^20

decrease

1.05 dB) ms

was

window :

while a statistically signi¢cant

observed

in

CAS (ANOVA, F = 5.165, P

EOAE

6

amplitude

during

0.05), no statistically sig-

ni¢cant shift in EOAE amplitude S.D. was obtained

2.7. Measurements and statistics

Statistical analysis was performed using

0 Sigmastat

with CAS (ANOVA, F = 2.98, NS). 8^20

ms

window :

a highly signi¢cant decrease in

analysis of variance (ANOVA) for repeated measures.

EOAE amplitude was observed during CAS (Friedman 2 repeated measures ANOVA on ranks : = 9.3,

These parametric procedures were applied when the re-

P

sults were normally distributed. If not, non-parametric

EOAE amplitude S.D. was obtained with CAS (AN-

test was used (Friedman repeated measures ANOVA on

OVA, F = 0.366, NS).

software (version 1.02) and included linear regression,

M

= 0.009), whereas no statistically signi¢cant shift in

ranks). 3.1.2. Group B : EA greater than control median (

s

1.05 dB)

2.5^20 ms window :

3. Results

EOAE amplitude decreased stat-

istically during CAS (ANOVA, F = 13.82, P 3.1. EOAE amplitude variability with contralateral broad-band noise

did P

6

EOAE

amplitude

(ANOVA,

0.001), as F

= 3.67,

0.05).

8^20 ms window :

Fig. 1 shows EOAE amplitude means (left) and S.D.s

S.D.

6

EOAE amplitude decreased during

CAS,

CAS (Friedman repeated measures ANOVA on ranks : 2 = 11.2, P = 0.004), as did, once again, EOAE ampli-

POST) in control subjects. EOAE amplitudes were an-

tude S.D. with a higher statistical signi¢cance level

alyzed with a 2.5^20 ms (black symbols) or 8^20 ms

(Friedman repeated 2 = 9.5, P = 0.009).

(right)

calculated

for

three

(white symbols) time window.

conditions

(PRE,

M

M

measures

ANOVA

on

ranks :

Fig. 1. Comparison of EOAE amplitude and EOAE amplitude variability without (PRE and POST) and with (CAS) contralateral 30 dB SL BBN. Normal-hearing subjects were divided into two groups : group A (top), subjects with EA equal to or less than the median (i.e. 1.05 dB) ; group B (bottom), subjects with EA greater than the median. Mean EOAE relative amplitude (left) and its S.D. (right) are described. EOAE amplitude and S.D. were computed for two di¡erent time windows, i.e. 2.5^20 ms (black) and 8^20 ms (white). Mean EOAE amplitude for condition PRE, analyzed on a time window of 2.5^20 ms, equals 0 dB. Bars indicate standard errors.

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S. Maison et al. / Hearing Research 113 (1997) 89^98

93

Fig. 2. Comparison of EOAE amplitude and EOAE amplitude variability without and with CAS in neurotomized subjects. EOAE relative amplitude (left) and S.D. (right) are described for healthy and operated ears. Mean EOAE amplitude for condition PRE = 0 dB. Bars indicate standard errors of the EOAEs.

3.1.3. EOAE variability in vestibular neurotomy patients The left side of Fig. 2 shows EOAE amplitudes recorded in both ears. While CAS induced EOAE amplitude attenuation in the healthy ear (ANOVA,

F = 6.964,

P

6

0.01), no such attenuation was observed on the

opposite

side,

F = 0.077,

NS). The right side of Fig. 2 shows EOAE

i.e.

in

the

operated

ear

(ANOVA,

amplitude S.D.s. While no statistically signi¢cant di¡erence was found between the three conditions (PRE, CAS, POST) in the operated ear (ANOVA,

Table 1 Correlations between EA and EOAE amplitude and between EA and EOAE variability Correlation between EA and

Correlation between EA and

EOAE amplitude

EOAE variability

PRE

r P n

F=0.665,

NS), a signi¢cant CAS e¡ect was found in the healthy

CAS

POST

ear (Friedman repeated measures ANOVA on ranks : 2 = 9.000, P = 0.01).

M

3.2. Surgical controls (hemifacial spasm patients)

PRE

CAS

POST

3

3

3

0.071

0.466

0.293

Fig. 3 shows EOAE amplitude, recorded in both ears

0.281

0.322

0.246

0.768

0.038*

0.211

20

20

20

20

20

20

for the three subjects. A decrease in EOAE amplitude

0.253

0.234

0.272

during CAS was found in both ears. However, due to

HEARES 2891 28-11-97

S. Maison et al. / Hearing Research 113 (1997) 89^98

94

Fig. 3. Comparison of EOAE amplitude and EOAE amplitude variability without and with CAS in subjects operated for hemifacial spasm. EOAE relative amplitude (left) and S.D. (right) are described for healthy and operated ears. Mean EOAE amplitude for condition PRE = 0 dB. Bars indicate standard errors of the EOAEs.

the small number of subjects (n = 3), no statistical tests

S.D. (CAS) (top) and as a function of S.D. (POST)

could be performed. The right side of Fig. 3 shows a

minus S.D. (CAS) (bottom). This ¢gure shows that in

decrease in EOAE amplitude as well as a decrease in

both

S.D., found in both ears.

linked EA and EOAE variability expressed by di¡er-

cases

a

statistically

signi¢cant

linear

relation

ences between S.D.s obtained in the two conditions

3.3. Correlation between EA and EOAE amplitude/ EOAE amplitude variability in control subjects

(without or with CAS). Both ¢gures show that the larger the EA, the more the EOAE amplitude variability was reduced with CAS.

Table 1 shows correlations between EA and EOAE amplitude/EAOE amplitude variability with or with-

3.4. In£uence of ipsilateral stimulus intensity

out CAS. Whereas no statistically signi¢cant correlation between EOAE amplitude and EA can be found

Fig. 5 shows EOAE amplitude S.D.s from 10 record-

whatever the condition (with or without CAS), only

ings with ipsilateral stimulus intensities of 60, 63 and 66

one

variabil-

dB SPL, respectively. This ¢gure shows that the higher

(r = 0.47,

the ipsilateral stimulus intensity, the greater the mean

correlation

ity

and

P

0.05).

6

EA

between

can

be

EOAE

found

amplitude

during

CAS

EOAE amplitude and the smaller the EOAE amplitude

Fig. 4 shows EA as a function of S.D. (PRE) minus

S.D.

HEARES 2891 28-11-97

S. Maison et al. / Hearing Research 113 (1997) 89^98 both

subgroups

95

showed

statistically

signi¢cant

de-

creases in EOAE amplitude under contralateral noise stimulation, only subjects with strong MOCS activity, i.e.

EA

equal

to

or

greater

than

the

median

EA

of

normal-hearing subjects (group B), showed a statistically signi¢cant decrease in EOAE amplitude variability.

The

following

discussion

aims

to

demonstrate

MOCS involvement in the e¡ects observed. A complementary experiment was performed in order to rule out interpretations based on a decrease in EOAE amplitude variability due to EOAE amplitude decrease. Indeed, EOAE amplitude variability was computed at three ipsilateral stimulus intensities. The results in Fig. 5 showed that the higher the ipsilateral stimulus intensity, the greater the EOAE amplitude while the less the

EOAE

amplitude

variability.

These

results

show

that EOAE amplitude variability decrease is not linked to a decrease in EOAE amplitude. Several factors are thought to act on EOAE amplitude : hearing sensitivity (Collet et al., 1989 ; Johnsen and Elberling, 1982 ; Kemp and Souter, 1978), ageing (Norton and Widen, 1990), noise exposure (Rossi et al., 1991), visual tasks or directed attention (Froehlich et al., 1990, 1993). In the present study, given the conditions described in Section 2, these e¡ects could not be involved in the variability decrease with CAS. Other `technical factors' known to induce changes in EOAE amplitude, such as probe position, ear canal pressure (Naeve et al., 1992 ; Robinson and Haughton, 1991) or

Fig. 4. EA as a function of S.D. suppression. The S.D. suppression e¡ect and

was

with

described (CAS)

a

by

S.D.

CAS.

di¡erences

Linear

without

regression

was

(PRE

or

assessed

S.D. suppression e¡ect and EA. Correlation coe¤cient and

POST) between

P

value

are indicated.

4. Discussion

The main ¢nding of the present decrease

in

EOAE

amplitude

study concerns a

variability

under

CAS.

Two subgroups were formed within the group of normal-hearing subjects, to distinguish between those with

Fig. 5. EAOE amplitude and EOAE amplitude variability as a function of ipsilateral stimulus intensity. Mean EOAE amplitude (¢lled circles) and its S.D. (hollow bars) for 10 recordings are indicated ac-

good and poor MOCS functioning under CAS. EA was

cording to ipsilateral stimulus intensity. Bars indicate standard er-

taken as a quanti¢cation of MOCS activity. Whereas

rors of the EOAEs.

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S. Maison et al. / Hearing Research 113 (1997) 89^98

96

Another important point may be added to the fore-

posture (Wilson, 1980), can also be ruled out since these

going. MOCS activity, which can be quanti¢ed by EA,

factors were controlled in this experiment. Several previous studies have shown suppression of EOAE

amplitude

induced

by

contralateral

clicks

or

presented great intersubject variability (Giraud et al., 1995 ;

Collet

et

al.,

1992).

Fig.

4

clearly

shows

that

noises (Maison et al., 1997 ; Ryan et al., 1991 ; Veuillet

the greater the decrease in EOAE amplitude variability,

et al., 1991, 1992 ; Collet et al., 1990). This suppression

the greater the EA. This argues for MOCS involvement

e¡ect cannot be explained by either acoustic cross-talk

in the variability decrease with CAS.

or the acoustic re£ex, as no signi¢cant suppression ef-

Since EOAEs are thought to re£ect OHC rapid mo-

fect was observed when Veuillet et al. (1991) applied

tility, the present study, showing signi¢cant amplitude

contralateral sound stimulation to patients presenting

and variability decreases under MOCS activation, indi-

total

fact that

cates an involvement of the MOCS in the stabilization

the suppression e¡ect persists in human subjects with

of OHC motility. This result con¢rms that of LePage

unilateral

1991)

(1989), who linked the olivocochlear bundle to a motor

rules out interpretations based on an exclusive involve-

unit control system in the mammalian cochlea. Due to

ment of the middle ear. The frequency speci¢city in-

the present lack of data, the exact mechanism under-

volved in the suppression e¡ect (Liberman, 1989) adds

lying the stabilization of OHC motility remains specu-

a further argument against middle ear e¡ects. It seems

lative. Nevertheless, it is noteworthy that the main neu-

likely that meatal and middle ear echoes become small-

rotransmitter

er using a time window analysis of 2.5^20 ms, but a

(Kujawa

possible

1974). Several previous studies have shown that ACh

unilateral hearing

stapedial

remnant

loss.

re£ex

may

Moreover,

loss

(Veuillet

the

et

al.,

be still adding signi¢cantly to

et

in

MOCS

al.,

1992 ;

¢bers

is

Bobbin

acetylcholine and

(ACh)

Konishi,

1971,

excluded

infusion on in vitro OHCs induces cell membrane hy-

can be increased so as to present a time window anal-

perpolarization (Fuchs et al., 1983 ; Ashmore and Rus-

ysis of 8^20 ms, known to exclude all of the `middle-ear

sell, 1982) by means of potassium current (Art et al.,

echo'. Similar results were observed and con¢rmed that

1984).

the SD decrease under CAS is not an exclusively mid-

hance second messenger production involved in the in-

dle-ear e¡ect.

crease

the

EOAE

value.

The

post-click

duration

EOAEs represent a means of functional exploration of

OHC

active

micromechanical

properties.

E¡erent

The

in

ACh-cholinergic

intracellular

constitutes

MOCS,

as

Brown,

OHC motility.

modifying

suggested OHC

that

motility

CAS

excites

(Liberman

the and

As

a

should

en-

consequence,

a

loop for rapid OHC motility. This negative feedback

It

been

calcium.

link

slow OHC contraction is induced and forms a control

MOCS ¢bers contact the basolateral OHC membrane. has

receptor

a

a

resonator

consequence,

for

could

rapid

OHC

decrease

the

motility

and,

variability

of

1986). Our results con¢rm this and specify that, during

This demonstrated ability of MOCS ¢bers provides a

CAS, MOCS inhibits OHC motility. As a consequence,

basis for one of the possible roles of the MOCS. By

EOAE amplitude is reduced under CAS, with a reduc-

reducing the variability in the responses of the periph-

tion of OHC motility variability.

eral auditory system to incoming signals, MOCS acti-

During vestibular neurotomy the MOCS is sectioned,

vation should result in an improvement in the encoding

since e¡erent ¢bers travel along the vestibular division

of signals presented at threshold in background noise as

of the eight nerve. Neurotomized subjects are taken to

recently observed in a previous study (Micheyl and Col-

represent

let, 1996).

an

interesting

human

model,

where

the

MOCS can be assumed not to act on the auditory periphery. The normal ears in our neurotomized patients presented a functioning non-sectioned MOCS with regard to EOAE amplitude and EOAE amplitude variability, a statistically signi¢cant decrease being observed during CAS. On the other hand, no such e¡ect was observed

for

either

factor

tested

in

this

References Amesen, A.R., 1984. Fiber population of the vestibulocochlear anastomosis in humans. Acta Otolaryngol. (Stockh). 98, 501^518.

experiment

Art, J.J., Fettiplace, R., Fuchs, P.A., 1984. Synaptic hyperpolarization

when EOAEs were recorded in the operated ear. The

and inhibition of turtle cochlear hair cells. J. Physiol. 356, 525^

retrosigmoid approach used in the surgical procedure cannot be linked to the results observed in the operated

550. Ashmore, J.F., Russell, I.J., 1982. E¡ect of e¡erent nerve stimulation on hair cells in the frog sacculus. J. Physiol. 329, 26^27P.

ear. Indeed, patients with hemifacial spasm, in whom

Berlin, C.I., Hood, L.J., Szabo, P., Cecola, R.P., Rigby, P., Jackson,

the same approach was used, showed a decrease in both

D.F., 1993. Contralateral suppression of non-linear click-evoked

factors tested. Unfortunately, the small number of subjects (

n = 3)

did not permit statistical testing. Neverthe-

less, the results in neurotomized subjects clearly argue

otoacoustic emissions. Hear. Res. 71, 1^11. Bobbin, R.P., Konishi, T., 1971. Acetylcholine mimics crossed olivocochlear bundle stimulation. Nature 231, 222^223. Bobbin, R.P., Konishi, T., 1974. Action of cholinergic and anticholi-

for MOCS involvement in EOAE amplitude variability

nergic drugs at the crossed olivocochlear bundle-hair cell junction.

decrease.

Acta Otolaryngol. 77, 656^665.

HEARES 2891 28-11-97

S. Maison et al. / Hearing Research 113 (1997) 89^98 Bray, P., Kemp, D.T., 1987. An advanced cochlear echo technique suitable for infant screening. Br. J. Audiol. 21, 191^204.

97

cochlear feedback : suppression of compound action potentials by contralateral sound. Hear. Res. 39, 47^56.

Buno, W., 1978. Auditory nerve activity in£uenced by contralateral ear sound stimulation. Exp. Neurol. 59, 62^74.

Liberman, M.C., Brown, M.C., 1986. Physiology and anatomy of single olivocochlear neurons in the cat. Hear. Res. 24, 17^36.

è ry-Croze, S., Moulin, A., Collet, L., Morgon, A., 1994. Is the test Che

Magnan, J., Bremond, G., Chays, A., Gignac, D., Florence, A., 1991.

of medial e¡erent system function a relevant investigation in tin-

Vestibular neurotomy by retrosigmoid approach : technique, indi-

nitus ? Br. J. Audiol. 28, 13^25.

cations and results. Am. J. Otol. 12, 101^105.

Collet, L., Garten, M., Moulin, A., Kau¡mann, I., Disant, F., Mor-

Magnan, J., Chays, A., Lepetre, C., Pencro¤, E., Locatelli, P., 1994.

gon, A., 1989. Evoked otoacoustic emissions and sensorineural

Surgical perspectives of endoscopy of the cerebellopontine angle.

hearing loss. Arch. Otolaryngol. Head Neck Surg. 115, 1060^1063.

Am. J. Otol. 15, 366^370.

Collet, L., Kemp, D.T., Veuillet, E., Duclaux, R., Moulin, A., Mor-

Maison, S., Micheyl, C., Collet, L., 1997. Medial olivocochlear e¡er-

gon, A., 1990. E¡ects of contralateral auditory stimuli on active

ent system in humans studied with amplitude-modulated tones.

cochlear micromechanical properties in human subjects. Hear. Res. 43, 251^262.

J. Neurophysiol. 77, 1759^1768. Micheyl, C., Collet, L., 1996. Involvement of the olivocochlear bundle

Collet, L., Veuillet, E., Bene, J., Morgon, A., 1992. E¡ects of contralateral white noise on clicks evoked emissions in normal and sensorineural ears : towards an exploration of the medial olivocochlear system. Audiology 31, 1^7.

in the detection of tones in noise. J. Acoust. Soc. Am. 3, 1604^ 1610. Mountain,

D.C.,

1980.

Changes

in

endolymphatic

potential

and

crossed olivocochlear bundle stimulation alter cochlear mechanics.

Desmedt, J.E., Monaco, P., 1961. Mode of action of the e¡erent olivo-cochlear bundle on the inner ear. Nature 192, 1263^1265. Fex, J., 1959. Augmentation of the cochlear microphonics by stimulation of e¡erent ¢bers to cochlea. Acta Otolaryngol. 50, 540.

Science 210, 71^72. Naeve, S.L., Margolis, R.H., Levine, S.C., Fournier, E.M., 1992. Effect of ear-canal air pressure on evoked otoacoustic emissions. J. Acoust. Soc. Am. 91, 2091^2095.

Fex, J., 1962. Auditory nerve activity in centrifugal and centripetal

Norton, S.J., Widen, J.E., 1990. Evoked otoacoustic emissions in

cochlear ¢bers in cat. A study of a feedback system. Acta Physiol.

normal-hearing infants and children : emerging data and issues.

Scand. 55 (Suppl. 189), 1^72.

Ear Hear. 11, 121^127.

Folsom, R.L., Owsley, R.M., 1987. N1 action potentials in humans.

Quaranta, A., Salonna, I., 1990. Evoked otoacoustic emissions and

In£uence of simultaneous contralateral stimulation. Acta Otolar-

cochlear psychoacoustic tests : e¡ects of atropine. In : Grandori,

yngol. 103, 262^265.

F., Cianfrone, G., Kemp, D.T. (Eds.), Cochlear Mechanisms

Froehlich, P., Collet, L., Chanal, J.M., Morgon, A., 1990. Variability of the in£uence of a visual task on the active micromechanical properties of the cochlea. Brain Res. 508, 286^288.

and Otoacoustic Emissions. Advances in Audiology, Vol. 7. Karger, Basel, pp. 171^179. Rajan, R., Johnstone, B.M., 1988. Binaural acoustic stimulation ex-

Froehlich, P., Collet, L., Morgon, A., 1993. Transiently otoacoustic

ercises protective e¡ects at the cochlea that mimic the e¡ects of

emissions amplitudes change with changes of directed attention.

electrical stimulation of an auditory e¡erent pathway. Brain Res.

Physiol. Behav. 53, 679^682.

459, 241^255.

Fuchs, P.A., Fettiplace, R., Crawford, A.C., Art, J.J., 1983. In : Klinke, R., Hartmann, R. (Eds.), Hearing ^ Physiology and Psychophysical Basis. Springer-Verlag, Berlin, pp. 25^31.

Rasmussen,

G.,

1946.

The

olivary

peduncle

and

other

¢bre

projections of the superior olivary complex. J. Comp. Neurol. 84, 141^219.

Galambos, R., 1956. Suppression of auditory nerve activity by stim-

Robinson, P.M., Haughton, P.M., 1991. Modi¢cation of evoked oto-

ulation of e¡erent ¢bers to cochlea. J. Neurophysiol. 19, 424^437.

acoustic emissions by changes in pressure in the external ear. Br.

è ry-Croze, S., Magnan, J., Chays, A., Giraud, A.L., Collet, L., Che

J. Audiol. 25, 131^133.

1995. Evidence of a medial olivocochlear involvement in contra-

Rossi, G., Solero, P., Rolando, M., Olina, M., 1991. Recovery time of

lateral suppression of otoacoustic emissions in humans. Brain Res.

the temporary threshold shift for delayed evoked otoacoustic emis-

705, 15^23.

sions and tone bursts. Otorhinolaryngology 53, 15^28.

Guinan, J.J., Gi¡ord, M.L., 1988. E¡ects of electrical stimulation of

Ryan, S., Kemp, D.T., Hinchcli¡e, R., 1991. The in£uence of con-

e¡erent olivocochlear neurons on cat auditory-nerve ¢bers. I. Rate-

tralateral acoustic stimulation on click-evoked otoacoustic emis-

level functions. Hear. Res. 33, 97^114.

sions in humans. Br. J. Audiol. 25, 391^397.

Guinan, J.J., Jr., Warr, W.B., Norris, B.E., 1983. Di¡erential olivo-

Siegel, J.H., Kim, D.O., 1982. E¡erent control of cochlear mechanics.

cochlear projections from lateral vs medial zones of the superior

Olivocochlear bundle stimulation a¡ects cochlear biomechanical

olivary complex. J. Comp. Neurol. 221, 358^370.

non-linearity. Hear. Res. 6, 172^182.

Guinan, J.J., Jr., Warr, W.B., Norris, B.E., 1984. Topographic organ-

Veuillet, E., Collet, L., Duclaux, R., 1991. E¡ect of contralateral

ization on the olivocochlear projections from the lateral and me-

auditory stimulation on active cochlear micromechanical proper-

dial zones of the superior olivary complex. J. Comp. Neurol. 226,

ties in human subjects : dependence on stimulus variables. J. Neu-

21^27.

rophysiol. 65, 724^735.

Johnsen, N.J., Elberling, B., 1982. Evoked acoustic emissions from

Veuillet, E., Collet, L., Morgon, A., 1992. Di¡erential e¡ects of ear-

the human ear. II. Normative data in young adults and in£uence

canal pressure and contralateral acoustic stimulation on evoked

of posture. Scand. Audiol. 11, 69^77.

otoacoustic emissions in humans. Hear. Res. 61, 47^55.

Kemp, D.T., Souter, M., 1978. Stimulated acoustic emissions from

Warr, W.B., 1975. Olivocochlear and vestibular e¡erent neurons of

within the human auditory system. J. Acoust. Soc. Am. 64,

the feline brain stem : their location, morphology, and number

1386^1391.

determined by retrograde axonal transport and acetylcholinester-

Kujawa, S.G., Glattke, T.J., Fallon, M., Bobbin, R.P., 1992. Intracochlear application of acetylcholine alters sound-induced mechanical events within the cochlear partition. Hear. Res. 61, 106^116.

ase histochemistry. J. Comp. Neurol. 161, 159^182. Warr, W.B., Guinan, J.J., Jr., 1979. E¡erent innervation of the organ of Corti : two separate systems. Brain Res. 173, 152^155. Warr, W.B., Guinan, J.J. Jr., White J.S., 1986. Organization of the

Lepage, E.L., 1989. Functional role of the olivo-cochlear bundle : a

e¡erent ¢bers : the lateral and medial olivocochlear systems. In :

motor unit control system in the mammalian cochlea. Hear. Res.

Altschuler, R.A., Ho¡man, D.W., Bobbin, R.P. (Eds.), Neurobi-

38, 177^198.

ology of Hearing : The Cochlea. Raven, New York, pp. 333^348.

Liberman, M.C., 1989. Rapid assessment of sound-evoked olivo-

Wiederhold, M.L., Kiang, N.Y.S., 1970. E¡ects of electrical stimula-

HEARES 2891 28-11-97

98

S. Maison et al. / Hearing Research 113 (1997) 89^98 tion of the crossed olivocochlear bundle on single auditory-nerve ¢bers in the cat. J. Acoust. Soc. Am. 48, 950^965.

Wilson, L.P., 1980. Evidence for a cochlear origin for acoustic reemissions, threshold ¢ne-structure and tonal tinnitus. Hear. Res.

Williams, E.A., Brookes, G.B., Prasher, D.K., 1993. E¡ect of con-

2, 233^252.

tralateral acoustic stimulation on otoacoustic emissions following vestibular neurotomy. Scand. Audiol. 22, 197^203.

HEARES 2891 28-11-97