ffeunng Research, 48 (1990) 209-220
Elsevier
209
HEARES 01448
Electrophysiolo~cal aspects of the middle ear muscle reflex in Latency, rise time and effect on sound transmission
H. van den Berge, H. Kingma, C. Kluge and E.H.M.A. Marres Department oj Otorhinolmyngology. Uniwrsity Hospital, Maastricht, The Netherlands
(Received 15 June 1989; accepted 25 April 1990)
the rat:
The latency, the rise time and the influence of the acoustic reflex on sound transmission were investigated in the adult rat during
ketamin anaesthesia. This was done by recordings of the cochlear microphonics (CM) and electromyographic (EMG) recordings of
the reflex responses of the tensor tympani muscle. The acoustic reflex was elicited by contralateral acoustic stimuli of which the
intensity and frequency was varied. Ipsiiaterally, the effect on sound transmission was determined by estimating the change in
amplitude of the CM’s of ipsilateral administered subliminal stimuli. It was shown that both the tensor tympani muscle and the
stapedius muscle contribute in the refIex. The latency as well as the rise time of the reflex determined by CM recordings showed to be
short (minimal values: 12 and 7 ms respectively). The mean latency of the tensor tympani muscle reflex. measured by EMG, was
about 7 ms. The attenuation of 0.25-8 kHz tone bursts upto 115 dB SPL is limited to a mean maximum of 15 dB SPL. The maximal
attenuation was shown to occur at 1 kHz. Frequencies above 2 kHz appeared to be the best elicitor of the middle ear muscle reflex.
Middle ear muscle reflex; Latency: Contraction time; Attenuation; Electromyography
Introduction
The middle ear muscle reflex has been the subject of research for many years. This has led to
various speculations on the function of the reflex. One of the most attractive theories is that the
middle ear muscles protect the inner ear from noise damage. However, several objections to this
theory have been made (for references see Bosatra et al., 1984). Firstly, the latency of the reflex is
thought to be too long to protect effectively against impact noise. Secondly, the attenuation of sound transmission as a result of contraction of the muscles would be limited. Finally, a process of
fatigue, which occurs during exposure to noise over a longer period of time, would restrict the
protective value of the reflex. Experiments on these subjects have been intensive, but often frag- mentary. and they were performed using different
Correspondence too: H. van den Berge, University Hospital
Maastricht, Department of Otorhinolaryngology, Postbox 1918.
6201 BX Maastricht, The Netherlands,
animal species. Since major interspecies dif- ferences exist in both structure and function of the
middIe ear muscles, an integrated mo~holo~cal and electrophysiological study in one animaf
species would be required. Therefore, we initiated such an integrated study in the rat. The morpho-
logical characteristics of both the tensor tympani and stapedius muscles have already been pre-
sented (Berge and Wirtz, 1989a; Berge and Wirtz, 1989b; Berge and Wal, 1990). These studies
showed that both muscles are able to contract fast, that they have a high fatigue resistance and a well developed motor innervation pattern together with a probably absent sensory innervation.
Concerning the noise protection theory im- portant characteristics to be investigated would be the latency, the rise time, the quantitative effect on sound transmission and the fatiguability of the reflex. In the past, the effect on sound transmis- sion was usually estimated in an artificial situation for example during and after recovery of stapedius muscle paralysis (Borg, 1968; Borg and Zakrisson, 1974; Zakrisson, 1979) and by electrical stimula-
0378-5955/90/$03.50 IQ 1990 Elsevier Science Publishers B.V. (Biomedical Division)
210
tion of the muscles or brainstem nuclei (Moller, 1965; Teig, 1973). Furthermore, the quantitative effect on sound transmission has often been de-
rived indirectly from contraction force studies
(Wever and Bray, 1937, 1942; Teig, 1972a) and
masking studies (Borg and Zakrisson, 1974). The latency of the acoustic reflex has mostly been
determined by the relatively indirect method of
acoustic impedance measurements (see for refer- ences Bosatra et al., 1984). Finally not much is known about the rise time of the reflex, which is here defined as the time lapse between the begin- ning and the moment of maximal effect on sound transmission, measured at the level of the cochlea. This characteristic, which is a measure for the
contraction time of the muscles, determines, to- gether with the latency how fast sound transmis-
sion can be influenced. We therefore set out to investigate the latency,
rise time and quantitative effect on sound trans- mission of the acoustic reflex in the rat by direct
methods, leaving the middle ear muscles and their
inne~ation intact.
Materials and Methods
Surgical procedures
Ten twelve week old male Lewis rats were anesthesized with ketamin (Vetalar”), as this drug is assumed not to influence the middle ear muscle reflex (Bosatra et al., 1984). Following administra- tion of 1.3 ml/kg bodyweight of Vetalar@ i.p., the
anaesthesia was maintained by 0.1 ml Vetalar@ i.m. every 30 min. The tympanic bulla was ex-
posed by a retroaural approach, leaving the outer ear canal intact. The rats were placed in a fixator
especially designed for this purpose. Body temper- ature was controlled at 38*C via a feed back
heating system attached to the fixator. For acous- tic stimulation, Nicolet Model TIP-300 trans- ducers with a tube length of 25 cm were used on both sides, the ends of which were inserted till close to the tympanic membrane. During stimula- tion the outer ear canal was completely sealed by the tube. For measuring cochlear microphonics (CM), a silver ball electrode (0 0.8 mm) was inserted through a small hole made in the bulla and placed on the promontory close to the round window niche. This was done using a micromani-
pulator and operation stereo microscope. For se- cording electromyograms (EMG) a silver wire
electrode was placed on the belly of the tensor
tympani muscle. In both cases a reference elec-
trode and a ground electrode were placed in the
muscles near the bulla and in a hind limb, respec- tively.
Experiments were performed in a total number
of ten rats. Control measurements during total muscular relaxation by Pavulon9Vetalar” intuba- tion anesthesia and by tenotomy of the tensor tympani muscle were performed in two rats. Con- traction of the tensor tympani muscle was moni- tored during all experiments by direct inspection using the operation microscope.
Acou.~tic stimulation
Acoustic stimuli were administered contralater- ally (i.e. the nonoperated ear) and ipsilaterally (i.e.
the operated ear). In general, both ears were stimulated simultaneously, the contralateral stimu-
lus to induce a (bilateral~ middle ear muscle con-
traction and the ipsilateral to determine effects of the contraction on sound transmission, the latency
and the rise time of the reflex (see below). The ipsilateral stimuli were generated by a Nicolet CA-2000 and the contralateral stimuli by an Acoustics AC3 audiometer or the Nicolet CA- 2000. The stimulus parameters indicated in this study (intensity, duration, frequency, envelope, repetition rate) refer to the output characteristics
of the transducer tubes (Nicolet Model TIP-300). Acoustic stimuli were calibrated for each trans-
ducer tube by using a 2 cc Bruel and Kjaer DB- Ol38 coupler and expressed in terms of dB re 20
Pa (SPL). At 500 Hz, 118.5 dBSPL, 1.4% distor- tion was measured. In all experiments the Nicolet
CA 2OOO was used for data-acquisition and signal processing. The bandwidth during registration of the CM was 150 Hz-10 kHz (low and high pass filters 12 dB/octave).
Several experiments were performed to de- termine (a) the relation between CM amplitude and stimulus intensity at various frequencies, (b) the latency of the reflex, fc) the rise time of the reflex, (d) the effect of the reflex on sound trans- mission and (e) the most effective acoustic stimu- lus that elicits the middle ear muscle reflex.
211
In order to establish the relation between CM amplitude and stimulus intensity, 50 tone bursts with a plateau of 15 ms and a rise and fall time of
I ms. were given at a repetition rate of 0.3 Hz or 3.1 Hz. The responses were averaged. Measure-
ments were done at various frequencies (0.25. 0.5. 1.0, 1.5, 2.0, 4.0, 8.0 kHz) and with increasing
stimulus intensity (37-112 dB SPL). The amph- tudes of the CM were determined at 4 ms after the
onset of the stimulus. All CM amplitudes in this
study were measured peak to peak.
The latency and rise time of the reflex were determined from the change in the averaged CM
amplitudes following ipsilateral acoustic stimula-
tion above the reflex threshold (i.e. 50 tone bursts of 50 ms. 87-112 dB SPL. 0.25-8 kHz, repetition rate 3.1 or 0.3, rise- and fall time 1 ms). The
latency was estimated from the time between the beginning of the stimulus and beginning of the change in CM amplitude. A change in CM ampli-
tude was considered to be significant when it was larger than 10%. The rise time was estimated from the time between the beginning and the end of the
change in CM amplitude. To determine the effect of the middle ear muscle
reflex on sound transmission, contralateral acous- tic stimuli were given to elicite a (bilateral) reflex.
Ipsilaterally. the effect of the contraction on sound transmission was determined by measuring the
difference of the averaged CM amplitude of a
sub-threshold ipsilateral stimulus (see below) with and without contralateral stimulation. The con- tralateral stimuli were administered manually from
0.5- 1.0 s prior to. till 0.5-1.0 s after the ipsilater- ally administered tone bursts. The ipsilateral
stimulus consisted of 50 tone bursts of 67 dB SPL (i.e. below the reflex threshold) administered with a repetition rate of 3.1 Hz at various frequencies (0.25, 0.5. 1, 1.5. 2, 4 and 8 kHz). An intensity of 67 dB SPL was chosen since this induced a CM with a good signal to noise ratio, the stimulus did not elicit an middle ear muscle contraction, and the stimulus CM amplitude response curve showed to be linear around this intensity (see results). To quantify a possible subthreshold facilitation (Sim-
mons, 1965; Blood and Greenburg, 1981) of the 67 dBSPL stimulus, measurements with a stimuli of 57 dB at 1, 1.5, 2 and 4 kHz were done in two animals (see results). The CM amplitude without
contralateral stimulation was measured before as well as following contralateral stimulation to check for reproducibility and cochlear damage. Only those data sets were used for analysis of which
these two CM amplitudes without contralateral stimulation showed a test-retest variation of less
than 5%. The effectiveness of contralateral stimuli in
eliciting the middle ear muscle reflex was de-
termined from the difference in peak to peak CM amplitude of an ipsilateral administered stimulus
of 67 dB SPL and 1.5 kHz (50 tone bursts of 15
ms, repetition rate 3.1 Hz) with and without the
contralateral eliciting stimulus. Ipsilaterally. 1.5 kHz was chosen as this frequency appeared to be very sensitive (see results). The contralateral
stimulus was administered manually from 0.551.0 s prior to, till 0.5- 1 .O s after the ipsilaterally administered 50 tone bursts (frequency: 0.25. 0.5.
1. 1.5. 2. 4 and 8 kHz and intensity 65. 115 dB SPL). Again, reproducibility was taken within 5%‘.
Next to the estimation of the latency by CM recordings the latency of tensor tympani muscle reflex was investigated by EMG recordings. using
a silver wire surface electrode on the belly of the muscle. For data-acquisition and signal processing
the Nicolet CA 2000 was used. The bandwidth
during registration of the EMG was 300 Hz-10 kHz (low and high pass filters 12 dB/octave).
Contraction was induced by single ipsilateral stimuli with a duration of 15.-200 ms, frequency
of 0.5. 1.0, 1.5. 2 and 4 kHz and intensity varying from 27 to 107 dB SPL. The latency was de- termined from the time between beginning of the stimulus and the beginning of the muscular action potentials.
Results
Fig. 1 (trace a) shows a typical electrocochleo- gram induced by ipsilateral 1.5 kHz sinusoidal stimulation at 67 dB SPL. In the first two millisec-
onds the response shows a fast increase in ampli- tude, which was also seen at higher stimulus inten- sities. In this time lapse the response predomi- nantly reflects contributions of the nerve action potential and the CM. After a few milliseconds
212
I
0 7.5 1s m
Fig. 1. Examples of cochlear microphonics in the rat. (a) Averaged CM recording of a stimulus of 67 dB SPL 1.5 kHz; stimulus onset at t = 0 (stimulus duration: 50 ms; repetition frequency 3.1 Hz; number of stimuli: 50). (b) The same record- ing as in (a), during total muscular relaxation by Pavulot?-
Vetalar” anesthesia.
1OC
1C
2
the response amplitude decreases slightly and stabilizes. Then the sinusoidal changes of the
potentials most likely reflects the CM. It was not to be expected that the decrease in CM amplitude
at t = 2-3 ms was induced by the middle ear
muscles. Nevertheless we checked this by measur- ing the ECoch during total muscle relaxation by
anesthesia with Pavulon8. Regardless the stimulus intensity, the initial response pattern is the same
with and without total muscle relaxation (see trace b in Fig. 1).
In Fig. 2a the CM amplitude and the standard deviation (SD) (IV = 4) of a 1.5 kHz stimulus is plotted as a function of the stimulus intensity.
There is a linear relations~p upto 74 dB SPL, whereas above 74 dB SPL a saturation, and above
405080708090 loo 110 1M 30 40 50 60 70 80 90 loo 110 120
Sttmulus Intensity WEPL.) B
Stkn&us Freciuemcy Wizf
Stimulus lntensty UEXSFU
Fig. 2. Relation between stimulus intensity and CM amplitude. (a) Mean CM amplitude of a stimulus of 1.5 kHz as a function of the stimulus intensity. Vertical bars: +/- 1 SD (b) The same form as the previous for different frequencies (D----- 0: 0.5 kHz: A-A: 1 kHz: O- o: 1.5 kHz; 0 -0: 2 kHz; I- l : 4 kHz). (c) Sensitivity curve of the CM amplitude. The
curve represents the mean intensity required to induce a 15 nV CM amplitude as a function of stimutus frequency (a-c: N = 4)
87 dB SPL a diminuation occurs. There are only slight inter-individual differences in amplitudes
between the four rats. The relationship between the CM response amplitude and stimulus intensity depends on frequency as is shown in Fig. 2b. Fig.
2c shows the sensitivity curve of the CM ampli-
tude. The intensity required to induce an CM amplitude of 15 PV is plotted as a function of the
stimulus frequency. It can be seen that the maxi-
mal sensitivity is found at 1.5 kHz. At stimulus intensities above 77 dB SPL the response pattern appears to be less sinusoidal for most frequencies.
Furthermore, at these higher stimulus intensities (Fig. 3, trace a) the amplitude of the response
appears to decrease after about 15-30 ms depend-
ing on the stimulus intensity. The decrease itself takes about 5-15 ms. This response pattern is the
same at low (0.3 Hz) and at higher (3.1 Hz) stimulus repetition rates. This suggests that at
these repetition frequency no adaptation occurs. The time lapse between the beginning of the stimulus and the beginning of the decrease of the CM amplitude represents the latency of the mid- dle ear muscle reflex. Fig. 3 trace a, depicts the CM with both muscles intact. Trace b shows the CM recorded following tenotomy of the tensor tympani muscle. In both situations the amplitude
of the CM starts to decrease at about t = 15 ms
(onset stimulus at t = 0). However, the amplitude of the CM decreases more with both muscles
intact. Furthermore with the tensor tympani muscle tenotomized the decrease is followed by a
I 0 20 40
mm
Fig. 3. (a) Averaged CM recording of a 107 dE SPL. 1 kHz
stimulus (stimulus duration: 50 ms; r-petition frequency 3.1
Hz; number of stimuli: 50). (b) Tine same form as the previous.
however. tensor tympa?si muscle tenotomized (see text).
----__-.--__-._I’“-.~ , _?I-‘\*,., <“-^u--.H-
\/
,\ d
._-.__~l__-___.___Xr.- _A,_\. _n/--_-,-- __._.__-- e
0 I A’ 15 30 ms
Fig. 4. EMG recordings of the reflex response of the tensor
tympani muscle. (a) Example of a EMG response following a
ipsilateral stimulus of 107 dB SPL, 2 kHz (stimulus duration:
200 ms). (h-e) EMG responses at a shorter time scale at
decreasing stimulus intensity following a tone burst of 2 kHz.
(b) 107 dB SPL. (c) 97 dB 5PL. (d) 87 dB SPL. (e) 77 dB SPL.
Arrow: beginning of the stimulus (see text).
slight increase of the CM amplitude at about t = 25 ms.
In order to estimate the beginning of the musc- ular potentials of the tensor tympani muscle EMG
recordings were made. Fig. 4 shows the recordings of the EMG of the tensor tympani muscle at two
different time scales (traces a and b-d, respec- tively) following ipsilateral stimulation. The muscle
potentials could be induced by both ipsi- and
contralateral auditory stimulation. We recorded these potentials while the measuring electrode was placed on the belly of the tensor tympani. No such potentials could be detected when this electrode
was placed on the promontory. This confirms that these potentials are generated in the tensor tympani muscle and not in the muscles surround- ing the bulla. The rms value of the EMG activity increases with increasing stimulus intensity. Fig.
4b-d shows that the latency of the muscle re- sponses increases only slightly with decreasing stimulus intensity, in contrast to the stronger de-
crease of the latency when estimated from the CM recordings. This is depicted in Fig. 5. which shows the latency of the reflex as a function of stimulus intensity determined by CM recordings (curve a) and the latency of the tensor tympani muscle determined by EMG recordings (curve b). The curves show that the change in CM amplitude-
214
i 1:: *\ g lo- 2
8 *-----------------*_________________ * _J 5-
0’ 80 85 90 95 100 105 110
Stimulus ~Intenslty MBWL)
Fig. 5. Latency of the midole ear muscle reflex. Curve a: mean
latency determined from CM recordings as a function of
stimulus intensity (N = 5). Curve b: mean latency of the EMG
‘response of the tensor tympam muscle (N = 2) (see text).
latency is larger than the EMG-latency at every stimulus intensity. The latency decreases with in- creasing stimulus intensity.
Fig. 6 shows the mean time lapse between the beginning and the end of the decrease of the CM
amplitude (rise time of the middle ear muscle reflex) as a function of stimulus intensity with
both middle ear muscles intact. The rise time varies from 7 to 12 ms and decreases at higher
stimulus intensities. In Figs. 7 and 8 the effect of the contralaterally
induced middle ear muscle reflex on the ipsilateral CM amplitude of tones of various frequencies is shown. Examples of CM recordings with and without contralateral stimulation are shown in
80 85 90 95 100 105 110
Stmhs lntenslty (dBsPL)
Fig. 6. Mean rise time of the middle ear muscle reflex as a
function of stimulus intensity (N = 5) (see text).
Fig. 7. The effect of a contralaterally induced middle ear
muscle reflex on the CM amplitude of an ipsilaterally adminis-
tered stimulus, without and with total muscular relaxation. (a)
CM response of a 67 dB SPL 1.5 kHz tone (averaged response
of 50 tone bursts administered at a repetition rate of 3.1 Hz,
stimulus rise and fall time: 1 ms; single stimulus duration: 15
ms), (b) CM response of the same stimulus like in (a), during
contralateral stimulation with a 97 dB SPL and 1.5 kHz tone.
(c-d) The same stimulus situation as in a-b respectively,
however, during Pavulon@-Vetalar” anesthesia. Note the de-
crease in CM amplitude during contralateral stimulation (b
versus a) This effect disappears during total muscular relaxa-
tion (c-d).
Fig. 7 (traces a and b). These show that con- tralateral stimulation with a stimulus of 97 dB
SPL at 1.5 kHz causes a decrease of the CM amplitude of the ipsilaterally administered stimu- lus (67 dB SPL, 1.5 kHz). The lower two traces (c and d) show the same stimulus situation during total muscle relaxation by means of Pavulon@-
Vetalar @ anesthesia. Contralateral stimulation (trace d) did not affect the CM amplitude any- more. Inspection of the tensor tympani muscle
with the operation microscope did not reveal any sign of contraction in this situation.
In Fig. 8a the mean change in CM amplitude of ipsilateral stimuli of 67 dB SPL at various fre-
quencies (+/ - 1 SD) during 97 dB SPL con- tralateral stimulation (1.5 kHz) is shown ( N = 6). As can be seen in the figure, for most intensities, the maximal change was found at 1 kHz, whereas at lower and higher frequencies the decrease was less. The SD is relatively large. Fig. 8b shows the same curves for the various intensities of the con- tralateral stimulus. At all contralateral intensities 1 kHz is influenced most. This is shown in another way in Fig. 8e: the contralateral stimulus intensity (1.5 kHz) required to induce a fixed decrease in
215
Measulng Frequency (kt-+zJ
65 70 75 80 85 90 95 100 105 110
C Sttmulus lntenslty (dElSPL)
65 ,
I . . ..I
02 1
B Measwng Freauency CkHz)
g -7 -..-..*_. f *;L --‘--------o._.._~~
---______ -..-ir- ..-.. ----O -+ - .__ *
5- ~~~_~...,~_.%_
4
‘---__&, “--::.;_*_
-..:;y_ ---._ * -_p._$
c --.. --_*
a 5 ‘0
--.
65 70 7s 80 85 90 95 loo 105 110
D Stimulus lntenslty (dBSPL)
02 1 IO
E Measuring Frequency (ktiz)
Fig. X. The effect of contralaterally induced contraction of the middle ear muscles on CM amplitudes of ipsiiaterally administered
tones. (a) The effect of contralateral stimulation (97 dB SPL, 1.5 kHz) on the mean CM amplitudes (+ / - 1 SD) of ipsilaterally
administered 67 dB SPL tones with various frequencies, (b) The same form as the previous; with increasing contralateral stimulus
mtensity (77-107 d3 SPL) (O- o: 77 dB SPL: A-A: 87 dB SPL; l - 0: 97 dB SPL; + ~ + : 107 dB SPL). (c),
The same stimulus situationas in (a-b); decrease in CM amplitude of 1 kHz tones plotted as a function of contralateral stimulus
intensity (+ / - 1 SD). (d) The same form as (c), for different frequencies (0.2558 kHz) (+ - +: 0.25 kHz; .- A*: 0.5
kHz; O- l : 1 kHz: A -A: 1.5 kHz; o- o: 2 kHz; 8----- I: 4 kHz; Cl- 0: 8 kHz. (e), iso-decrease in CM
amplitude curves; frequency (ipsilateral) as a function of stimulus intensity (contralateral). o -0: 1.5 dB: CI- D: 2 dB;
0-W 2.5 dB: A- A: 3 dB; .- .: 4.5 dB; n -a: 6 dB. (a-e: N = 6).
1 IO
Sttmulus Frequency (kHz) B Sttmulus Frequency (kt-iz)
0 St8mulus Intensity k33SPi_)
02 1 10
E Stimulus Frequency (kHr)
Fig. 9. The influence of the frequency and the intensity of contrrdateral acoustic stimuli in eliciting the middle ear muscle reflex. (a)
Mean change in CM amplitude (+ / - 1 SD) of a 67 dB SPL 1.5 kHz tone (averaged response of 50 tone bursts administered at a
repetition rate of 3.1 Hz, stimulus rise time: 1 ms; single stimulus duration: 15 ms) as a function of the contralateral stimuhrs
frequency at 97 dB SPL (eliciting a middle ear muscle reflex). (bj The same form as the previous, at 77-107 dB SPL. (O-O:
77-84 dB SPL; A- A: 87-94 dB SPL; +----- l : 97-104 dB SPL: + ~ f: 107-114 dB SPL). (c) The change in CM amphtude plotted as a function of (contralateral) stimulus intensity at 1 kHZ ( +/ - 1 SD). (d) The same form as the previous, at
0.25-8 kHz. ( + - + : 0.25 kHz; .----- A: 0.5 kHz; 0 -0: 1 kHz; A- A: 1.5 kHz; Q- 0:2kHz;W------ m: 4 kHz. (e) Ho-change in CM amplitude curves as a function of the contralateral stimulus frequency, o -0: 3 dB; 0-U: 6
dB. (a-e: N = 6).
217
CM amplitude depends on the (ipsilateral) mea- suring frequency. The decrease is maximal at 1 kHz. In Fig. 8c and 8d the change in CM ampli-
tude of various frequencies is plotted versus the intensity of the contralateral stimulus. For 1 kHz (Fig. 8c), the CM amplitude decreases with in-
creasing stimulus intensity. The mean maximal
decrease in CM amplitude at this frequency is 9-10 dB. Fig. 8d shows the intensity dependence
at other frequencies. At 1.0. 1.5, 2.0 and 4.0 kHz we also measured the effect of the middle ear muscle reflex on the CM amplitude of a 57 dB
SPL (instead of the standard 67 dB SPL) sub- threshold ipsilateral stimulus. The signal to noise
ratio was reduced but the relative changes of the CM amplitude remained the same within 5510%.
Apparently no substantial subthreshold facilita- tion occurs (see Simmons. 1965; Blood and
Greenburg, 1981). Fig. 9 shows the influence of the frequency and
the intensity of the contralateral (middle ear
muscle reflex eliciting) stimulus on the CM ampli- tude of a 67 dB SPL, 1.5 kHz ipsilateral stimulus. Fig. 9a, b illustrate that the frequencies above 2
kHz are the most effective stimulus frequencies in
inducing a middle ear muscle reflex. This trend of lower frequencies being less effective then higher frequencies is found for all stimulus intensities.
Furthermore, the CM amplitude decreases some- what more with increasing stimulus intensity. This
is more clearly shown in Fig. 9c, d, where attenua- tion is plotted against stimulus intensity. The ef- fectiveness of the contralateral stimulus is shown in another way in Fig. 9e. The contralateral stimulus intensity required to induce a fixed de- crease in CM amplitude (1.5 kHz) depends on the
(contralateral) stimulus frequency. 2.5 kHz is the most effective stimulus. A similar curve is ob-
tained when the ipsilateral frequency was changed to 4 kHz (data not shown).
Discussion
The aim of this study was to investigate the latency, the rise time and the effect on sound transmission of the middle ear muscle reflex in the rat.
The latency of the acoustic reflex can be mea- sured by various methods. However, the most
direct methods are EMG and the recording of the CM. From our recordings of the CM it was shown that middle ear muscle reflex latency in the rat is
very short. While it was shown that both muscles
take part in the acoustic reflex in the rat. no differentiation in latency of the two muscles could
be revealed. When the tendon of the tensor
tympani muscle was cut the latency did not change. This would indicate that the latency of the stapedius muscle reflex is at least the same, or
possibly shorter than that of the tensor tympani muscle reflex. In most mammals the latency of the
stapedius muscle is shorter than that of the tensor tympani muscle, while in man only the stapedius
muscle is believed to be active in the acoustic reflex (Borg et al.. 1984). The EMG’s of the tensor
tympani muscle confirm that the reflex latency of the muscle is shorter than the latency of the reflex measured at the level of the cochlea by means of
CM recordings. This difference can be attributed to the time lapse between activation of the muscles
(EMG) and, via the influence on the biomechani- cal system of the ossicular chain, the ultimately
resulting effect on the amplitude of the CM. Com-
pared to most other mammals the latency of the tensor tympani response in the rat measured by
EMG is relatively short (See Wersall. 1958: Fisch and Schulthess. 1963). Only the EMG latency of
tensor tympani responses in the mouse and cat were shown to be as short as about 4 and 7 ms.
respectively (Horner. 1986; Eliasson. 1955). One should be careful when comparing all these results
as the latency depends on various stimulus char- acteristics as rise time, frequency and intensity of
the activating stimulus (Bosatra et al., 1984). Fur- thermore. as was shown in this study, latency
depends on the method of measurement (e.g. EMG. ECoch or impedance). In our opinion, the
latency determined by the diminuation of the am- plitude of the CMs seems to be the most relevant one, as it reflects the influence of the muscles on sound transmission at the level of the cochlea.
The change in CM amplitude in time can be considered as the result of contraction of the middle ear muscles as, firstly. this phenomenon disappeared during total muscular relaxation, and, secondly, it was influenced by tenotomy of the tensor tympani muscle. The time lapse between the beginning and the end of the decrease of the
21x
CM amplitude reflects the rise time of the reflex and can be considered as a measure for the con- traction time of the muscles. The rise time of the
reflex together with its CM-latency determines the clinically important time lapse between the begin- ning of the acoustic stimulus and the effect of
middle ear muscle contraction at the level of the cochlea. As far as we know measurements of the rise time of the muscles by CM recordings have
not been done. Measurements of the contraction
time have been done by stimulating the motor nerves of the muscles (Werdll, 1958; Teig, 1972a).
Teig (1972a) showed that with supramaximal
stimulation of the motor nerves, the contraction time of the muscles in the cat and and rabbit was 20-30 ms. This confirmed findings of Wersgll
(1958) who found a contraction time of the stapedius muscle in the rabbit of about 20 ms. The rise time of about 7-12 ms for both muscles
together in our study is very short and supports the results of morphological studies which showed
that both muscles are composed of mainly fast twitch muscle fibres (Berge and Wirtz, 1989a; Berge and Wirtz, 1989b; Berge and Wal, 1990). In this study no exact differentiation could be made
between the rise time of the tensor tympani and stapedius muscles. However, it was shown that the rise time of the stapedius muscle alone was shorter
than that of the two muscles together. This can be explained by either a shorter latency of the
stapedius muscle or a longer rise time of the tensor tympani muscle. The relatively short rise time of the reflex with both muscles intact to- gether with the relatively short latency of the
reflex indicate that the acoustic reflex in the rat has a very fast reaction pattern. This fast reaction pattern is an important characteristic in the light of prevention of noise damage to the inner ear.
With regard to the quantitative effect of the middle ear muscle reflex on sound transmission it became clear that the mean decrease of CM am- plitude in the rat is limited to a maximum of about 10 dB at I kHz. From the slope of the CM amplitude versus stimulus intensity curve at 1 kHz (Fig. 2b), it can be calculated that this corre- sponds with an attenuation of sound transmission of about 15 dB SPL. This is less in comparison with findings in, for example, the cat, the guinea pig and the rabbit (Wiggers, 1937; Wever and
Bray, 1937. 1942; Wever and Vernon. 1955; Teig. 1972a; Teig, 1973) and in man (Borg, 1968; Borg and Zakrisson, 1974). However several aspects have to be taken into account.
Firstly, in this study measurements were per- formed leaving both middle ear musles and their innervation intact, while in a number of other
studies attenuation was measured after tenotomy or attenuation was calculated from indirect meth- ods like monaural masking in patients with stape-
dial paralysis (Borg and Zakrisson, 1974) and con-
traction force studies (Wever and Bray, 1942; Teig,
1972a). Under the experimental conditions of this
study, when the middle ear muscles are activated, attenuation occurs, resulting in a diminished sound level. As a result the contraction of the muscles
might be adjusted to this lower level (as was shown in Fig. 3 curve b), ultimately resulting in a
steady state. Secondly, measurements were performed only
up to 107 dB SPL for most frequencies. This was done because measurements took many hours and had appeared to result in inner ear damage at these high sound levels in pilot studies. Finaily.
our data were derived from contralateral activa- tion of the middle ear muscle reflex. Activation of the reflex might occur at lower intensities and can
result in higher attenuation when stimulated ipsi- laterally or bilaterally (Guinan and McCue, 1987).
As regards the stimulus intensity-attenuation curves it was shown that the largest effect oc-
curred between 65-77 dB SPL. Further increase of the stimulus intensity did not result in a accord-
ingly larger increase of attenuation. This could possibly be explained by the findings of Teig (1973) who showed in the cat that stronger con-
tractions gave less reduction of sound transmis- sion per gram tension.
The finding that tones of 1 kHz are attenuated most is difficult to explain. In most animals at- tenuation is maximal at lower frequencies (i.e. less than 1000 Hz) and decreases towards higher fre- quencies. However, it seems likely that the acous- tic reflex is adapted to the special needs for a certain species, as was shown, for example, in the bat (Pollak and Henson, 1973). Supposedly, in the rat, 1 kHz is a frequency that needs to be at- tenuated, possibly to avoid masking of higher tones during vocalisation. In addition it appeared
219
that the higher tones were the most effective eiici- tor of the middle ear muscle reflex. This might
indicate the importance of high tones for the rat.
Sensitivy studies of the CM in the rat have shown peak sensitivity at 3 kHz and 40 kHz (Crowley
and Hepp-Reymond, 1966). However, in the Lewis rat we found peak sensitivity at 1.5 kHz (Fig. 2~).
This seems to be paradoxal since attenuation is most at 1.0-1.5 kHz. In summary. the acoustic
reflex in the rat has been shown to be fast reactive both in latency and rise time. The attenuation of 0.25-8 kHz upto stimulus intensities of 115 dB SPL is (while both middle ear muscles and their
innervation are intact) limited to a mean maxi- mum of 15 dB SPL. The tones above 2 kHz
appear to be the best elicitor of the middle ear muscle reflex. However, relevant inter-indivudual
differences appear to exist. One kHz appears to be attenuated the most in the rat, the reason of which remains obscure. In addition to this phenomenon,
interesting aspects for further research into the function of the middle ear muscles would be;
measurements during ipsilateral activation of the muscles, the fatiguability of the reflex, as well as
the activity of the muscles following noise ex-
posure.
Aknowledgements
We thank V. Bongers and C. ter Riet for their contributions to the experiments and J. Huntjens for the technical assistance. This study was sup- ported by the Heinsius-Houbolt foundation.
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