Download Effects of sympathetic stimulation on the round window compound

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127
Krsrtrrc~h. I9 ( 19X5) 127 - 134
F.lsevier
HRR
00630
Effects of sympathetic
stimulation on the round window compound
potential in the rat
action
Albert H. Lee and Aage R. Mdller
Depttrtntent
of Nrurologtd
Surge<v, Unrrwsr!,~ CIJPlttshurgh
(Received 29 November
The effect on the ear of stimulating
potentials (N,N?)
the sympathetic
School of ,Mrd~crw
nervous system was studied
than at moderate
stimulation
animals varied in their responses to stimulation
ms at approximately
as a result of sympathetic
stimulation
(0.07
systematrcally
related
before sympathetic
autonomic
to sympathetrc
stimulation.
After
the adminstration
in three rats there was no effect on the latency of the N,
Individual
Further.
of
hexamethonium
potential
and although
the change in the amplitude
(which
from sympathetic
block.\
not studled
of N, was not
transmiswn
stimulation
In
as recorded
stimulation.
nervous system. auditory
nerve. compound
action potential
Introduction
The hypothesis
that sympathetic
activity can
influence
sensory
receptors
is not new. Sympathetic stimulation
has been shown to enhance
the response of muscle spindles [5,8]. taste receptors, and touch and pressure receptors [2]. and
Nilsson [ 151 showed that sympathetic
stimulation
of the mechanoreceptors
of cat vibrissae can lead
to an increase in the latency of dynamic responses.
In addition.
the cochlea has been shown to be
innervated
sympathetically
[3,19.20,24]. with two
different groups of adrenergic fibers having been
identified:
perivascular.
around the labyrinthine
artery and its branches [22], and vessel-independent fibers in the lamina spiralis ossea where a
plexus is formed in the area of the habenula
perforata at the point where the afferent auditory
nerve fibers become myelinated [3,4,19].
The results of studies designed to examine these
037%5955/X5/$03.30
In addition.
of the response. In one of the twelve animals there was a
low frequencies seemed to be affected more than high frequencies.
ganglia)
dB above threshold).
ms (LE.)
with little change in
some animals evidencing a great change I” the
ms at 5 dB ahove threshold).
systematically.
autonomic
of the
and others showing very little change in latency. This variabilit>
could not be related to the condition of the animal at the time of observation
in latency
25-30
action
of the superior cervical ganglion \~a\
ms at 15 dB above threshold).
of the superior cervical ganghon. wth
latency of the response (0.4 ms increase at 10 dB above threshold)
the compound
at low stimulus intensities (mean value 0.09+0.04
intensities (0.08*0.04
latency occurring at the highest intensity tested (0.02+0.01
alight decrease
in rats by recording
rats before. during. and after electrical strmulatlon
the changes in N, latency which resulted. Stimulation
found to cause an increase in the N, latency which was more pronounced
at 5 dB above threshold)
P.4 /52/_~. C X.4
19X4; accepted 26 June 1985)
in response to 2 kHz tonebursts presented to anesthetized
superior cervical ganglion. and evaluating
Pttt.~htrrgh.
’
neural interactions
in the ear prompted researchera
to investigate the role of the sympathetic
nervous
system in controlling
ear function, and to perform
experiments in which the sympathetic ganglia were
stimulated
electrically
and in which the superior
cervical ganglion
and the stellate ganglion
were
transected
so that autonomic
control of auditory
function could be studied. Seymour and Tappin
[18] found that the amplitude
of cochlear microphonics (CM) decreased by 3OG50% during electrical stimulation
of the cervical sympathetic
trunk.
but Krejci and Bornschein [9] found that stimulation of the cervical sympathetic
trunk had no
effect on the CM, and Baust et al. [l] found that
sympathetic
stimulation
had no effect on either
the CM or the compound
action potential (CAP)
in curarized cats. However, while Pickles [16] reported that sympathetic
stimulation
had no effect
on CM. he did find that it caused a 16% increase
in the amplitude
of the N, peak of the CAP
19X5 Elsevier Science Publishers 1S.V. (Biomedical
Di\i\ion)
evoked by clicks. Along the same lines, Hultcrantz
et al. [7] found that cervical sympathectomy
resulted in a 30% decrease in the amplitude
of the
CAP.
Other investigators
have studied the effects on
cochlear blood flow of stimulating
the cervical
sympathetic
trunk electrically.
Rambo et al. [17]
found that sympathetic
denervation
did not affect
labyrinthine
vessels, and Todd et al. [23] found
that sympathetic
stimulation
had no significant
effect on cochlear blood flow. Further. Hultcrantz
et al. [6] found
that sympathetic
stimulation
changed cochlear blood flow only at low blood
pressures. Thus, despite the fact that much of our
knowledge of the effects of sympathetic
stimulation on cochlear electrophysiology
is fragmentary
and often contradictory,
the fact that cochlear
blood flow does not change as a result of sympathetic
stimulation
seems to suggest that the
mechanism
for autonomic
modulation
of cochlear
potentials is neural.
For this reason, the present study was conducted to measure the shifts in latency and amplitude of the N, peak of the CAP that result from
electrical stimulation
of the superior cervical ganglion.
Materials and Methods
Each of 12 female Sprague Dawley rats, weighing 250-350
g apiece, was anesthetized
with
urethane
(1.5 g/kg body weight, i.p.), which is
known not to interfere with ganglionic
transmission [ll]. The animal was maintained
at a constant
rectal temperature
of 37°C and a tracheotomy
was
performed
in order to facilitate ventilation.
The
bulla was exposed
using a ventral
approach,
opened, and a silver wire electrode was placed on
or near the round window. A gold cup electrode
was placed on exposed neck muscles, serving as a
reference. After the round window electrode had
been sutured securely in place, the hole in the
bulla was closed with petroleum jelly. Next, the
superior cervical ganglion was approached
through
an incision caudal to the pinna. Muscle was dissected bluntly until the internal carotid artery and
vagus nerve could be identified
in the carotid
sheath, and the sympathetic trunk and the superior
cervical ganglion
were sought near the carotid
sheath. The ganglion was identified positively by
observation
of dilatation of the ipsilateral pupil in
response to electrical stimulation
of the nerve tihsue. Stimulation
was applied using bipolar xilver
wire electrodes placed on the ganglion or on the
sympathetic
trunk adjacent to the ganglion. and
rarely (1 in 13 animals) was the response accompanied by protrusion
of the entire eye. A Grass SD9
stimulator
was used to deliver 3.5 V (constant
voltage) rectangular
pulses with zero net charge.
20/s and 1 ms in duration, to the ganglion. These
stimulus parameters
were chosen to give a consistent widening of the pupil but a minimum
of
changes in respiration and heart rate. The stimulation was applied for an average of 30 min.
Sound was delivered through the hollow earbars
of a headholder using a condenser earphone (Briiel
and Kjaer, Type 4131) [12], and consisted of 2
kHz tonebursts,
3 ms in duration, with a rise time
of 0.5 ms to 90% of maximal amplitude and a fall
time of 0.5 ms to 10% of the maximal amplitude.
The tonebursts were presented with an interstimulus interval of 100 ms. The potentials were amplified and filtered (30 Hz highpass and 3000 Hz
lowpass) using a Grass P5 amplifier. 2000 responses
were averaged on a PDP 1 l/73
minicomputer
using artifact rejection based upon the amplitude
of the response. The rejection level was set to
reject all responses
that included
an electrical
stimulus.
The recorded potentials
were sampled
every 20 ~LSand the resultant averaged potentials
were digitally filtered off-line using a zero-phase
shift filter [14] which suppresses
low-frequency
components
without
causing
any shift in the
latency of the peaks. The latencies were determined
using a program that automatically
identified the
peaks and printed the latency values.
Responses to 2 kHz tonebursts
were recorded
using tones of different
intensities
during sympathetic stimulation
beginning
with high intensities. Control experiments in which the tones of low
sound intensities
were presented
first showed no
discernible
difference
in the results. A similar
scheme of sound stimulation
was used for a period
of 30 min after the termination
of the sympathetic
stimulation.
In addition, short epochs of 50 auditory responses each were recorded immediately
before and immediately
after the onset of the
stimulation
and averaged in order to estimate the
IZY
2.9
time of onset of any effect. Finally, the responses
of some animals to 20 kHz tones were recorded
before and after sympathetic stimulation,
and three
rats in the study were given hexamethonium
bromide
(Sigma
Chemical
Co.), a ganglionic
blocker, before electrical stimulation
of the supe-
C
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>
0
1.9
2.0
i
6
z
-I
?
1.1’
40
1.6
D
50
dB SPL
70
60
l
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1.6
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40
50
60
70
8
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z 2.1
dB SPL
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B
2.7
O-._
5
5
5 1.9
0\
1.7
1.1
40
50
-60~
-70
dB SPL
Fig. 1. Latency of the N, response as a function of stimulus
durintensity (in dB relative to threshold) before (0 -0).
X ) electrical stimulation
mg (O---O)
and after (Xof the superior cervical ganglion.
The stimuli were 2 kH[
tonebursts and the results are from 4 different animals.
1.9
--
1.1
40
50
dB SPL
60
70
rior cervical ganglion,
which presumably
makes
the ganglion less sensitive to electrical stimulation.
The drug was given in a dose of 10 mg/kg body
weight via a femoral vein catheter.
In addition, several pilot experiments
were conducted in order to provide adequate control information. Four animals were tested with the same
protocol after the administration
of tubocurarine
were mechanically
venti(0.2 ml, i.m.; animals
lated) in order to assure that middle ear muscle
contraction
played no part. Two animals
were
tested after sectioning
of the sympathetic
chain,
approximately
at the level of the superior cervical
ganglion, in order to assure that vascular changes
induced by the electrical stimulation
played no
part in any observed effects.
tive latency--il~tensity
curves from 4 rats are reproduced. In 1 of these 4 animals sympathetic
stimulation produced
a substantial
increase
in the
latency of the N, peak of the CAP evoked by 2
kHz tones (A), in 2 animals a moderate change
was evoked (B and C), and in 1 rat there was very
little change in response to sympathetic
stimulation (Df. However, it is evident from Fig. I that in
all cases in which latency increased the increase
was greatest at low stimulus intensities. In addition,
the latency values approach
pre-stimulus
values
when recorded at least l-2 h after the end of the
stimulation.
Table I gives the data for the average change in
latency with sympathetic
stimulation
at different
stimulus intensities. At stimulus Levels of 5- 10 dB
above threshold the latency of the N, response
increased by approximately
0.1 ms, which corresponds to the latency change which occurs with
approximately
a 5 dB change in sound intensity.
Little or no increase in latency was observed at
high intensities
(approximately
25-30 dB above
Results
In 9 of the 12 rats the latency of the N, potential increased
in response to stimulation
of the
superior
cervical ganglion,
while in 2 rats the
latency of N, remained the same, and in 1 rat the
latency decreased with stimulation. There was great
individual variation in the magnitude of the change
in N, latency, as shown in Fig. 1 where representa-
FILTERED
UNFILT.
1
0
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1
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I
1
2
3
4
5
6
0
1
2
3
4
5
6
TIME IN t.&LLlSECONDS
TIME IN MILLISECONDS
Fig. 2. Examples of actual recordings before (A), during (6) and after (C) stimulation of the superior cervical ganglion. The stimuli
were 2 kHz tonebursts, presented at an intensity of 10 dB above threshold. The latency measurements were based upon the filtered
recordings shown to the right.
131
TABLE
2.1
I
1 A
DIFFERENCE
IN N, LATENCY
AS A RESULT
OF
STIMULATION
OF THE SUPERIOR
CERVICAL
GANGLION IN THE RAT
+ 5 dB above threshold
+ 10 dB above threshold
+ 15 dB above threshold
Highest Intensity tested
u + SE. (ms)
n
0.09
0.11
0.08
0.02
12
I2
12
12
f
i
*
*
0.04
0.042
0.04
0.01
threshold) so that the latency-intensity
curves are
steeper during sympathetic
activation.
The difference between the results obtained
at +5 dB
above threshold as well as the difference between
the results obtained at the highest intensity tested
were significant (P < 0.05 using Student’s t-test).
The second peak in the auditory
potentials
recorded
from the round window in the rat is
often the largest of the two peaks, and the general
morphology
of the response
seemed
to be
unchanged
by sympathetic
stimulation;
both of
the negative peaks of the CAP were clearly present
throughout
the experiment.
Fig. 2 shows examples
of actual responses
that were recorded
before,
during, and after sympathetic stimulation.
From evaluation of several recordings of a small
number of sweeps it was apparent
that the N,
latency began to lengthen from 1 to 5 min after
sympathetic
stimulation
was begun, and returned
to baseline values fairly slowly, sometimes over a
period of 30 min to 1 h after the stimulation
was
discontinued.
This indicates that the mechanism
by which sympathetic activation affects the ear is a
slow process, which may explain why N, latencies
[POKHZ]
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30
40
50
60
70
dB SPL
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1.9
I20KHz
8
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z 1.7.
4
p
4
]
1.5
1.3
I
/
l.lL
30
40
50
60
70
d0 SPL
TABLE
II
DIFFERENCE
IN N, AMPLITUDE
STIMULATION
OF THE SUPERIOR
GLION IN THE RAT (in ?? of initial)
+ 5 dB above threshold
+ IO dB above threshold
+ 15 dB above threshold
Highest Intensity tested
AS A RESULT
OF
CERVICAL
GAN-
u + SE.(%)
II
105.7*13.7
9n.4+ 14.3
98.4+ 10.9
96.8 f 7.7
11
12
12
12
Fig. 3. Responses
of 2 rats to electrical stimulation
of the
superior cervical ganglion. Latency was measured as a function
of stimulus intensity before (Ol), during (O------O)
X) stimulation
with 20 kHz tonehurst\.
and after ( x ~
The responses in A are from the same rat as that shown in Fig.
1A.
failed to return completely
to baseline in some
cases, although they did return to near baseline in
most experiments.
This variability
in results from
individual
animals could not be correlated
with
the condition
of the animal.
although
the dif-
l.l’_
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60
70
dB SPL
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X ‘\ ‘\
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x
%
;
/
1.1’
40
50
60
70
dB SPL
Fig. 4. (A) Graph similar to that in Fig. 1, showing the effect of
hexamethonium
on the effect of electrical
stimulation
superior cervical ganglion on the latency of the N,
O---O,
results obtained
before stimulation
cervical ganglion and before administration
O----O.
results obtained
during
stimulation
of the superior
of hexamethonium.
x .results obtained after sympathetic stimulation. (B)
The effect of administering
and
of the superior
of hexamethonium.
cervical ganglion and after administration
x ~
of the
response.
of
administering
hexamethonium
hexamethonium
ference in latency before and after sympathetic
stimulation
may have been smaller if a longer time
had been allowed between the end of sympathetic
stin~uiation and recording.
caused
by symChanges
in N, amplitude
pathetic stimulation
were much less consistent than
were changes in N, latency. In 2 rats N, amplitude
increased upon stimulation,
in 4 rats the amplitude
remained the same, and in 6 rats the N, amplitude
decreased with sympathetic stimulation.
There was
also considerable
variability
in the magnitude
of
the amplitude changes. Overall. however. as Table
II illustrates,
sympathetic
stimulation
caused no
significant
changes in N, amplitude at any 2 kHz
toneburst
intensity
used. The difference between
the result obtained at + 5 dB above threshold and
that obtained at the highest intensity tested is not
significant (P > 0.05
using Student’s t-test).
The dependence
of the effect of sympathetic
stimulation
on the frequency of the stimulus was
not studied systematically
in this series of experiments. However, the results of previous experiments show that the greatest effect is obtained
when relatively low-frequency
stimuli are used. In
this series of experiments
the effect of sympathetic
stimuli on the response to 2 kHz tones was compared to the response to 20 kHz tonebursts in two
rats (Fig. 3). The N, latency. upon sympathetic
stimulation,
was either smaller than the increase
found with 2 kHz tonebursts
(Fig. 3A) or it was
not increased at all (Fig. 3B).
Hexamethonium,
which blocks transmission
in
sympathetic
ganglia, was administered
to 3 rats in
order to confirm that the changes introduced
by
the stimulation
were
indeed
autonomically
induced. Fig. 4 shows the results of administering
the drug in 2 of these rats: application
of sympathetic
stimulation
resulted
in no significant
change in either N, latency or amplitude,
but
administration
of hexamethonium
increased
the
baseline N, latencies. This may be a result of
reducing the sympathetic
resting activity or it may
be a result of altering respiration or blood pressure
[IO]. In Fig. 4B, in which the responses obtained
immediately
after the administration
of hexa-
atone (O----O)
in conjunction
with
stimulation
O--O.
ill~th~~niunl.
of the superior
results
obtained
cervical
ganglion
before
(x -
administering
x ).
hexa-
methonium
and after stimulation
of the superior
cervical ganglion alone are shown separately, it is
evident that stimulation
of the superior cervical
ganglion does not increase the N, latency when the
ganglion is blocked.
In animals that were paralyzed with curare, in
order to exclude middle ear muscle activation, the
N, latency to 2 kHz tonebursts
was unchanged
upon sympathetic
stimulation.
In the animals that
had sectioning of the sympathetic
chain, the sectioning itself seemed to have little effect on the
latency of the N,. However. stimulation
of the
proximal cut portion of the chain showed an increase in N, latency of approximately
0.1-0.2 ms
upon stimulation.
Discussion
The results of these experiments
show that
stimulation
of the superior cervical ganglion delays
the N, response to 2 kHz tonebursts.
However,
although the change in latency is always largest at
low stimulus intensities,
there is substantial
individual variation in the magnitude of the shift. The
effect of sympathetic
stimulation
on the latency of
N, is abolished
by the administration
of hexamethonium.
Several control experiments
were performed to
ensure that the latency change was due to autonomic activation
and not to other factors. For
example,
in order to exclude activation
of the
middle ear muscles as a possible explanation,
some
animals were paralyzed with curare. Because curare
blocks transmission
through the autonomic ganglia.
the latency of N, during sympathetic
stimulation
was unaffected.
However, the effect of contractions of the middle ear on N, latency should take
the form of a parallel shift in the stimulus latency
curve (because
contraction
of the middle
ear
muscles causes a change in the way sound is
conducted to the cochlea and thus is effectively the
same as changing the sound intensity);
this effect
was then sought. What was observed as the result
of sympathetic stimulation
was a change in latency
of N, equivalent
to a decrease in sensitivity
of
approximately
5 dB near threshold, approximately
4 dB at 15 dB above threshold, and 0 dB at the
highest intensity tested (approximately
25-30 dB
above threshold).
Thus. no parallel shift in the
stimulus latency curve occurred. and therefore, it
is unlikely that the results are due to contraction
of the middle ear muscles. Further. the fact that
the effects of electrical stimulation
appear only
after a period of minutes makes it highly unlikely
that these results could be due to contraction
of
the middle ear muscles.
Another possibility
is that the effect observed
was mediated
through activation
of the olivocochlear bundle. However. this is also unlikely.
and the fact that an autonomic
ganglion blocker
(hexamethonium)
abolishes the effect of electrical
stimulation
supports the assumption
that the results of such stimulation
are indeed mediated by
the sympathetic
nervous
system. However, how
sympathetic
activation
affects the ear is unclear.
Since results of studying inner ear circulation make
it unlikely that the effect is vascular [21]. it may
seem more likely that the effect is exerted directly
upon the auditory nerve fibers where they leave
the hair cells. It has been shown that there is an
abundant
autonomic innervation
in the area where
the afferent
auditory
nerve
fibers
become
myelinated
[19]. The effect of hexamethonium
itself is an increase in the latency, which is in
agreement with results by Hultcrantz
et al. [7]. II
hexamethonium
decreased the tonic resting activity of the sympathetic
system, one would expect
that an increased activity (as, e.g., through electrical stimulation
of the sympathetic
ganglia) would
have the opposite effect. However, we found in
this study that electrical stimulation
increased the
latency.
When the stimulus intensity is changed or the
sensitivity of the ear varies. the amplitude
of the
N, response and its latency are expected to vary.
Thus, if stimulation
of the sympathetic
nervous
system leads to a decrease in sensitivity. we would
expect to see a decrease in amplitude
of the N,
response compatible
with the observed increase in
latency. In fact, although the amplitude of the N,
peaks is more affected by such factors as changes
in shunting
of the recording electrode than are
changes in latency, the results of this study seem to
show that indeed the amplitude of the N, changes
very little as a result of sympathetic
activation.
The change in amplitude
that corresponds
to a
decrease in latency of 0.1 ms is about 15%. enough
to be detected readily, and no such change wa\
observed. Thus this change in latency is probably
not caused by a simple decrease in sensitivity.
In order to explain the observed results, then, it
is necessary to focus upon the results of a change
in conduction
time. A shift in the location of the
envelope of the traveling wave on the basilar membrane towards the apex will cause an increase in
latency because of added travel time. but will
cause little change in amplitude.
Such a change in
the location of the envelope has been inferred to
occur when the stimulus
intensity
is increased.
although in the opposite direction [13,14]. It was
seen to occur in conjunction
with widening
of
basilar membrane tuning and is assumed to be the
result of a change in the stiffness of the hairs on
the hair cells.
How stimulation
of the autonomic nervous system affects the auditory system depends not only
upon the level of stimulation
but also upon the
level of activity of the sympathetic
nervous system
which explains
how even
prior to stimulation,
animals of inbred strains may vary in their responses to such electrical stimulation.
However,
although the results of the present study show that
stimulation
of the sympathetic
nervous
system
clearly affects the ear, how the autonomic nervous
system exerts control over the ear under physiological conditions
remains unclear. For this reason, further investigation
of the effects of such
stimulation
is warranted.
Acknowledgements
This work was supported
by a grant from the
National
Institutes
of Health
(No.
1 ROl
NS21378-01). The authors thank Cleat Szczepaniak
for her assistance in preparing this article.
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