Download Effect of high-frequency hearing loss on compound action potentials

Hearing Research, 55 (1991) 9-23
0 1991 Elsevier Science Publishers
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01596
Effect of high-frequency hearing loss on compound action potentials
recorded from the intracranial portion of the human eighth nerve
Aage R. Mgller and Hae Dong Jho
Department of Neurological Surgery, University of Pittsburgh School of Medicine, Pittsburgh, Pennsylvania, U.S.A
(Received
12 September
1990; accepted
30 January
1991)
Compound
action potentials (CAP) were recorded from the exposed intracranial
portion of the eighth nerve to stimulation
with click sounds
in patients with sensorineural
high-frequency
hearing loss who underwent
microvascular
decompression
(MVD) operations
to treat trigeminal
neuralgia (TN). In patients with normal hearing the CAP recorded in that way is characterized
by a negative peak, preceded by a small positivity
and followed by a positivity and sometimes
a second negative peak. In patients with high-frequency
hearing loss the CAP also usually had an
initial sharp negative peak in response to clicks of high intensity (105 to 110 dB Pe SPL), similar to findings in patients with normal hearing, but
in patients with high-frequency
hearing loss the initial negative peak was often followed by a slow negative deflection. The latency of the initial
negative peak in the CAP in patients with high-frequency
hearing loss was longer than the latency of this peak in patients with normal hearing,
but the difference
in latencies of this peak to condensation
and rarefaction
clicks was small. When the stimulus intensity was lowered the
amplitude of the initial peak decreased,
and the CAP became dominated
by a broad negative peak with a latency of 6 to 8 ms.
In 11 of 15 patients with severe high-frequency
hearing loss, a series of quasiperiodic
waves was superimposed
on the CAP. The frequency of
these waves varied between 500 and 1200 Hz, and the waves could be detected between 6 and 16 ms after presentation
of the click stimulus.
These waves were usually present in the response to stimuli in the intensity range from 75 to 110 dB Pe SPL. Only 4 of 17 patients with normal
hearing had similar waves.
Human
auditory
nerve; Compound
action
potentials;
Intraoperative
Introduction
Studies of the neural generators of the brainstem
auditory evoked potentials (BAEP) have shown that it
is difficult to draw conclusions about the human auditory system from the results of studies in animals.
Thus, although the results of animal studies have advanced our understanding of the anatomy and physiology of the auditory system in general, the performance
of studies in man has been crucial for the identification
of the neural generators of the BAEP in man. This is
also true for studies of the pathophysiology of the
human auditory system. Studies of the neural generators of the BAEP, on the basis of intracranially
recorded evoked potentials, have also mostly been performed in patients with normal hearing (Moller et al.,
1981a,b; Hashimoto et al., 1981).
In previous studies (Moller and Jho, 1988, 1989a,b,
19911, we showed how the compound action potential
(CAP) that can be recorded from the exposed intracranial portion of the eighth nerve in patients with normal
hearing varies as a function of stimulus intensity and
Correspondence to: Aage R. Moller,
Surgery, 9402 Presbyterian-University
Pittsburgh,
PA 15213, U.S.A.
Department
of Neurological
Hospital, 230 Lothrop Street,
recordings;
Active cochlear
processes
click polarity. These studies were performed in patients who underwent operation for vascular compression of the fifth and seventh cranial nerves by the
microvascular decompression (MVD) technique (Jannetta 1977, 1981a,b). We have also shown that in some
patients a series of more or less periodic waves appears
superimposed on the recorded potentials (Moller and
Jho, 1990).
Because patients who undergo operation for microvascular decompression of cranial nerves may have
normal hearing or various forms of hearing loss, related or unrelated to the disorder for which they are
undergoing operation, recording CAP directly from the
exposed intracranial portion of the eighth nerve during
such operations provides an opportunity to study these
potentials in patients with various types of hearing loss
as well as in patients with normal hearing.
We showed earlier (Moller et al., 1991) that the
CAP recorded in response to broadband clicks from
patients with various degrees of hearing loss have a
multitude of different shapes. In the present paper we
present the results of recording CAP from the exposed
intracranial portion of the eighth nerve in patients with
high-frequency hearing loss, while the patients underwent MVD operations of the fifth cranial nerve to
treat trigeminal neuralgia (TN). We show how the CAP
recorded from the exposed eighth nerve changes as a
function of the stimulus intensity, and we analyze the
waves that are superimposed on the late slow components of the CAP in some of these patients.
Methods
The results reported in the present paper are based
on recordings obtained intraoperatively in patients undergoing microvascular decompression (MVD) of the
fifth cranial nerve to treat trigeminal neuralgia (TN).
In all patients a complete audiological and otological
evaluation was performed before the operation. Testing included pure tone audiometry, speech audiometry
using recorded lists (NW61, tympanometry, and recording of the acoustic middle ear reflexes. The audiological tests were performed in a sound-insulated booth by
a certified audiologist using modern, calibrated equipment (Msller and Moller, 1989): Patients whose pure
tone thresholds were elevated by 20 dB or more at
more than 2 frequencies of presumed cochlear origin
were included in the present study, but those with a
conductive hearing loss or a hearing loss that was
presumed to be a result of an auditory nerve lesion
were excluded. Thus, only patients who had nearly the
same hearing loss on both sides and who had speech
discrimination scores and acoustic middle ear reflex
thresholds within the range expected with regard to
their pure tone audiograms were included in the study
(although one patient had not mastered the English
language sufficiently to permit speech discrimination
testing to be performed). These selection criteria were
chosen to exclude patients who might have had a lesion
on the auditory nerve.
Earlier reports describe the operative techniques
used (Jannetta, 1977, 1981a,b) and the technique that
was used to record brainstem auditory evoked potentials (BAEP) and compound action potentials (CAP)
from the exposed eighth cranial nerve (Moller and
k
Jannetta, 1983; Moller, 1988a; Msller and Jho, 1988,
1989a,b), and therefore only a brief description of
these methods will be given here.
BAEP were recorded intraoperatively from the time
that the patient was anesthetized to the time that the
wound was closed. Click sounds were generated by
applying 100~PS duration rectangular waves (delivered
by a Grass Instrument Co., audio-stimulator, Type SlO
CTCMA) to miniature stereo earphones (Radio Shack,
Realistic) that were fitted into the patient’s outer ear
and kept in place with adhesive tape. The ambient
noise level in the operating room is a limiting factor as
to how low sound levels can be studied. In order to
obtain the best possible sound insulation in the ear
that was tested, the earphone was placed so that it fit
tightly over the entrance to the patient’s ear canal, and
it was sealed in the outer ear in an water-tight fashion,
with several layers of adhesive plastic tape being applied so that tape covered the entire outer ear.
All the sounds were presented at a rate of 19 pps.
The earphones were calibrated by attaching them to a
2.5-cc slightly damped cavity to which a l/4-inch condenser microphone (Bruel and Kjaer, Type 4135) was
attached. The sound pressure of the click sounds was
also measured at the entrance of the ear canal using
the same l/4-inch condenser microphone. The click
sounds presented in that way produced a waveform
characteristic of a slight ringing (Fig. 1A) and had a
spectrum that included a broad peak around 600 Hz
and a smaller peak around 5 kHz (Moller and Jho,
1991). The spectrum of the lOO-l.~srectangular pulse
used to drive the earphone has a ‘null’ at 10 kHz,
which also is reflected in the spectrum of the sound
(Fig. 1B). The clicks of opposite polarity had identical
waveforms (except that the waveforms were also inverted) and their spectra were not noticeably different.
The mean threshold of click sounds presented at a
rate of 19 pps was determined in 4 persons with normal
hearing (threshold equal to or better than 10 dB be-
!I
Fig. l.(A) Waveform of the click sound recorded at the entrance of the ear canal. A l/&inch
condenser
microphone
(Bruel and Kjaer. Type
4135) had been placed in the recess between the tragus and the antitragus,
and the earphone
had been positioned for intraoperative
recording.
Solid lines, condensation
click. Dashed lines, rarefaction
click. Peak equivalent sound pressure level (Pe SPL) was 105 dB. (B) Spectrum of the
sound (condensation
click), the waveform of which is shown in A.
11
tween 250 and 4000 Hz and 20 dB or better between 6
and 8 kHz) with the earphone placed in the same way
as in the operating room. This threshold was 39.5 f 1.9
dB Pe SPL (range, 36 to 41 dB).
The CAP from the exposed eighth nerve were
recorded using a monopolar electrode made from a
multistrand
Teflon-insulated
silver wire (Medwire
Corp., Type Ag 7/40) to the uninsulated tip of which a
small cotton wick was sutured (Mgller and Jannetta,
1983; Moller, 1988a). The cotton wick was placed on
the exposed eighth nerve, and the reference electrode
for the recording of CAP from NV111 was placed on
the opposite earlobe. The potentials were amplified
(Grass Instrument Co., ac amplifiers, Type 12) at a
gain of 20,000 x . Filter settings were 3 Hz highpass (6
dB point with 6 dB/octave rolloff) and 3000 Hz lowpass (6 dB point with 24 dB/octave
rolloff). The
recorded potentials were averaged using an LSI 11/73
microprocessor or an Apollo DM 3000 computer with a
sampling interval of 40 or 80 &S and 256 or 512
datapoints in each record. In the operating room a
baseline record was displayed together with a display
of the actual record for easy detection of changes in
the recorded potentials. BAEP were always recorded
simultaneously with CAP recorded from the eighth
nerve, and the averaged responses were stored together on computer disks for further processing.
The differences between responses recorded to condensation and rarefaction clicks were obtained, and
these differences were highpass filtered, to eliminate
low-frequency components, with a zero-phase digital
highpass filter. The power spectra of these difference
records were obtained by computing (fast) Fourier
transforms (using a Hanning window) of autocorrelograms of the highpass filtered difference records (see
Blackman and Tukey, 1959).
The results presented in this paper were obtained
during intraoperative monitoring of evoked potentials
that is performed routinely in patients undergoing
MVD operations at our institution. The procedure was
approved by the Biomedical Institutional Review Board
of the University of Pittsburgh School of Medicine, and
the patients gave their informed consent to participation in monitoring and use of the results for scientific
purposes.
Results
In patients with moderate degrees of high-frequency
hearing loss (Fig. 2A), the shape of the CAP (Fig. 3) is
rather similar to what is seen in patients with normal
hearing (Fig. 4), namely a large and sharp negative
peak, preceded by a small positivity. The large negative
peak is followed by a small negative peak. When the
stimulus intensity is decreased the latency of the initial
Fig. 2. Audiograms (A through E) of the 5 patients studied. Speech
discrimination score is given in insert (the patient without a speech
discrimination score had not mastered the English language sufficiently for this testing to be performed).
Lower data points are
acoustic
middle ear reflex thresholds.
110
105
creased, but its latency remained
almost independent
of the stimulus intensity. When stimulus intensity was
less than 90 dB there was no discernible
initial peak,
and the responses consisted of a single broad, negative
peak. The response
to llO-dB clicks also showed a
broad negative deflection
that directly followed the
initial negative peak and lasted for about 10 ms. When
the stimulus intensity was decreased
this negative deflection shifted towards longer latencies,
and it appeared as a separate peak at stimulus intensities of 100
dB and below. There were periodic waves superimposed on this broad peak, and the phase of these waves
reversed exactly when the polarity of the clicks was
reversed.
Such waves were not seen in the patient
whose results are shown in Fig. 3.
d0
dB
110
dB
‘,, ,
65
75
dB
105
d6
100
dE
dB
I
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I
1
I
I
I
0
2
4
6
6
10
12
14
16
Fig. 3. CAP
obtained
shows a high-frequency
upward deflection.
in the patient
hearing
dashed lines. The amplitude
the calibration
to condensation
calibrations
I
16
whose audiogram
loss. Negativity
The responses to rarefaction
solid lines and the responses
‘I
20
ms
in Fig. 2,A
is shown
as an
clicks are shown as
clicks are shown as
apply to the records above
bars, and the sound pressure
95
dt?
65
dB
is given in dB Pe SPL.
The same conventions are used in all subsequent figures.
negative peak increases and the peak broadens. There
is only a slight difference
between
the responses
to
condensation
and rarefaction
clicks.
In patients with severe high-frequency
hearing loss
(Figs. 2B and 5) there is a distinct initial peak in the
response to high-intensity
clicks (110 to 90 dB), similar
to the peak seen in patients with normal hearing except that its latency (4.2 ms) is longer than the latency
of the peak in patients with normal hearing (Msller et
al., 1988).
The amplitude
of this initial negative
peak decreased rapidly when the stimulus intensity
was de-
I
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I
I
I
0
1
2
3
4
5
6
7
6
9
10
Fig. 4. Typical CAP obtained
in a patient with normal hearing
ms
13
110
dB
105
dB
waves superimposed on this broad peak. The patient
whose results are shown in Fig. 6 is the only patient
reported on in this paper who had a BAEP component
that led to a suspicion of retrocochlear involvement.
However, this patient’s acoustic middle ear reflex and
speech discrimination scores were normal and his hearing loss was almost equal on both sides.
For the patient whose results are shown in Fig. 7, an
initial negative peak was present in the CAP in response to high-intensity clicks, but this peak was different for condensation and rarefaction clicks. This patient also had waves superimposed on the slow negative deflection that followed the initial peak, the phase
’
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100
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85
110
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dB
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80
dB
-\
105
dB
95
dB
65
dB
75
dB
\
\
;
:
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-\
60
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dB
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f-_-.
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.-
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.--.
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2
4
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6
6
10
12
14
16
16
20
Ills
Fig. 5. Results similar to those shown in Figs. 3 and 4, but from
another patient. This patient’s audiogram
is shown in Fig. 2B.
Similar results were obtained in two other patients
with severe high-frequency hearing losses (Figs. 2C and
6 and Figs. 2D and 7). In the patient whose results are
shown in Fig. 6 there was almost no initial negative
peak in the CAP, even at 110 dB, and the response
consisted of a broad negative peak with a latency
between 8 and 10 ms that resembled the response at 95
dB of the patient illustrated in Fig. 5. Also in the
patient illustrated in Fig. 6 there were several distinct
I
I
1
0
2
4
I
I
I
B
6
10
_
_
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12
14
16
16
20
tn8
Fig. 6. Recordings
similar to those shown in Figs. 3, 4. and 5. but
obtained
in another patient. This patient’s audiogram
is shown in
Fig. 2C.
13
110 dt3
curves. And, in fact, these early components in the
difference curves decrease rapidly in amplitude when
the stimulus intensity is decreased, although clear oscillations may be seen to occur over a large range of
stimulus intensities. These oscillations occur between 6
and 16 ms after the click stimulus, and when examined
closely these oscillations are found to be of slightly
higher frequency in the early portion than in the portions with longer latencies. Corresponding multiple
peaks are seen between fiO0 and 1200 Hz in the power
spectra of these difference functions. It is also notable
that the individual waves appear with almost the same
latency at the different stimulus intensities.
,,^_.
‘/
105
95
dB
dtl
110
dB
..I
85
i_.-
dB
I_.
.-i.
--.
:’
-
_.,“.Z
r
i
‘J
105 df
‘.
1
1
0
2
I
4
1
I
I
I
I
I
I
I
6
6
10
12
14
16
18
20
,-
--
/lOpV
/
ins
Fig. 7. Recordings
similar to those shown in Figs. 3. 4, 5, and 6, but
obtained
in another patient. This patient’s audiogram
is shown in
Fig. 2D.
of which reversed exactly when the polarity of the click
stimuli were reversed,
In a patient with both high- and low-frequency hearing loss, the waveform of the CAP had the normaf
triphasic shape in response to cIicks of high intensity
(105 dB), and there was little difference in the CAP in
response to condensation and rarefaction clicks (Figs.
2E and 8). When the stimulus intensity was decreased
to 90 dB or beIow in this patient, the CAP changed to
a broad negative deflection on which numerous waves
were superimposed, and the phase of these waves
reversed when the click polarity was reversed.
The nature of the waves that are superimposed on
the CAP in patients with hearing loss can be understood better by examining Figs. 9-11, which show
curves representing the difference between the responses to clicks of opposite polarity, together with the
power spectra of these difference functions. The initial
deflection in these curves reflects the difference between responses to rarefaction and condensation clicks
in the initial triphasic component of the CAP. A difference in the latencies of the initial components in the
responses to condensation and rarefaction clicks appears as a large, early deflection in the difference
05
dB
I
,i
;.
80 dEi
0
2
8
6
6
10
$2
14
16
18
20
ms
to those shown in Figs. 3, 4, 5, 6, and 7,
Fig. 8. Recordings
imiiar
but obtained in a patient with both high- and low-frequency
hearing
loss. This patient’s audiogram is shown in Fig. 2E.
15
It may be seen by reviewing Figs. 9-12 that the late
components of the CAP increased with increasing stimulus intensity. This is illustrated in Fig. 13, which shows
the root mean square (RMS) values of the difference
between the responses to condensation and rarefaction
cficks within the interval 4.5-14.5 ms (Fig. 13A). Also
shown is the RMS value of the sum of the responses to
clicks of opposite polarity (Fig. 13B). Fig. 13 shows that
both these measures increase at about the same rate
with increasing stimulus intensity, but the RMS value
of the sum of the responses is about 5 times larger than
the RMS value of the sum of the differences.
There was usually little change in the waveform of
the recorded potentials during the intradural portion
of the operation, but the amplitudes of the potentials
changed in relation to how wet the recording site
became (although the recording electrode was never
covered by fluid when recordings were being made). A
comparison of the late components obtained at different times after the beginning of the intracranial por-
105
d8
75
d8
tion of the operation shows little difference in these
components over time, except for a slight change in
amplitude (Fig. 14). When the recording electrode was
moved from a middle position on the intracranial portion of the eighth nerve to a more distal location near
the porus acusticus, the fatency of ail components
decreased, which is in good agreement with the assumption that the recorded potentials are a result of
propagated neural activity in the auditory nerve.
Of the 4 patients with high-frequency hearing losses
whose results were reported on in the present paper, 3
had such late quasiperiodic waves in their CAP. Of 6
other patients with high-frequency hearing losses who
were operated upon to relieve trigeminal neuralgia
(TN), 4 had such waves in their CAP, and of 5 patients
with both high- and Iow-frequency hearing losses 4 had
similar waves in their CAP. In contrast, only 4 of 17
patients with normal hearing who were operated upon
to relieve TN had detectable waves in their CAP.
Thus, although the late waves occur more frequently
Frewuency
in
kHz
Fig. 9. Difference between the responses to condensation and rarefaction clicks (lefthand curves) in the patient whose audiogram and CAP are
shown in Figs. 2B and 5, and the power spectra (righthand graphs) of these differences. The power spectrum was computed from a 10.24-ms-long
autocorrelation of fhe response shown to its left.
in patients with high-frequency hearing loss, they are
also seen in patients with normal hearing. In these
patients with normal hearing or a mild hearing loss the
late components often consist of a single wave (Fig.
1%.
A typical example of a recording from a patient who
had a noticeable high-frequency hearing loss but no
discernible late components is shown in Fig. 16. It is
seen that the initial negative peak is similar to what is
110
dB
105
dB
100
dB
95
dB
90
65
60
75
seen in patients with normal hearing. However, there is
no discernible response at 90 dB Pe SPL and below,
due to the patient’s hearing loss.
Discussion
The results of the present study show that the
waveform of the CAP that can be recorded from the
110
dB
105
dB
100
dB
dB
95
dB
90
dB
65
dB
80
dB
75
dB
dB
dB
dB
_-_-
5
I
0
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2
4
6
a
10
12
14
16
16
20
ms
0.02
0.05
0.1
0.2
0.5
Frequency
Fig. IO. Results similar to results shown in Fig. 9, but for the patient whose audiogram
0.7
1
in
2
3
5
7
dB
10
kHz
and CAP are shown in Figs. 2C and 6. The small peak!
seen in the spectra at about 1500 Hz are probably a result of electrical
interference.
17
intracranial portion of the eighth nerve in patients with
different degrees of high-frequency hearing loss is more
complex than the waveform of the response in patients
with normal hearing. The CAP recorded from the
eighth nerve in patients with high-frequency hearing
loss has a broad peak with a latency between 6 and 10
ms in the response to clicks presented at an intensity of
90 dB or less. In a high proportion of such patients,
quasiperiodic oscillations occur in the interval between
6 and 16 ms after the stimulus. Similar waves are seen
less often in patients with normal hearing. Based on
the latency and the frequency of oscillation of these
components in the CAP in response to broadband
clicks, they are believed to be a result of excitatory
vibrations of the apical portion of the basilar membrane.
Because the CAP recorded from a nerve is the
convolution of a single nerve impulse with the weighted
sum of the temporal distribution of nerve impulses in
all the nerve fibers contributing to the response (Goldstein, 19601, the waveform of the CAP recorded from
the eighth nerve reflects the distribution in time of
110
dB
nerve impulses in the population of nerve fibers that
are activated. When the waveform of a single action
potential is known, the distribution of nerve impulses
can be estimated by deconvolution of the recorded
CAP and a single nerve action potential. Deconvolution of two waveforms in the time domain is equivalent
to dividing the spectra of the two waveforms. Because
the spectrum of a single action potential has a bandpass characteristic, rapid changes in the distribution of
nerve impulses will appear more prominently in the
CAP than slow changes, and steady-state discharge
rates are not reflected at all in the CAP. The sharp
initial wave of the CAP may therefore reflect the
distribution of nerve impulses in time more accurately
than the broad wave in the CAP, and the distribution
of nerve impulses in time is likely to be even broader
than the broad peak in the CAP. This is naturally
predicated on the assumption that the waveforms of
single nerve impulses are all the same and not noticeably different in patients with hearing loss from waveforms of nerve impulses in patients with normal hearing. That this is indeed the case is indicated by the fact
n
105 dB
95
dB
110
65
75
I
dB
dB
dB
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I
95
dB
55
d0
75
dB
I
Frequency
Fig. 11. Results
similar
to results
shown
in
kHz
in Fig. 9, but for the patient whose audiogram
and CAP are shown in Figs. 2D and 7. The sharp
seen above about 1800 Hz are the result of electrical interference.
peaks
that the initial negative peak in the CAP elicited by
high-intensity sounds is similar in patients with hearing
loss and those with normal hearing. Thus, it seems
reasonable to assume that the hearing loss of the
patients presented in this study was a result of cochlear
impairment and thus was unlikely to have caused any
change in the waveforms of single nerve impulses.
The CAP that can be recorded from the inner ear
using the technique known as electrocochleography
(ECoG) is in many ways similar to the CAP that can be
recorded from the intracranial portion of the eighth
nerve. Late and broad peaks in the CAP from the
eighth nerve, similar to those seen in the present study,
have been reported in the ECoG response of a patient
with high-frequency hearing loss (Elberling, 1974). In
these recordings from the ear canal, the initial sharp
negative peak that was present at high sound intensities was lost when the stimulus intensity was lowered to
75 dB Pe SPL, and below this stimulus intensity only a
slow and broad peak remained. Elberling (1974) used
masking with highpass-filtered noise, similar to a technique used in animal experiments (Teas et al., 1962), to
determine derived action potentials in normal-hearing
110
dB
105
dB
95
human subjects. These derived responses were assumed to represent the responses of specific areas of
the basilar membrane, and Elberling (1974) concluded
that this broad peak was the result of excitation of the
1500-Hz region of the basilar membrane, thus the area
immediately below the sharp cutoff of the patient’s
pure tone audiogram. At 95 dB Pe SPL, the latencies
of these derived action potentials were 6.5 ms at 0 to
500 Hz, 4.8 ms for the range 500 to 1000 Hz, 3 ms at 1
to 2 kHz, 2.5 ms for 2 to 4 kHz, and about 1.8 ms for
the range above 4 kHz. The conduction time in the
auditory nerve from the cochlea to the location on the
eighth nerve from which we recorded can be assumed
to be about 1 ms on the basis of its conduction velocity
(20 to 40 m/set, Lazorthes et al., 1961; Spoendlin and
Schrott, 1989) and the distance (which is about 2 cm,
Lang, 1981, 1983). The latency of the broad peak in the
CAP in the patient in our study who had a hearing loss
above 1000 Hz (Fig. 2D) was 8 to 10 ms, which indicates that this peak originated from the 500 to 1000 Hz
region of the basilar membrane, a situation similar to
the one reported by Elberling (1974).
The findings of the present study are in agreement
dB
,
85
110
dB
105
dB
dB
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18
dB
85
dB
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95
ms
0.02
5
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I111111
0.05
0.1
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0.2
I I II
III
0.5
Frequency
Fig. 12. Results similar to those shown in Fig. 0, but from the patient whose audiogram
0.7
1
,n
I
I
lllllll
2
3
5
ktir
and CAP are showm,ln Figs. 2E and 8
7
dB
10
19
with those of Coats and Martin (1977) that the latenties of the nerve action potentials recorded from the
ear canal are generally prolonged in patients with
high-frequency hearing loss and that in these patients
there is a greater difference between the responses to
clicks of opposite polarity than is found for patients
with normal hearing. Although we studied only a small
number of patients and their audiograms represent
only a portion of the spectrum of results that may be
expected from those with high-frequency hearing loss,
our results also agree with those of Coats and Martin
(1977) in that they show that there is poor correlation
between deviation of the CAP from normal and the
shape of the audiogram in individual patients. Coats
and Martin (1977) also found that the components
following the initial negative peak in the response
recorded from the ear canal seemingly reversed in
phase when click polarity was reversed. Because this
component consists of only one wave it is difficult to
distinguish such a shift from a shift in latency. We see
similar components in our recordings from the exposed
intracranial-portion
of the eighth nerve (c.f., Fig. 3 at
110 dB). These components are different from the
much more prolonged quasiperiodic oscillations that
we
have shown occur in recordings from the exposed
intracranial portion of the eighth nerve in the present
study as well as in a previous study (Moller and Jho,
1990). These oscillations occur in the time interval
between 5 and 15 ms after the click sound.
In the present study we showed that such waves are
indeed common in patients with severe high-frequency
hearing loss, although they do occur in individuals with
normal or near-normal hearing.
We earlier pointed out that there are similarities in
latency and frequency range between the oscillations
we observed in the CAP recorded from the eighth
nerve and evoked otoacoustic emissions (Moller and
Jho, 1990). However, there is at least one important
difference, namely that otoacoustic emissions are a
nearly constant phenomenon and most pronounced in
people with normal hearing, while the late waves in the
CAP occur rarely in individuals with normal hearing
and preferentially in patients with high-frequency hearing losses of cochlear origin.
The long duration of these oscillations and the fact
that they reverse precisely when the polarity of the
click sound is reversed indicate that they are the result
of a damped oscillation of a bandpass filter that has a
UV
0
6.0
r
DIFFERENCE
4.0
-
3.5
-
2.5
-
0.25
70
75
00
05
90
95
100
dB
105
110
70
PeSPL
I
I
I
I
I
75
60
65
90
95
dB
I
100
I
105
I
110
PeSPL
Fig. 13. (A) RMS values of the difference between the late waves in response to condensation
and rarefaction
clicks determined
in the interval
4.5 to 14.5 ms after the stimulus and shown as a function of the stimulus intensity. (B) RMS values of the sum of the responses to condensation
and rarefaction
clicks in the interval 0 to 20 ms after the stimulus. In both graphs, open circles represent data from the patient illustrated in Fig.
2A, crosses show data illustrated
in Fig. 2B, filled circles show data illustrated
in Fig. 2C, squares show data illustrated in Fig. 2D, and triangles
show data illustrated
in Fig. 2E.
narrow bandwidth. The fact that the latencies of the
individual waves of this oscillation are nearly independent of the stimulus intensity indicates that these components are the neural responses to continuous excitation. In this respect, these oscillations are similar to
responses caused by stimulation with low-frequency
tonebursts, where the latency of the individual waves in
the response also is nearly independent of the stimulus
intensity (Moller and Jho, 1989a). Similar results have
been obtained in animal experiments using noise stimuli (Msller, 1975, 1983).
The relatively high amplitude of these oscillations
(about 20% of the total amplitude of the CAP) is an
indication that these late waves represent neural activity in a large number of nerve fibers that is phase-locked
to frequencies within a very narrow range. If the frequencies of the damped oscillations to which the individual nerve fibers were phase-locked differed by any
noticeable amount from each other, the resulting gross
response would not contain such sustained oscillations
but rather would have the shape of a single deflection
marking the beginning of the damped oscillations. In
order to account for the results of this study and the
105
dB
105
dB
95
d6
.",--)\;
a5
dB
/_
75
d6
,__-
-.
:
6._-
d’
13:26
,’
65
dB
$1
i,
13136
DISTAL
I(
‘1
I
11
I
Fig. 15. CAP recorded
(normal
I
I
I
I
I
I
I
I
I
I
I
0
2
4
6
a
IO
12
14
16
ia
20
Fig.
14. Difference
rarefaction
between
clicks obtained
bers) during
the intradural
the
responses
at different
portion
to condensation
to relieve
and
TN.
The three top recordings were made from the middle portion of the
intracranial
obtained
ings were
portion
of the eighth nerve, and the bottom record was
from a distal location near the porus acusticus. The recordobtained
from
the same patient
whose
atidiogram
CAP are shown in Figs. 2D and 7, respectively.
I
I
L
11
12
13
14
from a patient with only a slight hearing
15
Ills
loss
to 4000 Hz, 25 and 20 dB at 6000 and 8000 Hz, respectively).
ms
times (given by legend num-
of an operation
I
10
0123456789
and
earlier one (Moller and Jho, 19901, it seems necessary
to assume that as many as 20% of the nerve fibers that
are activated by a high-intensity click sound are phaselocked to low frequencies within a very narrow range to
produce these oscillations. If we accept that the basilar
membrane is the source of the oscillation to which the
neural activity is phase-locked and that the basilar
21
110
dB
105
dB
95
dB
90
d0
/
2.5~”
1 0.5pv
I
0
I
1
I
I
I
I
I
I
2
3
4
5
6
7
I
I
I
8
9
10
ms
Fig. 16. CAP recorded from a patient with a rather severe hearing
loss but no discernible late waves. (Normal to 1000 Hz, down 55 dB
at 2000 and 4000 Hz, and 85 dB at 6000 and 8000 Hz.)
membrane is continuously tuned along its length to
frequencies within the audible range, then it is difficult
to understand how so many nerve fibers could be tuned
to nearly the same frequency.
The oscillations in the CAP could be explained in
another way. Perhaps there are one or a few narrow
regions of the basilar membrane with extreme degrees
of frequency selectivity. This would result in prolonged
ringing when the ear is excited by a broadband transient sound. Such a high degree of frequency selectivity
could occur at localized spots on the basilar membrane
as a result of large discontinuities in the properties of
the basilar membrane. In explaining the mechanism of
otoacoustic emission, it has been put forward that
positive feedback systems could produce very high degrees of spectral selectivity at a certain point on the
basilar membrane, which would account for the prolonged oscillations. The long latency of the otoacoustic
emissions was explained by a slowing in propagation of
the traveling wave as it approaches the region of high
selectivity (Kemp, 1978). While this is a plausible explanation for the otoacoustic emission, it is difficult to
understand how a sufficient number of nerve fibers
could be activated by the vibration of such a small area
of the basilar membrane that would account for the
large amplitude of the oscillations in the CAP.
There are two reasons why it does not seem likely
that these waves are a result of the loss of hair cells in
the basilar region of the cochlea per se. First, the
low-frequency nature of the oscillations and their long
latency indicate that the waves originate from apical
cochlear regions, which on the basis of the normal
low-frequency hearing threshold may be assumed to be
normal. Second, the long latency of these waves seems
to indicate that the traveling wave has already passed
the region of the cochlea that represents the frequency
region of impaired hearing threshold. It thus seems
that noise exposure, aging, or whatever other factor
caused the (selective) high-frequency hearing loss in
these patients also in one way or another injured or
affected the low-frequency region of the basilar membrane in such a way that it produced these abnormal
oscillations, without affecting the threshold for pure
tones to a noticeable degree. Studies of changes in the
cochlea that occur as a result of aging or exposure to
noise have shown a loss of hair cells in the basal
portion of the cochlea but no noticeable pathologies in
the more apical portion of the cochlea (Hawkins and
Johnsson, 1976).
It is naturally difficult to speculate about what effect
these late waves in the CAP of patients with highfrequency hearing losses may play in auditory function,
but in view of the large amplitude of these oscillations
and the fact that they occur over a large range of sound
intensities, one would expect that they would have
perceptual correlates. However, so far the only such
abnormal phenomenon observed in patients with highfrequency hearing loss is tinnitus, and this is often
associated with high-frequency hearing loss.
It is surprising that, in the numerous animal experiments that have been carried out on noise-induced
hearing loss and hearing loss caused by ototoxic drugs,
no such waves have been reported. If similar waves do
not exist in animals in which hearing loss has been
induced by exposure to noise or ototoxic drugs, other
explanations for their existence in man must be sought.
One difference between most studies of noise-induced
22
hearing loss in animals and those in man is that most
animals are studied relatively soon after a hearing loss
has been induced, whereas the patients we have studied have in most cases had the hearing loss for many
years. Perhaps there are changes that occur over time
that are not noticeable in the acute or relatively acute
time frame of the animal experiments performed to
date.
In the present study we only included data from
patients who were operated upon for relief of TN,
although we have data from patients operated upon for
relief of hemifacial spasm (HFS) or disabling positional
vertigo (DPV). We did not include patients with HFS
or DPV in this study because of the possibility that
their auditory nerves might have been affected by the
vascular compression of the facial nerve or the vestibular nerve that causes these diseases. In fact it has been
shown (Moller and Moller, 1985) that some patients
with HFS have audiometric abnormalities that can be
associated with vascular compression of the auditory
nerve, in addition to the vascular compression of the
facial nerve that is the cause of their disease, and that
these audiometric abnormalities occur only on the side
with HFS. Because the anatomic distance between the
eighth nerve and the trigeminal nerve is quite large, it
is unlikely that the blood vessel that compresses the
trigeminal nerve could also affect the eighth nerve.
Also, the fact that the patients we studied had similar
hearing loss on both sides while only the trigeminal
nerve on one side was affected by vascular compression
further indicates that the hearing loss was not a result
of the vascular abnormality that gave rise to TN.
Finally, the operating room is not an ideal environment for recording CAP from the eighth nerve because
it is impossible to shield the patient fully from electrical and acoustic noise. The effects of electrical interference can be reduced by averaging more responses,
but ambient sounds will always mask the test sounds to
some extent. This masking prevents measurement of
responses to test sounds of low intensities, and thus
limits the range of sound intensities over which responses can be studied. In addition, the ambient noise
in the operating room may affect the responses in one
way or another, but since the noise changes constantly
in nature it is difficult to obtain a valid estimate of its
character. Nevertheless, we have attempted to reduce
the noise that reaches the patient’s ear by careful
placement and taping of the earphone in the ear, and
the fact that we can obtain responses from patients
with normal hearing down to 25 to 30 dB above the
perceptual threshold of the clicks indicates that the
degree to which ambient noise in the operating room
masks the test tones is moderate. Thus, we believe that
such ambient noise has not affected the results presented in this paper except for limiting the intensity
range over which potentials could be studied.
Acknowledgements
This work was supported by the National Institutes
of Health (Grants No. ROl-NS21378 and No. ROlDC00272). The authors are grateful to Peter J. Jannetta, M.D., for making patients under his care available for this study, and to Margareta B. Moller, M.D.,
D.Med.Sci., for audiological evaluation of the patients
in the present study.
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