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Hearing Research 306 (2013) 11e20

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Hearing Research
journal homepage: www.elsevier.com/locate/heares

Research paper

Transmission of bone conducted sound e Correlation between hearing


perception and cochlear vibration
Måns Eeg-Olofsson a, *, Stefan Stenfelt b, Hamidreza Taghavi c, Sabine Reinfeldt c,
Bo Håkansson c, Tomas Tengstrand d, Caterina Finizia a
a
Department of Otorhinolaryngology Head and Neck Surgery, Sahlgrenska University Hospital, The Sahlgrenska Academy, Göteborg University,
Gröna Stråket 5, S-413 45 Göteborg, Sweden
b
Department of Clinical and Experimental Medicine, Linköping University, Linköping, Sweden
c
Department of Signals and Systems, Chalmers University of Technology, Göteborg, Sweden
d
Department of Technical Audiology, Sahlgrenska University Hospital, Göteborg, Sweden

a r t i c l e i n f o a b s t r a c t

Article history: The vibration velocity of the lateral semicircular canal and the cochlear promontory was measured on 16
Received 15 June 2013 subjects with a unilateral middle ear common cavity, using a laser Doppler vibrometer, when the
Received in revised form stimulation was by bone conduction (BC). Four stimulation positions were used: three ipsilateral posi-
26 August 2013
tions and one contralateral position. Masked BC pure tone thresholds were measured with the stimu-
Accepted 28 August 2013
Available online 15 September 2013
lation at the same four positions. Valid vibration data were obtained at frequencies between 0.3 and
5.0 kHz. Large intersubject variation of the results was found with both methods. The difference in
cochlear velocity with BC stimulation at the four positions varied as a function of frequency while the
tone thresholds showed a tendency of lower thresholds with stimulation at positions close to the co-
chlea. The correlation between the vibration velocities of the two measuring sites of the otic capsule was
high. Also, relative median data showed similar trends for both vibration and threshold measurements.
However, due to the high variability for both vibration and perceptual data, low correlation between the
two methods was found at the individual level. The results from this study indicated that human hearing
perception from BC sound can be estimated from the measure of cochlear vibrations of the otic capsule. It
also showed that vibration measurements of the cochlea in cadaver heads are similar to that measured in
live humans.
Ó 2013 Elsevier B.V. All rights reserved.

1. Introduction transducer results in a standardized and known perception of the


BC stimulation, as specified by the Reference Equivalent Threshold
If the vibration level of a transducer is high enough, stimulation Force Level in the international standard ISO 389-3 (1994). This
of bone conducted (BC) sound can be heard from any position of the means that when the transducer and/or position are altered, the BC
head, and most probably from other positions on the body as well. perception is altered and reference data are required (McBride
One problem is that in practice, only stimulation at the mastoid et al., 2008). Such normalization is burdensome and requires a
(and to some extent, the forehead) using a Radioear B-71 large number of humans for the data to be reliable. Another way to
estimate the sensitivity of the BC stimulation has been proposed by
the measure of cochlear vibration (Buchman et al., 1991; Eeg-
Abbreviations: AC, air conduction; BAHA, Bone anchored hearing aid; BC, bone Olofsson et al., 2008, 2011; Håkansson et al., 2008; Håkansson
conduction; BCI, bone conduction implant; CSF, cerebrospinal fluid; dB, decibels;
et al., 2010; Stenfelt, 2005; Stenfelt, 2006; Stenfelt and Goode,
HL, hearing level; LDV, laser Doppler vibrometer; LSCC, lateral semicircular canal;
MAPP, mastoid surface area that attaches to the petrous part of the temporal bone; 2005b; Stenfelt et al., 2000, 2002, 2003b, 2004a, 2004b). Even if
SD, standard deviation; SNR, signal to noise ratio; TA, transcranial attenuation vibration data have shown correlation to perceptual data (Stenfelt,
* Corresponding author. Tel.: þ46 706569586. 2012), there are no publications of direct measures linking BC
E-mail addresses: manseegolofsson@gmail.com, m.eeg-o@bredband2.com perception and cochlear vibrations.
(M. Eeg-Olofsson), stefan.stenfelt@liu.se (S. Stenfelt), taghavi@chalmers.se
(H. Taghavi), sabine.reinfeldt@chalmers.se (S. Reinfeldt), boh@chalmers.se
One issue is how valid the cochlear vibrations are for estima-
(B. Håkansson), tomas.tengstrand@vgregion.se (T. Tengstrand), caterina.finizia@ tions of BC hearing and another issue is how the vibrations of the
orlss.gu.se (C. Finizia). cochlea should be measured. Unlike for air conduction (AC), where

0378-5955/$ e see front matter Ó 2013 Elsevier B.V. All rights reserved.
http://dx.doi.org/10.1016/j.heares.2013.08.015
12 M. Eeg-Olofsson et al. / Hearing Research 306 (2013) 11e20

the ear canal sound pressure serves as an easily accessible good outer ear called “radical mastoidectomy”. This surgical method
proxy of the cochlear stimulation (given a normal functioning implies that the posterior ear canal wall is removed and the ear
middle ear), the measurement of cochlear vibration during BC vi- canal opening is widened. If the middle ear space is sealed, it is
bration is complicated. As a consequence, most measures of called a modified radical mastoidectomy. The result in both cases is
cochlear vibration have been conducted in temporal bones, dry called a middle ear common cavity. When examining an ear with a
skulls, and cadaver heads (Eeg-Olofsson et al., 2008, 2011; middle ear common cavity, the lateral semicircular canal (LSCC) is
Håkansson et al., 2008; Håkansson et al., 2010; Stenfelt, 2006; often exposed as well as the cochlear promontory. In previous
Stenfelt and Goode, 2005b; Stenfelt et al., 2000, 2002, 2003b, cadaver studies (Eeg-Olofsson et al., 2008, 2011; Håkansson et al.,
2004a, 2004b). To complicate things further, BC perception is not 2008; Håkansson et al., 2010; Stenfelt and Goode, 2005b; Stenfelt
an isolated phenomenon but several pathways contribute to the et al., 2000) the cochlear promontory was used as a target for the
perception (Stenfelt, 2011; Stenfelt and Goode, 2005b; Stenfelt laser beam. The cochlear promontory is easily exposed when lifting
et al., 2002, 2003a; Tonndorf, 1966). However, it has been shown the tympanic membrane and removing the middle ear ossicles. In a
that a vibration of the otic capsule produces basilar membrane live human with normal ear anatomy, this is not possible unless it is
vibration patterns similar to that with AC stimulation (Stenfelt done during middle ear surgery. Therefore, in this study, we have
et al., 2003b). Also, it is hypothesized that inertial effects of the included subjects with a middle ear common cavity where the laser
fluid in the cochlea is the major cause for BC response in the normal beam can be aimed through the wide ear canal opening. In these
ear at frequencies below 4.0 kHz (Stenfelt, 2011; Stenfelt and subjects, the LSCC and/or the cochlear promontory are accessible
Goode, 2005b; Stenfelt et al., 2004a). Thus, when the cochlea vi- for vibration measurements using an LDV.
brates the inner ear fluid flows between the scala vestibuli and the Both the LSCC and the cochlear promontory are part of the hard
scala tympani without any deformation of the cochlear walls. bone encapsulating the inner ear structures. This hard bone is
Above 4.0 kHz other pathways contribute to the basilar membrane called the otic capsule. At low enough frequencies, the otic capsule
stimulation, for example compression and expansion of the is expected to vibrate as a rigid body in response to BC stimulation.
cochlear walls (Stenfelt and Goode, 2005a; Tonndorf, 1962). Stim- This means that the LSCC and the cochlear promontory velocity
ulation of the inner ear through the cerebrospinal fluid (CSF) has responses are hypothesized to be similar. However, this hypothesis
also been proposed as a contribution to BC sound perception needs to be validated.
(Sohmer et al., 2000) based on the connection between the inner The aims of this study are to:
ear and the CSF through bony canals. If sound transmission from
the CSF is important for BC sound, the vibration of the cochlea may 1. Investigate the vibration pattern of the otic capsule in live
not be related to the perception of BC sound and estimation of BC humans during BC stimulation and compare it to similarly ob-
sound from cochlear vibrations would be invalid. However, there is tained cochlear vibration patterns in human cadavers presented
no indication that the CSF route is a major contributor for BC sound in the literature.
in the normal ear (Stenfelt and Goode, 2005b). 2. Investigate the relation between the otic capsule vibration and
The vibration of the cochlea has been measured with acceler- BC hearing thresholds.
ometers (Buchman et al., 1991; Stenfelt, 2005; Stenfelt, 2006; 3. Investigate the relation of the vibration level between the
Stenfelt and Goode, 2005b; Stenfelt et al., 2000) or by a laser cochlear promontory and the LSCC during BC sound stimulation.
Doppler vibrometer (LDV) (Eeg-Olofsson et al., 2008, 2011;
Håkansson et al., 2008; Håkansson et al., 2010; Stenfelt, 2006;
Stenfelt and Goode, 2005b; Stenfelt et al., 2002, 2003b, 2004a, 2. Materials and methods
2004b). Even if only accelerometers have been reported for the
estimation of the three-dimensional response of the cochlea This study was approved by the Regional Ethical Review board,
(Stenfelt and Goode, 2005b; Stenfelt et al., 2000), LDVs can be used Göteborg.
to measure the cochlear vibration in three-dimensions as well. The
drawback of using accelerometers is their size and that they require 2.1. Subjects and stimulation positions
a physical bond with the vibrating surface. The latter is difficult to
accomplish when measuring the cochlear vibrations, especially in The estimation of a sufficient sample size for the statistical an-
live humans. The LDV measures the velocity of the vibrations at a alyses was based on a power analysis using LDV data from a pre-
point with a thin laser beam enabling contactless measurements. vious cadaver study (Eeg-Olofsson et al., 2008) with a power of 0.8.
Studies on dry skulls and cadaver heads have used a single point The power analysis was based on the frequency response of the
LDV measuring one-dimensional response of the cochlear prom- cochlear vibration from ipsilateral BC stimulation positions similar
ontory (Eeg-Olofsson et al., 2008, 2011; Håkansson et al., 2008; to those in the current study. The results from the power analysis
Håkansson et al., 2010; Stenfelt and Goode, 2005b; Stenfelt et al., suggested that 14 subjects should be included. Patients were
2000). These studies have used the lateral-medial direction (here- identified from the database at the clinic of Otolaryngology Head
after termed x-direction) as the response direction with the argu- and Neck surgery at the Sahlgrenska University Hospital, Göteborg,
ment that it is close to the maximum vibration level of the cochlea Sweden, as being due for a “cleaning of a middle ear common
for any direction when the stimulation is at the skull surface cavity”. In total, 21 subjects were invited with the following in-
(Stenfelt and Goode, 2005b). As stated above, there are several clusion criteria: (1) unilateral middle ear common cavity (test ear
studies that have measured the cochlear vibration in cadaver heads side). (2) No major conductive impairment at the contralateral
but no reports on the cochlear vibration in live humans. Moreover, (non-test) ear (an average air-bone gap 25 dB was accepted at
no study on the correlation between the cochlear vibration and the frequencies between 0.5 and 4.0 kHz). Sensorineural hearing loss at
perceptual data in the same subjects has been published. the contralateral ear was accepted. (3) Either the LSCC or the
To enable comparison of cochlear vibration and perception of BC cochlear promontory (or both) visible in the test ear with an ear
sound, for example BC hearing thresholds, hearing assessment and microscope.
visible cochlear structures are required in the same subjects. Such Of the 21 invited subjects, 4 declined to participate. One addi-
subjects can be found among individuals who have been treated for tional subject terminated the study after some initial testing.
chronic ear disease with a surgical method of the middle and the Consequently, 16 subjects (7 females, 9 males, average age 48 years
M. Eeg-Olofsson et al. / Hearing Research 306 (2013) 11e20 13

ranging from 24 to 70 years) remained and completed the study


(see Table 1). Twelve subjects had access to both the cochlear
promontory and the LSCC, one subject only to the cochlear prom-
ontory, and in three subjects only to the LSCC.
The BC stimulation was generated by a B-71 transducer (Radi-
oear corp., USA) that was placed at four different predefined loca-
tions on the head. The same transducer was used for all
measurements. The B-71 was calibrated for the output force level
using a Brüel & Kjær artificial mastoid Type 4930 (Brüel & Kjær,
Nærum, Denmark) before and after the tests. A steel-spring head-
band kept the transducer at the positions with a static force of
approximately 5.4 N (Newtons). The four stimulation positions
where termed position A to D. Positions A, B and C were on the
ipsilateral side of the skull (the same as the test ear) and position D
was on the contralateral side opposite to position A (Fig. 1). First, a
straight line was identified with the direction from the lateral angle
of the eye (angulus oculi lateralis) and the upper boarder of the
pinna. Position A was the point where a 55 mm line from the
posterior boarder of the ear canal opening attached to the first line.
This is normally the position where an implant for the Bone
anchored hearing aid (BAHA) is attached (Tjellström et al., 2001).
Position B was as close to the pinna as possible on the line between
position A and the ear canal opening. During the measurements,
the pinna was pushed forward and secured with sticky tape to
avoid contact between the transducer casing and the pinna. Posi-
tion C was on the zygomatic root close to, but without touching, the
tragus. The distances between positions A and B as well as between
positions A and C were recorded. Position D was located using the Fig. 1. The four stimulation positions are shown and their identification illustrated.
same procedure as for position A, but on the contralateral side. Position A is 55 mm behind and slightly above the ear canal opening (normal site for
Bone anchored hearing aid implant). Position B is closer to the ear canal opening, on
the line between position A and the ear canal opening. Position C is on the zygomatic
2.2. Hearing thresholds root in front of the tragus. Position D is same as position A but on the contralateral side.

Hearing thresholds were obtained in a 6.5 m2 and 14.9 m3 sound noise according to ISO 389-4 (1994). Masked BC hearing thresholds
attenuated room according to ISO 8253-1 (2010). Masking in the at one-third octave frequencies between 0.25 and 8 kHz (total 16
contralateral (non-test) ear was achieved by a deeply inserted frequencies) were then obtained with stimulation at the positions
standard ER-2 plug. All thresholds were estimated by the ascending AeD using 5 dB step-size and narrow-band masking of the non-test
method of Hughson-Westlake (ISO 8253-1 (2010)). First, non- ear.
masked AC hearing thresholds at the non-test ear was obtained To ensure that the thresholds were not affected by airborne
for the frequencies 0.25, 0.5, 1, 2, 4, 6, and 8 kHz using a 5 dB step- sound radiation from the BC transducer, the ear canal sound pres-
size. These thresholds were used to determine the masking levels sure was monitored at 1 and 4 kHz using an ER7C probe-tube
for the BC threshold measurements with stimulation at the posi- microphone (Etymotic research Inc, Elk Grove Village, IL 60007,
tions AeD. Then, at the same ear and for the same frequencies, USA). The ear canal sound pressure was measured with BC stimu-
masked BC thresholds were obtained using narrow-band masking lation at positions A, B and C at a level of 50 dB HL and the results

Table 1
Individual data for the 16 subjects. BAHA ¼ Bone anchored hearing aid; A, B, C, ¼ stimulation positions; Prom ¼ Promontory; LSCC ¼ Lateral semicircular canal; PTA ¼ Pure tone
average; nt ¼ non-test ear; t ¼ test ear; SSD ¼ Single sided deafness.

Subject Sex Age BAHA Distance (mm) Prom LSSC PTA AC nt PTA BC nt PTA AC t 1/3 octave
AeB/AeC 0.25, 0.5, 1.0, 2.0/4.0, 6.0, 8.0 kHza 0.25, 0.5, 1.0, 2.0/4.0, 6.0, 8.0 kHz 0.25e2.0/2.5e8.0 kHz

1 M 70 Y 38/80 Y Y SSD SSD 59/70


2 M 67 N 30/59 N Y 38/58 24/45 72/71
3 F 64 Y 36/72 Y Y 28/65 34/62 (no result 8 kHz) 80/95 (no result 4, 5, 6.3, 8 kHz)
4 M 56 Y 36/76 Y Y 10/47 24/33 (no result 8 kHz) 95/>110 (discharge test ear)
5 M 54 N 38/69 N Y 28/55 6/50 47/72
6 F 54 Y 29/67 Y Y 31/38 26/45 74/65
7 F 53 Y 40/73 Y Y 5/28 25/12 79/78
8 M 51 N 24/64 N Y 23/47 16/22 49/74 (no result 8 kHz)
9 F 48 Y 37/77 Y N 28/28 0/10 56/41
10 M 47 N 20/59 Y Y 8/17 8/13 41/51
11 F 41 Y 26/72 Y Y 9/12 10/8 45/43
12 M 41 N 31/71 Y Y 1/15 11/20 67/46
13 F 36 N 32/62 Y Y 4/8 8/10 45/41
14 F 31 N 31/65 Y Y 4/8 10/17 59/57
15 M 24 N 27/68 Y Y 9/8 0/0 55/62
16 M 38 N 30/66 Y Y 11/18 0/17 27/43
a
Unmasked.
14 M. Eeg-Olofsson et al. / Hearing Research 306 (2013) 11e20

were recalculated to the sound pressure level at BC hearing different frequencies. The same signal analyzer recorded the
thresholds. The same transducer was used at all measurements. response signal from the LDV. The stimulation was a stepped sine
The results showed that the calculated sound pressure level in the between 0.1 and 10 kHz with a 1/64 octave band frequency reso-
ear canal at masked BC threshold for position A, B and C were lower lution (total 401 frequencies). The result was a frequency response
than the masked AC threshold of the test ear for all subjects. In function of the velocity of the cochlear promontory and the LSCC.
other words, the thresholds were not affected by airborne sound Three measurement sweeps were done and averaged for each
radiation from the BC transducer. stimulation position, both for the cochlear promontory and the
During the initial analysis of the results an unfortunate proce- LSCC.
dural error was discovered and the threshold measurements were Two noise estimates were made to investigate the quality of the
remeasured. When the initial thresholds for position D were measurements; one estimate with 100% laser beam reflection and
measured, the masking was incorrectly in the test ear. Another one with approximately 50% laser beam reflection as indicated on
problem at the initial threshold measurements was that the stan- the LDV apparatus. Almost all measurements of the LSCC and the
dard masking procedure (plateau technique) was not always suf- cochlear promontory vibration were done with a laser beam
ficient to mask the non-test ear. A substantial part of the thresholds reflection close to 100%. The results were recalculated to a BC
were heard in the non-test ear or in the middle of the head. As a stimulation level of 1 N using the calibration data of the B-71
result, at the second session when the thresholds were remeasured, transducer. This recalculation allowed comparisons with previous
the masking procedure was changed (described below) and warble studies (Eeg-Olofsson et al., 2008, 2011).
tones were used. Both sessions included threshold measurements
at all positions at 16 frequencies between 0.25 and 8.0 kHz with 1/3 2.4. Statistical methods
octave resolution. The following presents the masking level pro-
cedure used at the second session which always started at position Wilcoxon’s signed rank test was used in order to test differences
D: between positions within each frequency (third octave band).
An initial non-masked threshold was obtained. If the tone was Spearman correlation was calculated for a pair of variables within
heard in the test-ear, the masking level was set as the AC threshold each frequency band. The correlation coefficients were then tested
of the non-test ear plus 20 dB. However, if the tone was heard in the with Wilcoxon’s signed rank test. All tests were two-tailed.
non-test ear, the masking level was raised starting at the AC
threshold level of the non-test ear until: 3. Results

a. the tone was not heard. Then the masking level and the tone 3.1. General results
level were raised parallel until the tone was heard in the test ear.
b. the tone was heard in the test ear. The distance between position A and B was on average
32  6 mm (1 standard deviation (SD)), and between position A and
The masking level was then set at a 20 dB higher level. There- C on average 69  6 mm (1 SD). The individual results are given in
after, a masked threshold was obtained using 5 dB step size. From Table 1. The distance variation is primarily caused by the subjects’
this threshold, a more detailed masked threshold was obtained anatomy differences, but also a result from BAHA fixture abutments
using a 2 dB step size. The same threshold procedure was applied at in two subjects. These abutments were at, or in the vicinity of,
the other positions using the stored masking level obtained for position A and in subjects 3 and 9 position A was slightly behind
position D at each frequency. and below the normal position A to avoid interference with the
If the tone was heard in the non-test ear or in the middle of the BAHA abutment.
head despite the described masking procedure, the subject was Due to the generic design of the transducer (B71), the stimula-
instructed to indicate this and the threshold obtained was marked tion force levels at the transducereskull interface are low at low
as “wrong ear” or “both ears”. These marked thresholds were not and high frequencies. To ensure a valid response of the LDV mea-
included in the analysis of the thresholds. Also, if no threshold surements it was decided to only include data with a signal to noise
could be obtained for the reason of overmasking, no result was ratio (SNR) of a minimum 10 dB. When the responses from the LDV
registered for that specific frequency. were analyzed and compared to measurements of the noise only, a
valid frequency range for all measurements was determined to be
2.3. Laser measurements at frequencies between 0.3 kHz and 5.0 kHz. As a consequence,
even if all LDV measurements were done with a frequency range of
The identification of the 4 positions A, B, C and D was done by 0.1e10.0 kHz, the LDV results are only presented at frequencies
the first author. The measurements order for the LDV testing was: between 0.3 and 5.0 kHz. When the first and second measurement
A, B, C, D, A. The data from the second measurement at position A at position A was analyzed, the test-retest difference was on
were compared to the first measurement at position A and used to average below 0.5 dB (the average absolute difference was below
estimate the test-retest reliability. 2.8 dB).
The beam of the LDV (HLV-1000, Polytech Gmbh, Waldbronn,
Germany) was aimed at the skin covered cochlear promontory or 3.2. Velocity response of the otic capsule
the LSCC. To ensure a good reflection of the laser beam, small glass
spheres (P-Retro-x, Polytec) 45e63 mm in diameter were posi- In three subjects the promontory was not exposed and in one
tioned on the cochlear promontory and/or the LSCC using a thin subject the LSCC was not exposed. In the twelve subjects with both
steel pin with a cotton tip. The glass spheres were removed after measurement sites exposed, the measured velocities were analyzed
finishing the measurements. The signal level to the B-71 was and compared. For all four stimulation positions, the mean differ-
0.25 V rms and was fed from a signal analyzer (Agilent 35670A). ence between the promontory and the LSCC was close to 0 dB
The level 0.25 V rms was chosen since it was deemed to be suffi- (range: 0.1 dB to 0.3 dB) and the mean absolute difference was
ciently high to exceed the noise floor but still presented the sound below 1.7 dB. Together with the high correlation between results
at a level below the discomfort level. Thus the output level in dB HL from the two sites (r > 0.8, p < 0.001) they were deemed similar. As
was varying depending on the properties of the transducer at a consequence, data from the subjects with both sites measured
M. Eeg-Olofsson et al. / Hearing Research 306 (2013) 11e20 15

Fig. 2. The magnitude of the velocity of the otic capsule measured by the LDV at 1 N Fig. 4. The velocity magnitude of the otic capsule measured by the LDV at position B
stimulation at position A. The thin lines show the individual results from 16 subjects (standard position for BC audiometry). The stimulation level is recalculated to the
and the thick line shows the median result. reference equivalent threshold force level (RETFL) at 0 dB HL. For frequencies in-
between standard frequencies the data are interpolated. Included is also an arbitrary
velocity with a constant acceleration of the cochlea. Position B: solid line; constant
were calculated as the average from those sites, and used in the acceleration: dotted line.

analysis.
The vibration magnitude from 16 subjects as well as their me-
3.3. Velocity response at different positions
dian result is shown in Fig. 2 as the velocity response of the otic
capsule when the B71 transducer was at position A. All data are
In Fig. 3 the median absolute velocity responses from positions
recalculated to a stimulation level of 1 N. Even if all curves have
A, B, C and D are displayed. Below 1.0 kHz there is an anti-resonance
similar morphology, there are differences in the vibration magni-
around 0.4 kHz followed by a steep increase in velocity. From 1.0 to
tude amounting to about 4 times between the highest and lowest
2.0 kHz stimulation at position B gives the highest vibration ve-
magnitude. It should be noted that there is no overall best and
locity. Above 2.0 kHz, the velocity responses are similar for the
worst subject in terms of vibration magnitude but the high and low
stimulation positions. In Fig. 4 the vibration velocity response of the
results differ among the subjects at the different frequencies. There
otic capsule is shown when the stimulation is at position B. Here,
are indications of both resonances and anti-resonances in the re-
the stimulation is recalculated to 0 dB HL, i.e. the threshold level for
sponses, but no general similarity of their appearances among the
normal hearing subjects. Reference force levels are taken from ISO
curves is apparent. The term “anti-resonance” is here used to
389-3 (1994) and levels at frequencies not included in the standard
denote sharp minima in the measured response.
were interpolated. When shown in this way, there is a general
decrease in the vibration level with frequency. Also included in the
figure is an arbitrary dotted line with a slope of 20 dB/decade. As
can be seen, the slope of the dotted line follows approximately the
slope of the cochlear vibration response at frequencies between
0.4 kHz and 4.0 kHz. The dotted line corresponds to a constant
acceleration level, and it can be concluded that at this frequency
range, normal hearing thresholds are obtained at the same cochlear
acceleration level.
In Fig. 5 the velocity responses from position B, C and D in
relation to position A are displayed. The response functions are
recalculated from the initial 1/64 octave resolution to 1/3 octave
resolution for two reasons. First, the primary aim of this study was
to compare the vibration of the otic capsule with perceptual data,
and the tone thresholds were obtained at a resolution of 1/3 octave.
Second, the statistical analyses was based on 1/3 octave resolution
to make the result meaningful. Looking at the median data for all
subjects there are large response differences for the stimulation
positions in the frequency range 0.3 kHze2.0 kHz. Above 2.0 kHz
the different positions give a similar velocity response with only
minor differences.

3.4. Tone thresholds at different positions


Fig. 3. The magnitude of the velocity of the otic capsule measured by the LDV at 1 N
stimulation. The results are presented as the median result of positions AeD from 16
subjects. Position A: solid line; position B: dashed line; position C: dashed-dotted line; All results of the threshold measurements with BC stimulation
position D: dotted line. at the four positions are from the second session. The result from
16 M. Eeg-Olofsson et al. / Hearing Research 306 (2013) 11e20

Fig. 6. BC tone audiometry at 16 frequencies with a 1/3 octave frequency resolution.


The results are presented as the median threshold from positions B, C, D relative to
Fig. 5. The median velocity level of the otic capsule at positions B, C, D relative to
position A. A positive value indicates better (lower) threshold at the position compared
position A with a 1/3 octave frequency resolution. Position B re A: solid line; position C
with position A. The threshold difference is given on the left y-axis with thick lines
re A: dashed line; position D re A: dotted line.
while the standard deviations of the estimates are presented on the right y-axis with
thin lines. Position B re A: solid line; position C re A: dashed line; position D re A: dotted
line.
the threshold measurements are presented as relative differences
in threshold level related to position A (Fig. 6). As displayed here, a
positive result means better sensitivity (lower threshold) at the and C in relation to position A: at 1.0e1.6 kHz for position B
position compared with position A. There is an overall trend of (p < 0.05) and at 0.315e1.0 kHz and 2.5 kHz for position C
better thresholds with stimulation closer to the cochlea (positions B (p < 0.05). No significant differences were found for stimulation at
and C). In more detail, position B gives 0e5 dB better thresholds position D in relation to position A. Significant threshold differ-
than position A except between 2.5 kHz and 5.0 kHz where they are ences between positions B, C and D in relation to position A were
similar or position A slightly better. Position C is up to 5 dB more found between 0.5e1.6 kHz and at 8.0 kHz for position B (p < 0.05),
sensitive at the higher frequencies but at the low frequencies, at 0.315, 0.4, 2.5, 3.15 and 8.0 kHz for position C (p < 0.05), and at
below 0.8 kHz, the thresholds are 5e10 dB worse than position A. 0.3e0.5, 0.8 and 1.25e2.0 kHz (p < 0.05) for position D. Moreover
Position D has overall 0e5 dB worse thresholds than position A. the correlation between the relative tone thresholds and the rela-
tive vibration results was low while Wilcoxon’s signed rank test
3.5. Correlation between tone thresholds and the velocity response only indicated a statistical significant difference below 0.8 kHz for
of the otic capsule positions B, C and D, and at one additional frequency at 2.0 kHz for
position D.
LDV data are compared with tone thresholds from session two.
The median data for the LDV and the hearing thresholds are dis- 4. Discussion
played in Fig. 7aec. There are general similarities between the LDV
and threshold data, but also differences. The largest differences are 4.1. Laser Doppler vibrometry measurements
found at the lowest frequencies for all positions, but general
agreement is seen at frequencies above 0.8e1.0 kHz. Laser Doppler vibrometry has been reported in measurements
of cochlear vibration in cadavers and dry skulls. The rationale for
3.6. Comparison of the two tone audiogram sessions those studies, e.g. (Eeg-Olofsson et al., 2008, 2011; Håkansson et al.,
2008; Håkansson et al., 2010; Stenfelt and Goode, 2005b; Stenfelt
The two separate tone audiograms were executed with an in- et al., 2000) is that the vibration of the cochlea is correlated to a
terval of 2e5 months. Data from the first audiogram session are not hearing perception. To our knowledge, this is the first time that
presented in the current article. When comparing the two sessions vibration measurements of the otic capsule during BC stimulation
there was an overall higher threshold level in the second session, of live humans are reported. This is also the first time these vi-
most likely due to the change of masking procedure. In session one, brations are compared to hearing thresholds in the same
12% of the results were disregarded in the analysis due to hearing individual.
the tone in the wrong ear or that the tone was heard in the middle To ensure quality of the data, a restrictive SNR of better than
of the head. In session two, this percentage was 1%. 10 dB was used for the measurements. According to that restriction,
data are presented in the frequency range 0.3e5.0 kHz where the
3.7. Statistical analysis measurements gave results above this SNR limit. The problem with
the stimulation levels and low SNRs in the measurements are
The high correlation between the vibration results of the inherent to the B-71 transducer and the transducereskull interface.
promontory and the LSCC was described previously. However, At low frequencies, the skull impedance is high, which reduces the
there were large individual differences in the relative vibration vibration stimulation from the transducer, and an increase of
response and tone thresholds for the stimulation positions. Wil- stimulation level (higher input to the transducer) would result in
coxon’s signed rank test showed significant differences of the ve- large amount of distortion from the transducer itself, which is not
locity response at the otic capsule from stimulation at positions B acceptable. At the high frequencies, it is primarily a resonance in
M. Eeg-Olofsson et al. / Hearing Research 306 (2013) 11e20 17

Fig. 7. Sensitivity difference between positions in dB for the cochlear velocity and the
Fig. 8. The relative level of the cochlea measured by the LDV in the current study from
tone threshold results. The data are displayed as the median velocity and threshold
the positions B, C, D relative to position A, compared with published cadaver data.
result from positions B (graph a), C (graph b), D (graph c) relative to position A. The
Position B (graph a), position C (graph b) and position D (graph c) relative to position A.
results are presented so that a positive value indicates improved sensitivity. Tone
Present study: solid line; Eeg-Olofsson et al., 2008 or 2011: dashed line.
thresholds: solid line; velocity: dashed line.
18 M. Eeg-Olofsson et al. / Hearing Research 306 (2013) 11e20

the transducer design at around 4 kHz that results in reduced resonances) are similar in the cadaver head and the live human
stimulation level above this resonance frequency. Once again, skull, but differ significantly to the dry skull. Another difference is
higher stimulation levels might produce non-linear distortion as that the current study only included subjects with a middle ear
well as being perceived as too loud for the test subjects with near- common cavity. In Eeg-Olofsson et al. (2008) the mastoids were
normal cochlear function. intact for the stimulation positions discussed here. Position B is
Another issue is the use of glass sphere reflectors to enhance the approximately 3.1 cm from the ear canal opening. This is on the
backscatter of the laser beam. Similar glass spheres were used in border of, or most likely, just outside the mastoid surface area that
previous studies with valid results (Eeg-Olofsson et al., 2008, 2011; attaches to the petrous part of the temporal bone (MAPP) (Eeg-
Stenfelt and Goode, 2005b; Stenfelt et al., 2002). In this study the Olofsson et al., 2008). Within the MAPP-area, an increase in vi-
same method was used but the glass spheres were larger in bration transmission to the ipsilateral cochlea was noted in Eeg-
diameter. The promontory and the LSCC are closely situated in the Olofsson et al. (2008). An intact mastoid might have an important
same bony structure and thus the velocity response from BC influence on vibration transmission from the skull to the cochlea.
stimulation is expected to be similar using glass sphere reflectors. When the velocity data with stimulation at position B were
Since the velocity responses from the promontory and the LSCC are related to normal hearing thresholds (RETFL, Fig. 4) the response
highly correlated, and the transfer function of vibrations in the skull was similar to a constant acceleration at frequencies between 0.4
is assumed to be linear (Flottorp and Solberg, 1976; Håkansson and 4 kHz. This analysis is slightly outside the topic for the current
et al., 1996; Smith and Suggs, 1976) the vibration measured at the study, but the interesting finding is worth mentioning. The con-
otic capsule is suggested to be valid. stant acceleration implies that the mass of the cochlear interior, the
When the current results are compared with the velocity re- cochlear fluids, are affected by a constant force due to inertial ef-
sponses from previous studies (Eeg-Olofsson et al., 2008, 2011) the fects (inertial forces). It has been proposed that the cochlear
current responses differ from previous data. One difference is that response during BC excitation at frequencies below 4 kHz is
the stimulation is through the skin in this study while previous dominated by fluid inertia (Stenfelt and Goode, 2005b). Even if the
studies used a direct coupling to the skull. That can, at least partly, current result is not an irrefutable evidence for fluid inertia being
explain the 5e10 dB lower results at the higher frequencies in the an important contributor to BC hearing, it is a strong indication of
current study, that are in line with previous estimates (Håkansson its importance.
et al., 1984, 1985; Stenfelt and Håkansson, 1999). It is also clear that
the dry skull data (Stenfelt et al., 2000) is dissimilar indicating that 4.2. Tone audiometry results
a dry skull is not a good model for estimating cochlear response
during BC stimulation. However, there is a general agreement be- It should be noted that the threshold estimation is not done
tween cadavers’ and live humans’ cochlear response suggesting according to normal standard procedure in several aspects. Hearing
that preserved human cadaver heads can be used to estimate skull thresholds were tested at 16 frequencies at all four positions on the
vibrations during BC stimulation. The caveat is that the current head. Further, the level resolution to obtain the thresholds was
study measured the vibration on the skin covering the otic capsule 2 dB. The masking procedure was also different from the standard.
and not directly at the bone as in the other studies. However, if the These differences may alter the thresholds compared to normal
difference is due to the skin at the stimulation site alone, or is also clinical routine. However, the focus was on the relative threshold
affected by the skin covering the otic capsule in the current study is between stimulation positions, not the actual threshold per se. Even
impossible to determine. Consequently, even if the skin at the otic if the resolution of 2 dB do not enhance the accuracy in terms of the
capsule may have affected the current results, its effect is deemed variance between tests (Jerlvall and Arlinger, 1986), it facilitates
small. higher precision in the comparisons with the laser results, espe-
The velocity response of positions B, C and D in relation to po- cially at the individual level.
sition A for the current study and Eeg-Olofsson et al. (2008, 2011) Several factors add to the uncertainty in psychoacoustic testing.
are illustrated in Fig. 8aec. Even if the overall patterns are similar The approximate duration for the threshold measurements was 1 h
there are minor differences, especially for position C. In the Eeg- and 20 min including a 10 min pause. Fatigue can influence the
Olofsson et al. (2008) study, the velocity response differences at results. To minimize the effect of fatigue the test was balanced
the higher frequencies was 5e15 dB for position C relative to po- between positions. Another issue is the masking noise that could
sition A. This large difference is not found in the current study. The rise to high values, especially if the non-test ear had a hearing loss,
difference in stimulation method, through the skin here and or if the sound transmission to the test ear was low. High masking
directly to the bone in Eeg-Olofsson et al. (2008) does not explain levels lead to a higher degree of central masking, and can also cause
the difference seen as the data are relative measures. The root of the masking noise to be transmitted by means of BC to the test ear.
zygomatic bone has a sharp lateral angle which can give difficulties However, since a fixed masking level procedure was used, the same
when trying to get a stable and medially directed stimulation force masking level was used for all four positions and the relative
for the transducer when applied on the skin. On the cadavers, the measures are valid.
transducereskull interface was through a rigid titanium screw The transcranial attenuation (TA) is a measure that has a clinical
where both the stability and the direction of the stimulation force interest for masking in BC hearing assessment and also for reha-
were controlled. The method inequality and the fact that position C bilitation in single sided deafness. Another important aspect is the
in the cadavers was positioned slightly closer to the ear canal, could fact that BC sound stimulates both cochleae which has implications
explain the velocity response difference between cadavers and live for binaural hearing with bone conduction hearing devices. The
humans seen at position C. results from earlier studies (Hurley and Berger, 1970; Nolan and
Many authors have described a damping effect of BC vibration in Lyon, 1981; Snyder, 1973) show 0e15 dB TA in the frequency
a live human skull (Franke, 1956; Gurdjian et al., 1970; Håkansson range 0.25e4 kHz with large individual differences. A recent study
et al., 1986; Khalil, 1979). These comparisons were made to dry (Stenfelt, 2012) reported that the average TA in a group of in-
skulls but the difference between a human cadaver skull and a live dividuals with single sided deafness was close to 2.5 dB comparing
human skull is not described. The data from the current study the corresponding positions A and D in the current study. In the
compared with previous cadaver head studies indicate that the same study, the TA was on average 5.0 dB when measured between
damping of BC sound in the human skull (e.g. damping of skull positions B on both sides of the skull. It was also concluded that the
M. Eeg-Olofsson et al. / Hearing Research 306 (2013) 11e20 19

can lead to large threshold alteration (Khanna et al., 1976; von


Békésy, 1960). As recently shown in unilateral deaf subjects, a
change in stimulation position between corresponding positions A
and B could give BC sensitivity differences of 20 dB or more
(Stenfelt, 2012). Such large changes are also found in the vibration
data for stimulation at adjacent positions. One explanation here is
that the multiple pathways and the vibration of the cochlea in
different directions add constructively or destructively resulting in
large differences both for the cochlear vibration and the hearing
perception (Stenfelt and Goode, 2005b). Also, even if the first
author placed the transducer in both the perceptual and vibration
measurements, the exact same position was difficult to reproduce.
This slight misplacement add to the variance and affects the cor-
relation between perceptual and vibration measures. These varia-
tions, together with the uncertainty associated with threshold
estimations, prevent a significant correlation when investigating
individual subjects. However, when the data are averaged over the
whole group, similarities between perceptual measures and vi-
bration measures are seen, indicating that the cochlear vibration
Fig. 9. The relative difference between tone thresholds and cochlear vibration when serves as a good indicator of the perceived BC response for the
the stimulation is at positions B, C, and D relative to position A. The data are arranged
group, but does a poor job of predicting BC response in an
so that a positive value indicates greater increase in vibration data compared with the
threshold data. The median relative difference is given on the left y-axis while the individual.
standard deviations of the differences are presented on the right axis. Position B re A: According to previous studies (Stenfelt and Goode, 2005b;
solid line; position C re A: dashed line; position D re A: dotted line. Stenfelt et al., 2000) the x-direction (medial-lateral direction) is
the most important direction for measurement of BC stimulation at
the cochlea. This notion relies on findings that either the x-direc-
average threshold improvement comparing positions B and A was tion dominates the response (at low frequencies when the stimu-
2.5 dB. The latter meaning that the difference in TA between po- lation direction coincides with the x-direction) or is at a similar
sitions A and B emanates from the relative thresholds at the ipsi- level as the other directions (primarily at high frequencies) (Stenfelt
lateral side. The results from Stenfelt (2012) are similar to this study and Goode, 2005b). Consequently, an increased vibration in the x-
indicating limited threshold differences between positions and direction implies the same increase of the basilar membrane vi-
large spread between individuals. bration. Also, relative threshold measures of the transcranial
transmission indicated good correspondence between perceptual
4.3. Correlation between tone audiometry and velocity response of and x-direction measures (Stenfelt, 2012). However, that study
the otic capsule indicated that estimating the vibration response from all three di-
mensions was better than the x-direction alone. The caveat is that
One of the aims in this study was to investigate the correlation the Stenfelt (2012) study compared vibration measurements in
of the velocity of the otic capsule during BC stimulation to hearing cadaver heads and threshold measurements in a different group of
thresholds. If the vibration of the otic capsule mimics that of subjects; the current study compare thresholds and cochlear vi-
threshold measurements, vibration measurements can be used for bration in the same subjects.
estimating the BC perception in humans. When investigating Fig. 2 Another support of the x-direction importance for hearing
it is clear that there are intersubject differences in the vibration perception of BC sounds is found in individuals with middle ear
response of the otic capsule for the same BC stimulation position lesions. These are more affected when BC stimulation is on the
that should be reflected in the individuals BC perceptual data. mastoid than on the forehead (Goodhill et al., 1970; Studebaker,
However, since the subjects’ test ear was a middle ear common 1962). The above made comparison indicates that the middle ear
cavity, thus deviating from the standards according to ISO 8253-1, it is also sensitive to the vibration direction (Stenfelt et al., 2002).
is not possible to know the exact sensorineural component of the Further the level of influence of the CSF pathway during BC
ears. No comparison of absolute vibration as measured with the sound stimulation is not yet understood. In this perspective it is
LDV and thresholds was therefore made. difficult to draw any conclusions from the LDV measurements at the
A way to compare the vibration and perceptual data is to individual level. At the median level, it seems more promising but
examine the relative sensitivity difference between the different to get a statistical support, a larger material is needed. Even if the x-
positions. The hypothesis is that a lowering of thresholds (i.e. better direction is the most important vibration direction of the cochlea
sensitivity) is accompanied with higher vibration of equal level. All for BC hearing, it is a limitation to measure in only one direction. By
such comparisons are done between position A and the positions B, measuring the vibrations in multiple locations at one target site
C, and D. When the median thresholds change is compared with the (promontory or LSCC) a clearer picture of the three dimensional
median otic capsule vibration change, there are discrepancies at the motion of the otic capsule could be achieved, and give more in-
lowest frequencies (below 0.8e1.0 kHz), but at higher frequencies formation to understand the divergence between the individual
there is a general correspondence of the curves (Fig. 7). However, LDV and tone threshold results.
when the threshold change is compared with the associated vi-
bration change of the otic capsule in the individual subject, there is 4.4. Clinical implications
low correspondence (low correlation) between the results. The
median result and standard deviation (Fig. 9) illustrates the low Results from the current study support findings from previous
individual correspondence. This finding can, at least partly, be studies on vibration of the otic capsule. By stimulating with a bone
explained by the large variance of tone threshold measurements. conduction device closer to the cochlea than the standard BAHA
For example, a small change in stimulation position on the mastoid position, sound transmission improves to the ipsilateral cochlea.
20 M. Eeg-Olofsson et al. / Hearing Research 306 (2013) 11e20

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