Round window membrane motion with air conduction and bone conduction stimulation

Hearing Research 198 (2004) 10–24 www.elsevier.com/locate/heares

Round window membrane motion with air conduction and bone conduction stimulation Stefan Stenfelt

a,b,*

, Naohito Hato b, Richard L. Goode

b

a

b

Department of Signals and Systems, Chalmers University of Technology, SE-41296 Go¨teborg, Sweden Division of Otolaryngology-Head and Neck Surgery, Stanford University Medical Center, Stanford, CA, USA Received 12 August 2003; accepted 6 July 2004 Available online 11 September 2004

Abstract The vibration patterns of the round window (RW) membrane in human cadaver temporal bone specimens were assessed by measurements of the velocity of reflective targets placed on the RW membrane with an approximate spacing of 0.2 mm. The velocity was measured in the frequency range 0.1–10 kHz by a laser Doppler vibrometer in four specimens with air conduction (AC) stimulation and in four specimens with bone conduction (BC) stimulation. The response pattern was investigated by analyzing the velocity response of all targets on the RW membrane, by making iso-amplitude and iso-phase contour plots of the membrane surface, and by creating animations of the surface vibration at several frequencies. Similar response pattern was found with AC and BC stimulations. At frequencies below 1.5 kHz, the RW membrane vibrates nearly as a whole in an in-and-out motion and above 1.5 kHz, the membrane moves primarily in two sections that vibrate with approximately 180
difference. Indication of some traveling wave motion of the RW membrane at those frequencies was also found. At higher frequencies, above 3 kHz, the membrane motion is complex with a mixture of modal and traveling wave motion. An increase of the stimulation level did not alter the vibration pattern; it only gave an increase of the RW membrane vibration amplitude corresponding to the increase in stimulation. When the mode of stimulation at the oval window was altered, by the insertion of a 0.6 mm piston, the vibration pattern of the RW membrane changed.  2004 Elsevier B.V. All rights reserved. Keywords: Round window; Vibration pattern; Air conduction; Bone conduction; Middle ear reconstruction

1. Introduction A sound stimulation by air conduction (AC) enters the ear canal as a sound pressure, is converted to a vibration of the middle ear ossicles by the tympanic membrane (TM), and is converted to a sound pressure and corresponding motion in the cochlear fluid by the mo-

Abbreviations: AC, air conduction; BC, bone conduction; LDV, laser Doppler vibrometer; OW, oval window; RW, round window; TM, tympanic membrane * Corresponding author. Tel.: +46 31 772 1770; fax: +46 31 772 1782. E-mail address: [email protected] (S. Stenfelt). 0378-5955/$ - see front matter  2004 Elsevier B.V. All rights reserved. doi:10.1016/j.heares.2004.07.008

tion of the stapes footplate. This motion of the stapes footplate, or the oval window (OW), is reflected at the round window (RW) since at least for the low frequencies, the fluid volume displacement at the OW equals that at the RW but with opposite phase (Kringlebotn, 1995; Stenfelt et al., 2004). Further, the vibration of the stapes footplate and the amount of fluid displaced is a measure of the input to the cochlea (Puria et al., 1997). Hence, if the fluid flow at the RW equals that at the OW, the fluid flow at the RW can be used as an estimate of the stimulation of the cochlea. This could be interesting in cases where the actual stimulation of the cochlea is difficult to predict, e.g. when a middle ear ossicular prosthesis is inserted and transmits the

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vibration energy to the cochlea instead of the footplate. In such case, the stimulation mode is altered which can be difficult to verify by measurements at the OW; a measurement of fluid flow at the RW could determine the amount of stimulation at the OW. The volume flow at the RW can be obtained by applying a tube to the RW and measure the sound pressure in the tube (Kringlebotn, 1995), or by applying a sound pressure in the tube; when this sound pressure equals the sound pressure in the cochlear fluid a cancellation of the perceived sound is achieved (Be´ke´sy, 1948). These procedures have shown difficult and it would therefore be easier to estimate the volume displacement by the velocity of a single position of the RW membrane, e.g. at the center. This velocity could easily be obtained by a laser Doppler vibrometer (LDV). However, Khanna and Tonndorf (1971) by means of time-average holography found, when investigating the vibration pattern of the RW membrane in cats, the vibration pattern complex at as low frequencies as 125 Hz, where the RW window membrane appears to vibrate in several separate sections. A similar tendency was reported by Nomura (1984), who also measured the RW membrane pattern in cats by time-averaged holography. Another approach to estimate the effect of an alteration of the middle ear is to measure the relative change in the RW membrane motion. In this case the motion of the RW is measured at one (or several) position(s) of the RW membrane before the alteration (e.g. insertion of a prosthesis), and the same position(s) is remeasured afterwards. Provided the vibration pattern of the RW membrane is equal before and after the alteration procedure, the change in RW membrane motion gives an estimate of the change in stimulation level of the cochlea, caused by the procedure. In both the investigation by Khanna and Tonndorf (1971) and Nomura (1984), the vibration pattern of the RW membrane did not alter with a change of stimulation level. However, there were no reports of other stimulation alterations. When a vibration is applied to the skull, the ear is stimulated by bone conducted (BC) sound. In this case, several physical phenomena contribute to the stimulation of the inner ear such as sound radiated into the external ear canal that is subsequently transmitted to the cochlea, inertial (mass) effects of the middle ear ossicles and the cochlear fluid itself, as well as compression of the cochlear bone (Tonndorf, 1972). Since removal of the external ear and middle ear components only lead to a slight reduction of BC hearing, the effects of the inner ear, i.e. cochlear fluid inertia and compression of the cochlear bone, are the main contributors to the perceived BC sound. It has been shown that a BC sound influences the traveling wave on the basilar membrane in a similar way as with AC stimulation (Be´ke´sy, 1932, 1955; Wever and Lawrence, 1954; Khanna et al., 1976; Stenfelt et al.,

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2003). However, the stimulation mode of BC can be very different from AC stimulation, e.g. compression and expansion of the cochlear bone with BC stimulation and vibration of the stapes footplate in the OW with AC stimulation. Further, with BC stimulation, the fluid volume displacement at the OW and RW differs (Stenfelt et al., 2004). As a result of this stimulation difference, the vibration modes of the RW membrane can depend on the stimulation mode, i.e. AC or BC. Therefore, the vibration pattern of the human RW membrane will be investigated with both AC and BC stimulations. The aim of the study is to address the following questions:
What is the vibration pattern of the human RW membrane when stimulation is by AC?
Does the RW membrane vibration pattern change with stimulation level?
Is the RW membrane vibration pattern dependent on the stimulation (e.g. normal middle ear vs reconstructed middle ear)?
Is the vibration pattern of the human RW membrane similar for AC and BC sound?

2. Materials and methods 2.1. Temporal bone specimens In this investigation, 8 human temporal bones were studied (6 males and 2 females) with an average age of 71.0 and a range of 63–76 years. The temporal bones were extracted from human cadavers within 48 h of death using a Schuknecht bone saw at the time of autopsy. The temporal bone specimens were wrapped in gauze, placed in a 1:10000 merthiolate solution in normal saline and stored at 5
C. All measurements on individual bones were conducted on the same day within 6 days of death. The TM and middle ear were inspected in each bone using an operating microscope; bones with abnormal TMs or middle ears were excluded from the investigation. The temporal bones for AC and BC testings were prepared differently. A detailed description of the preparation of the temporal bones for AC stimulation is described in Hato et al. (2001) and for BC stimulation in Stenfelt et al. (2002). In what follows, a short description of the preparation process is presented. For the specimens investigated with AC stimulation, the attached connective tissue was removed and the bony wall of the external ear canal was drilled down to 2 mm from the tympanic annulus. A simple mastoidectomy (opening the mastoid antrum and removal of the mastoid air cells) and posterior hypotympanotomy (widely opening of the facial recess) were performed, including

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removal of the mastoid portion of the facial nerve and surrounding bone. In order to achieve a good view of the RW membrane, the RW niche had to be slightly widened. The ossicular ligaments, chorda tympani, tensor tympani and stapedius muscle were left intact. A 25 mm long plastic artificial external ear canal of 8.5 mm internal diameter was placed against the bony ear canal remnant; it was placed so the axis of the tube was approximately perpendicular to the annulus of the TM. The temporal bone was then put in a latex seal and covered with dental cement. This reduced the drying of the temporal bones during the measurement time. A similar approach was used with the temporal bone preparations tested with BC sound. Without damaging the ossicular, tympanic or vestibular structures, a slightly greater opening in the facial recess was made to obtain a perpendicular view of the RW membrane. This procedure was necessary in order to achieve reliable data when measuring the RW membrane motion with BC stimulation. A small connector with threaded ends was attached to a tapped hole in the temporal bone specimen close to the internal acoustic meatus, and glued with cyanoacrylate glue (Garf Reef glueTM, Garf Inc, Boise, ID). This connector was later connected to the B&K type 4810 mini-shaker (Bru¨el and Kjaer, Naerum, Denmark) and ensured rigid connection between the specimen and the mini-shaker. The connector was aligned so the motion of the temporal bone specimen was in line with the low-frequency in-and-out motion of the stapes footplate. To achieve good reflection of the laser beam, small reflective glass micro-spheres of about 5 lm in diameter were positioned at the measurement points. The positioning of these micro-spheres was similar for the AC and BC measurements. A matrix of micro-spheres was placed on the RW membrane with approximately 0.2 mm between the micro-spheres (Fig. 1). Depending on the size of the RW, somewhere between 28 and 40 equally spaced micro-spheres were placed on the RW membrane. When BC stimulation was used, additional micro-spheres were placed on the promontory bone close to the RW to measure the bone velocity perpendicular to the RW membrane. Afterwards, a calibrated photograph was taken of the RW that clearly showed the micro-sphere positions and the edges of the RW membrane. The coordinates of the micro-spheres were stored and later used for the calculation of RW membrane vibration pattern. The picture was also used to calculate the area of the RW membrane. 2.2. Measurement system The stimulations, either as a sound pressure in the artificial ear canal or a vibration of the temporal bone specimen, were provided by a PC based software, SYSid 6.5 (www.sysid-labs.com), using a DSP-16+ sig-

Fig. 1. Photo of a RW with 32 reflective targets on the membrane used for estimation of the membrane vibration pattern with AC stimulation. The RW niche was widened during the preparation to give a full view of the entire RW membrane.

nal processing card. The measurement system is shown in Fig. 2. The output from the computer was fed through a power amplifier (D-75, Crown, Elkhart, IN) and, in the case of AC stimulation, to a receiver in the artificial ear canal (Tibbets 83-13A/024, Tibbets Industries, Camden, ME). With BC stimulation, the output from the power amplifier was fed to a B&K type 4810 mini-shaker. The mini-shaker was rigidly coupled to the temporal bone by a threaded connector. The vibrations, either of the RW membrane or the promontory bone, were measured with a LDV, the HLV-1000 (Polytec, Waldbronn, Germany). The sensor head was mounted with a joystick-controlled mirror on an operating microscope enabling easy control of the laser beam. The ear canal sound pressure was measured with a probe tube microphone (ER-7C, Etymotic Research, Elk Grove Village, IL) positioned 2 mm from the TM in the artificial ear canal. First, with AC stimulation, the normal middle ear transfer function of the temporal bone (malleus umbo to stapes footplate) was measured to verify the specimen to be within normal limits. Then the vibrations of the targets on the RW membrane were measured consecutively. The whole measurement process lasted about half an hour. The results of the measurements were stored for later computation of the RW membrane motion pattern. Using AC stimulation, the angle when measuring on the RW membrane was about 30
; this was compensated for when calculating the displacement; the results were converted to a motion perpendicular to the RW membrane.

S. Stenfelt et al. / Hearing Research 198 (2004) 10–24

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Laser head HLV 1000 Earphone Laser beam

ER 7C Probe microphone Crown D-75

Bone specimen B&K 4810

Fig. 2. The setup for the measurements of RW membrane vibration. When AC stimulation was used, the amplified computer generated stimulation was supplied to the earphone giving a sound stimulation in the artificial ear-canal. The stimulation at the TM was measured by the Etymotic Research ER 7C probe microphone. The laser head of the Polytec HLV 1000 laser Doppler vibrometer was attached to an operating microscope and the laser beam measuring the vibration of the targets on the RW membrane was controlled by a joystick manipulator. When BC stimulation was used, the amplified computer generated stimulation was supplied to the Bru¨el & Kjaer type 4810 mini-shaker that was rigidly coupled to the specimen. The laser Doppler vibrometer measured the velocity of the targets on the RW membrane as well as the velocity of the targets positioned on the cochlear promontory.

The procedure was similar when stimulation was by BC. The exception was that the laser was aimed perpendicular to the surface of the RW membrane. This precaution minimized the influence from motion in other directions than perpendicular to the RW membrane surface. Therefore, no correction for misalignment had to be done for the RW membrane measurements with BC stimulation. Further, the velocity of the promontory bone close to the RW was measured in a direction perpendicular to the RW membrane. The promontory bone velocity was used as reference when the differential vibration between the RW membrane and the promontory bone was calculated. The measurement time for the RW membrane and promontory bone measurements with BC stimulation was also about half an hour. 2.3. Calibration To limit high frequency noise or overloading by low frequency vibrations, the filters of the HLV-1000 are used. The lowpass filter cutoff frequency was set at 15 kHz and the highpass filter cutoff frequency at 100 Hz. These settings affected the frequency response of the HLV-1000 and it was calibrated against a B&K type 4371 accelerometer. Below 10 kHz this accelerometer has, according to the manufacturer, a maximum level deviation of 0.2 dB and a maximum phase deviation of 5
. The accelerometer was mounted on the B&K 4810 mini-shaker and the laser aimed on the surface of the accelerometer in a line perpendicular to the accelerometer surface. This was used for calibration of the HLV-1000 for the frequency range 0.1–10 kHz (50 frequencies/decade). The ER-7C probe tube microphone

was calibrated against a B&K type 4138 1/8 inch microphone. The sensitivity of the B&K microphone was first determined in a B&K type 4230 sound level calibrator. Both microphones were then placed 1 mm apart in a small cavity, a sound introduced and the calibration curve of the ER-7C obtained for the frequency range 0.1–10 kHz (50 frequencies/decade). 2.4. Calculation of AC and BC response With BC stimulation, the important parameter to measure was the relative vibration of the RW membrane, i.e. the velocity difference between the RW membrane and the surrounding bone. This was obtained by calculating the difference between the RW membrane velocity and the velocity of the promontory bone close to the RW according to: vBC;RW ¼ vRW  vPromontory;RW :

ð1Þ

These velocities were obtained in a line perpendicular to the RW membrane. However, the vibration direction of the temporal bone specimen was in a line perpendicular to the stapes footplate. This vibration was also measured and defined as the stimulation velocity level. A difference between the AC and BC measurements was that the promontory bone velocity in the stimulation direction was used as input reference for BC stimulation whereas the sound pressure at the TM was used as the input reference for the AC measurements. The results with AC stimulation are presented at a stimulation level in front of the TM of 80 dB SPL. The sound pressure at the TM was measured with a probe microphone and the real stimulation level was

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between 80 and 95 dB SPL for the frequency range used: the result was then calculated for a sound pressure level at the TM of 80 dB SPL, assuming linearity. The BC results were calculated in a similar way: the stimulation velocity of the cochlear promontory was measured using the LDV and the result calculated for a stimulation velocity of 1 mm/s, assuming linearity. However, the stimulation velocity could not be measured with the laser beam in the stimulation direction but at an angle of approximately 30
. This angle was measured by a protractor placed on the mini-shaker. With BC stimulation of the specimens, the velocity ratio between the stimulation axis and the orthogonal plane is 15–20 dB (Stenfelt et al., 2002). Therefore, the BC stimulation level was calculated as the velocity of the promontory bone close to the RW measured by the LDV, and corrected for the angle between the measurement and stimulation direction. 2.5. Error analysis The vibration pattern of the RW membrane was obtained by non-uniform spatial sampling. This means that the distances between the targets on the RW membrane were not exactly equal. Instead, the two-dimensional position of each target was determined in a calibrated picture of the RW. In the same picture, the boarders of the RW membrane were determined. Using these target data, a grid of the RW membrane was created and the velocity data were interpolated on this grid by the MATLAB function griddata. 1 This function interpolates the non-uniformly spaced data to a predefined grid. Even if this interpolation would be perfect, there are still sources for errors. The two most serious are aliasing due to too large spatial distances between the targets and the uncertainties in the determination of the target positions (±5 lm). The uncertainty in determining the exact target position does not cause large errors in calculating the RW membrane vibration pattern provided the spatial vibration distribution is smooth. This is true at the lower frequencies where the RW membrane moves in a simple in-and-out pattern (below 1.5 kHz). At higher frequencies, the membrane breaks up in several modes in a complex vibration pattern. However, the targets on the RW membrane are close enough to fulfill the Nyquist two-dimensional sampling theorem for the frequencies used here. This was verified by examining the two-dimensional Fourier transform of the targets velocity on the RWmembrane. Consequently, aliasing is not expected to cause errors in the calculation of the RW membrane vibration pattern.

1 For more information of the function griddata, see www.mathworks.com.

Since the measurements are done in a consecutive order it is important that the same stimulation and response is obtained each time. Therefore, during each measurement session, only the laser beam was allowed to be moved in order to measure the vibration of all targets on and close to the RW membrane. If anything else was changed, that whole measurement session was remeasured. With that precaution, the consecutive testretest difference was less than 1 dB and 7
with AC stimulation and less than 0.2 dB and 4
with BC stimulation. This uncertainty in the measured data can give greater errors in the results with BC stimulation if the RW membrane velocity is close to the promontory bone velocity in both amplitude and phase: cancellation errors may occur. However, in a study measuring the fluid flow at the RW using similar measurement technique as here, the data obtained with BC stimulation was found valid for frequencies above 0.3 kHz (Stenfelt et al., 2004). Moreover, after all positions on the RW were measured, the first position measured on the RW membrane was remeasured. That measurement was within 1 dB and 10
of the first measurement, with AC as well as BC stimulation. The angle between the orientation of the OW and the RW is approximately 60
. This means that the angle between the vibration direction of the specimen using BC stimulation and the direction of the laser beam is also approximately 60
. At 0.1 kHz and with BC stimulation, the vibration peak amplitude of the specimen is about 20 mm/s; this vibration level decreases at 6 dB/octave. The peak displacement of the specimen perpendicular to the laser beam is 27 lm at 0.1 kHz whereas the target diameter is 5 lm. Consequently, at 0.1 kHz, the reflective target moves across the laser beam causing demodulation problems in the LDV. At 0.3 kHz, the displacement of the specimen perpendicular to the laser beam is of the same size as the reflective target. This gives a low-frequency limit of the result with BC stimulation of 0.3 kHz. The noise of the measurement system was assessed by measuring the response without any stimulation present. That response was compared with the results obtained with AC and BC stimulations. When stimulation is by AC, the signal-to-noise ratio (SNR) is better than 10 dB between 0.1 and 0.2 kHz, better than 20 dB between 0.2 and 0.4 kHz, better than 40 dB between 0.4 and 5.0 kHz, and better than 20 dB for frequencies above 5.0 kHz. With BC stimulation, the SNR was better than 60 dB for frequencies up to 2.0 kHz and better than 40 dB for frequencies above 2.0 kHz. The noise during the measurements is displayed in Fig. 7(a). It should be noted that, since the BC response is calculated as the difference between two velocities (the RW membrane and the bone), the BC response is more sensitive to noise than the AC results.

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according to the following: at a certain frequency (1, 2.5, 6, or 10 kHz), the maximum velocity amplitude of the RW membrane is according to the iso-amplitude contour plot, and the phase relation between the positions on the RW membrane is according to the iso-phase contour plot. To obtain the vibration pattern of the RW membrane, the amplitude A and phase / from the isocontour plots should be combined according to:

3. Results 3.1. AC stimulation The vibration pattern of the RW membrane was obtained by velocity measurements at multiple positions on the RW membrane. The result of the velocity measurements at the points on the RW membrane of specimen AC1 is shown in Fig. 3 for a frequency range of 0.1–10 kHz. Here, the magnitude and phase of the velocity at 32 positions on the RW membrane is plotted for a sound pressure of 80 dB SPL at the TM. Although the magnitude differs greatly among the measured positions (5–10 times), a general trend of the magnitudes can be seen. At low frequencies, the velocities rises at approximately 6 dB/octave, resonates around 1.0 kHz, and falls off at about 6 dB/octave at the higher frequencies. The variation from the general trend is greatest at the high frequencies where several peaks and valleys can be found in the data from individual targets. The phases of the velocities on the RW membrane in Fig. 3(b) show a decaying phase. This decay originates primarily from the time delay between the sound pressure in front of the TM and the vibration of the RW membrane. Above 0.5 kHz, a spread in phases between the positions on the RW can be seen; this spread becomes greater at higher frequencies. This means that, for frequencies above 0.5 kHz, the vibration of the RW membrane is not in phase for the entire area. The result from the measurements of the RW membrane vibration in four temporal bone specimens with AC stimulation is displayed in Fig. 4. The vibration is presented as peak amplitude and relative phase when a sound pressure of 80 dB SPL is present at the eardrum. The results are shown in iso-amplitude and iso-phase contour plots for the frequencies 1, 2.5, 6, and 10 kHz. The phases in Fig. 4 are presented relative to the center of the RW membrane. The plot should be interpreted

vðx; yÞ ¼ Aðx; yÞ cos½2pft þ /ðx; yÞ;

ð2Þ

where v is the resulting velocity of the RW membrane in a direction perpendicular to the membrane, f is the frequency in Hertz, t is the time in seconds, and (x, y) is the coordinate on the RW membrane. At 1 kHz, the distance between each iso-amplitude contour is 0.025 mm/s, and at 2.5, 6, and 10 kHz, the distances between the iso-amplitude contours are 0.01, 0.0025, and 0.001 mm/s, respectively. The distance between the iso-phase contours is 30
; a solid line indicates positive phase relation whereas a dotted line indicates negative phase relation. The RW membrane vibration of the four temporal bones shown in Fig. 4 differs. The size and geometrical shape of the RWs are not equal but are here shown similar for visibility purposes; the membrane area of each RW is given in Fig. 4. The RW are shown with the superior part towards the top, the anterior part to the left, the posterior part to the right, and the inferior part towards the bottom. Some general agreement and tendencies from the four specimens can be seen. At the low frequencies (here represented by 1 kHz), the entire RW membrane vibrates almost in-phase with the maximum displacement close to the center slightly towards the antero-superior side (the side closest to the OW). This nearly in-phase motion with a single maximum was found in all specimens up to approximately 1.5 kHz, where the pattern of the RW membrane motion became complex. Between 1.5 and 3 kHz, the RW membrane

AC stimulation 0

(a) 2

10

10

Phase (kilodegrees)

Magnitude of the velocity of the targets on the RW membrane with 80 dB SPL at the TM (µm/s)

15

1

10

(b)

-0.2 -0.4 -0.6 -0.8 -1.0

0

-1.2 0.1

0.2 0.3

0.5 0.7 1

2

Frequency kHz

3

5

7

10

0.1

0.2 0.3

0.5 0.7 1

2

3

5

7

10

Frequency kHz

Fig. 3. Magnitude (a) and phase (b) of the velocity of 31 targets on the RW membrane when the sound pressure is 80 dB SPL at the TM. The result is from specimen AC1. The phase in (b) is relative to the sound pressure measured at the TM. The frequency resolution is 50 points/decade.

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AC2

AC1 Phase

Amplitude

AC4

AC3 Phase

Amplitude

Phase

Amplitude

Phase

10 kHz

0.001 mm/s (80 dB SPL)

6 kHz

0.0025 mm/s (80 dB SPL)

2.5 kHz

0.01 mm/s (80 dB SPL)

1 kHz

0.025 mm/s (80 dB SPL)

Amplitude

2

Area: 2.73 mm

2

Area: 2.19 mm

2

Area: 1.68 mm

2

Area: 1.77 mm

Fig. 4. The vibration pattern of the RW membrane in four specimens stimulated with an AC sound is displayed as iso-amplitude and iso-phase contours. The result is shown for four frequencies: 1, 2.5, 6, and 10 kHz. The specimens are stimulated with a sound pressure level of 80 dB SPL at the TM and the velocity equidistance between the iso-amplitude contours are 0.025 mm/s at 1 kHz, 0.01 mm/s at 2.5 kHz, 0.0025 mm/s at 6 kHz, and 0.001 mm/s at 10 kHz. For the phase plots, the iso-phase contour equidistance is 30
and is related to the center of the RW membrane. A negative phase relation is shown as a dotted line while a positive phase relation is indicated with a solid line.

motion can be approximated by the motion of two sections moving approximately 180 degrees out-of-phase. One of these sections was generally dominating in the frequency range 1.5–2.5 kHz; this difference became less at 2.5–3 kHz. Above 3 kHz and up to approximately 7 kHz the distribution of magnitude and phase of motion along the surface of the RW membrane is complicated with no consistent spatial pattern. Above 7 kHz, less distinct maximum of the membrane were seen and the entire membrane moved with similar magnitude. While some of the differences in the phase of the RW membrane motion near 2.5 kHz with positive and negative phases regularly ordered around a boundary suggest the presence of modal motions of the membrane, the presence of gradual, spatial variations in phase is suggestive of some traveling wave component moving across the surface of the RW membrane at all frequencies reported. Another way to visualize the RW membrane pattern is shown in Fig. 5. Here, a cycle of vibration at 1, 2.5, 6, and 10 kHz is shown as snapshots at eight equally spaced time intervals of a cycle. The data are taken from specimen AC2 and the vibration amplitude in Fig. 5 is greatly enhanced (approximately 105–107 times). The displacement amplitude is color-coded and the corresponding displacement is given in the color-bar left of the animations in Fig. 5. At 1 kHz the membrane moves primarily in an in-and-out manner, though there is a

hint of a traveling wave going from the anterior side towards the posterior rim (seen in the peak during 0/8T–3/ 8T). At 2.5 kHz the anterior and posterior halves of the membrane show motions that are largely out of phase of each other, consistent with nodal separation of motion. However, a tendency of a traveling wave from the anterior towards the posterior side can be found here as well. At 6 and 10 kHz the patterns of displacement are quite complicated with multiple maxima and minima, but again there are clear signs of wave travel, the small peak visible in the anterior–inferior quadrant at 1/8T with 6 kHz stimulation travels towards the superior–inferior rim in the succeeding segments. It should be noted that Fig. 5 shows the displacement of the RW membrane whereas Figs. 3 and 4 show the velocity data. The vibration pattern of the RW membrane was investigated when the input stimulation was changed. In two of the specimens the input sound was increased by 10 dB relative to the original input. When the RW motion was compensated for the input increase, the isocontour plots obtained before and after the stimulation increase were compared. No difference in either magnitude or phase patterns of the RW membrane could be found, only an overall magnitude increase corresponding to the increase in stimulation level. Hence, at least for stimulation levels in the range 80–110 dB SPL at the TM, the RW membrane vibration pattern is independent of the stimulation level.

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Fig. 5. The vibration pattern of the RW membrane in specimen AC2 is shown as eight snapshots of a period when the stimulation is by AC. The result is shown for the frequencies: 1, 2.5, 6, and 10 kHz. The displacement amplitudes are greatly enhanced (about 105–107 times) for visibility purposes. The displacements are color-coded and the bar left of the RW figures indicate the displacement range at each frequency.

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AC stimulation 0.4

(a)

(b) 0.3 0.2

0

Phase (kilodegrees)

Velocity level change after a piston was inserted at the OW (dB)

10

-10

-20

0.1 0 -0.1 -0.2 -0.3

-30 0.1

0.2 0.3

0.5 0.7 1

2

3

5

7

Frequency kHz

-0.4 10

0.1

0.2 0.3

0.5 0.7 1

2

3

5

7

10

Frequency kHz

Fig. 6. Level (a) and phase (b) change of the velocities of nine central targets (3 · 3 matrix) on the RW membrane after a piston was inserted at the OW. The stimulation before and after the piston insertion was a sound pressure at the TM with a level of 80 dB SPL.

In the other two specimens used with AC stimulation, the stapes footplate was glued into the promontory bone, the superstructure removed and a small hole drilled into the footplate. A 0.6 mm teflon piston was then attached to the lenticular process of the incus and inserted into the hole in the glued stapes footplate. The RW membrane motion was then remeasured with a sound stimulation in the ear canal. The results from the nine target positions closest to the center (3 · 3 matrix) are presented in Fig. 6 as relative measures from one of the specimens: target velocities with the piston inserted compared with an intact middle and inner ear. Below 1.5 kHz the level of the targets vibration differs but their corresponding phases are similar. This is the frequency range where the RW membrane vibration is an in-and-out motion. The ratios of the targets are almost constant with frequency, i.e. the RW membrane vibration pattern with the piston inserted does not change much with frequency for frequencies below 1.5 kHz. However, the vibration pattern of the RW membrane differs between before and after the insertion of the piston at these frequencies. For frequencies above 1.5 kHz the relative measures of the nine positions changes considerable. No correlation of the nine positions is found, either in the level or phase data. The other specimen with a piston inserted showed similar result as the one presented in Fig. 6: for frequencies below 1.5 kHz, a nearly frequency independent level difference at all positions was found and, above 1.5 kHz, no correlation of the magnitude and phase changes of the vibration at the positions could be seen. 3.2. BC stimulation When the RW membrane vibration was measured during BC stimulation, the whole specimen vibrated. In order to obtain the relative motion between the RW membrane and the surrounding bone, the absolute velocity at the positions on the RW membrane as well as

the velocity of the bone surrounding the RW was measured. Since the relative motion of the RW membrane is calculated as the difference between the velocity of the RW membrane and the bone, the result may suffer from inaccuracies if the two velocities are of similar magnitude and phase. The absolute magnitude of the velocity from some of the positions in specimen BC1 is shown in Fig. 7(a); Fig. 7(b) shows the phase between the RW membrane and the bone for the same positions. The positions shown are: the bone surrounding the RW, the center, the superior part (top), the anterior part (left side), the posterior part (right side), and the inferior part (bottom) of the RW membrane. The superior, anterior, posterior, and inferior positions are approximately 0.2 mm from the RW membrane edge. The noise magnitude during measurements is displayed in Fig. 7(a). It was measured as the response magnitude from the LDV when the laser beam was aimed at a reflecting target but without stimulation. It should be noted that the measurement direction is perpendicular to the RW membrane and approximately 60
from the stimulation direction. This means that the specimen velocity in the stimulation direction is about twice that of the bone velocity shown in Fig. 7(a). At frequencies below 0.3 kHz, the vibration amplitude and phase of the positions on the RW membrane are similar to the bone surrounding the RW. At these low frequencies, a small error in the velocity measurement can cause large inaccuracies in the estimated velocity difference between the RW membrane and the bone. Above 0.3 kHz, the amplitude and phase of the RW membrane vibration is different from the bone vibration, except for the inferior position. The inferior position follows the bone velocity, in amplitude as well as in phase, for the whole frequency range measured. This may indicate that this position is actually very close to, or even outside the boarder of the RW. The other positions show velocity differences between the RW membrane and bone large enough to exclude significant bias for

S. Stenfelt et al. / Hearing Research 198 (2004) 10–24

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10

0.1

(a)

Superior Center

Phase between targets on the RW membrane and bone (kilodegrees)

Velocity magnitude of targets on the RW membrane and promontory bone (mm/s)

BC stimulation 1

Posterior

0

10

Bone

-1

10

Inferior

-2

10

Anterior

Noise

10-3 10-4 0.1

0.2 0.3

0.5 0.7 1

2

3

5

7

Superior

-0.1 -0.2

Center Posterior

-0.3

Anterior

-0.4 -0.5 0.1

10

(b)

Inferior

0

0.2 0.3

Frequency kHz

0.5 0.7 1

2

3

5

7

10

Frequency kHz

Fig. 7. (a) Magnitude of the absolute velocity of the temporal bone specimen and RW membrane and (b) phase between the RW membrane and promontory bone close to the RW. Stimulation is by BC in specimen BC1. The velocity of the temporal bone is indicated with a solid line, the target at the center of the RW is indicated with a dashed line, the target at the superior part of the RW membrane is indicated with a long dashed line, the target at the posterior part with a dotted line, the target at the anterior part with a dash-dotted line, and the target at the inferior part with a dashdouble-dotted line (not visible in (a)). In (a), the noise amplitude shown is measured with the LDV aimed at a target without stimulation of the specimen.

onates between 1.5 and 2.0 kHz. The amplitude differences between the positions are between 10 and 100 times for the entire frequency range. At the low frequencies, although at different amplitudes, the positions show similar characteristics. This alters above 1.5 kHz, where the positions show different frequency responses. A similar trend is seen in the phases of the positions: below 1.5 kHz the phases are within 100
while above 1.5 kHz, the spread in phases are great without any clear structure. Although different frequency response functions, the results with BC stimulation show overall characteristics similar to results with AC stimulation (Fig. 3): below 1.5 kHz there is a similarity in the characteristics of the magnitude and phase data between the positions on the RW membrane in the same specimen; above

BC stimulation 1

0.1

(a)

10

(b)

0

Phase (kilodegrees)

Differential velocity between RW membrane and bone at a stimulation velocity of 1 mm/s (mm/s)

frequencies above 0.3 kHz due to the computation of Eq. (1). There are other uncertainties in the measurements of the BC velocities for frequencies below 0.3 kHz (see Section 2.5) giving a low frequency limit at 0.3 kHz for the BC data. The differential velocities, as amplitudes and phases, between the RW membrane and the bone at 35 positions on the RW membrane in temporal bone specimen BC1 are displayed in Fig. 8. The data in Fig. 8 are shown at a BC stimulation of the temporal bone specimen of 1 mm/s in the stimulation direction (same as the low-frequency in-and-out motion of the stapes). In total, four specimens were tested with BC stimulation. All showed similar but not exactly the same result. At low frequencies, the amplitudes rise at about 12 dB/octave and res-

0

10

-1

10

-2

10

-0.1 -0.2 -0.3 -0.4 -0.5 -0.6 -0.7

-3

10

0.1

0.2 0.3

0.5 0.7 1

2

Frequency kHz

3

5

7

-0.8 10

0.1

0.2 0.3

0.5 0.7 1

2

3

5

7

10

Frequency kHz

Fig. 8. Magnitude (a) and phase (b) of the velocity difference between 35 targets on the RW membrane and the promontory bone close to the RW according to Eq. (1). The stimulation is a vibration of the temporal bone specimen BC1 at a velocity of 1 mm/s in line with the low-frequency in-andout motion of the stapes. The frequency resolution is 50 points/decade.

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S. Stenfelt et al. / Hearing Research 198 (2004) 10–24

BC1

BC3

BC2 Phase

Amplitude

Phase

Amplitude

BC4 Phase

Amplitude

Phase

10 kHz

2 mm/s (1 mm/s)

6 kHz

1 mm/s (1 mm/s)

2.5 kHz

1 mm/s (1 mm/s)

1 kHz

0.2 mm/s (1 mm/s)

Amplitude

2

Area: 2.87 mm

2

Area: 3.67 mm

2

Area: 2.97 mm

2

Area: 1.77 mm

Fig. 9. The vibration pattern of the RW membrane in four specimens stimulated with BC sound is displayed as iso-amplitude and iso-phase contours. The result is shown for four frequencies: 1, 2.5, 6, and 10 kHz. The specimens are stimulated with a vibration level of 1 mm/s measured at the cochlear promontory bone. The velocity equidistance between the iso-amplitude contours are 0.2 mm/s at 1 kHz, 1 mm/s at 2.5 kHz, 1 mm/s at 6 kHz, and 2 mm/s at 10 kHz. For the phase plots, the iso-phase contour equidistance is 30
and is related to the center of the RW membrane. A negative phase relation is shown as a dotted line while a positive phase relation is indicated with a solid line.

1.5 kHz no clear pattern is visible. Moreover, the amplitude and phase data of the RW membrane with BC stimulation shows similarities with measured stapes footplate velocity in temporal bone specimens stimulated by BC (Stenfelt et al., 2002). Iso-contour plots of the velocities for the four specimens stimulated by BC are shown in Fig. 9. They are displayed similar as in Fig. 4 with AC stimulation: each RW displays iso-amplitude and iso-phase contours when the stimulation of the temporal bone is 1 mm/s. The plots show the results at 1, 2.5, 6, and 10 kHz. At 1 kHz, the distance between each iso-amplitude contour is 0.2 mm/s, and at 2.5, 6, and 10 kHz, the distances between the iso-amplitude contours are 1, 1, and 2 mm/s, respectively. The iso-phase contours are relative to the center of the RW membrane and the distance between the iso-phase contours is 30 degrees; a solid line indicates a positive phase relation whereas a dotted line indicates a negative phase relation. Since different stimulation entities are used, the magnitudes and phases in Fig. 9 cannot be directly compared with those obtained at the RW with AC stimulation (Fig. 4); however, the patterns can be compared and they show an overall resemblance. At the lower frequencies (below 1.5 kHz) the RW membrane moves primarily in an in-and-out motion but the spatial distribution of the phase indicates some wave propagation over the membrane. At 2.5 kHz the motion is primarily two sections of the membrane moving with nearly opposite phase. However, the phase data indicates some traveling wave

behavior of the membrane as well. At 6 and 10 kHz, Fig. 9 shows complex spatial variation of magnitude and phase giving irregular motion of the RW membrane comprising a mixture of modal and traveling wave motion. Fig. 10 shows an animation of a vibration cycle of the RW membrane at eight equidistant time intervals (similar as Fig. 5). The data are from specimen BC4 and are shown at the frequencies 1, 2.5, 6 and 10 kHz. The vibration is displayed as the relative vibration between the RW membrane and the promontory bone surrounding the RW when the temporal bone is stimulated at a velocity of 1 mm/s in line with the vibration direction of the stapes. The result in Fig. 10 shows further the resemblance between AC and BC stimulations of the overall RW pattern: at 1 kHz the RW membrane moves primarily as a whole, at 2.5 kHz the membrane moves in two separate sections and at 6 and 10 kHz, the membrane displacement is complex with a mixture of modal and traveling wave motion. Two of the specimens stimulated with BC were retested with 10 dB higher stimulation level. Again, the isocontours were compensated for the stimulation increase and compared with the originals. No difference could be seen at the four frequencies 1, 2.5, 6, and 10 kHz. When the velocity increase for each target was inspected for the entire frequency range (0.1–10 kHz), differences in the amplitude were found below 0.3 kHz. These differences are attributed to inaccuracies in the BC measurements for frequencies below 0.3 kHz in this study.

S. Stenfelt et al. / Hearing Research 198 (2004) 10–24

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Fig. 10. The vibration pattern of the RW membrane in specimen BC4 is shown as eight snapshots of a period when the stimulation is a BC vibration velocity of 1 mm/s. The result is shown for the frequencies 1, 2.5, 6, and 10. The displacement amplitudes are greatly enhanced (about 104 times) for visibility purposes. The displacements are color-coded and the bar left of the RW figures indicate the displacement range at each frequency.

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4. Discussion 4.1. RW membrane vibration pattern The vibration pattern of the RW membrane in human cadaver specimens was obtained by measuring the velocity of 28–40 reflective glass-targets placed in a matrix with an approximately spacing of 0.2 mm on the RW membrane. The exact position of each target was determined in a calibrated photograph and mapped to a predefined matrix to visualize the vibration pattern of the RW membrane. This pattern was investigated using three approaches: (1) by analyzing the frequency response of all targets on the RW membrane (Figs. 3 and 8), (2) by analyzing the two-dimensional iso-amplitude and iso-phase contour plots (Figs. 4 and 9), and (3) by analyzing three-dimensional animations of the vibration pattern (Figs. 5 and 10). The entire analysis was done for steady state sinusoid stimulation; no analysis was conducted for impulse stimulation. Similar tests were conducted with AC stimulation and BC stimulation. However, the AC and BC tests were conducted in different specimens and no direct comparison of the RW membrane vibration pattern with AC and BC stimulations could be done. Moreover, the BC stimulation of the specimens was well defined: the specimens showed rigid body motion for the whole frequency range used. In a real head stimulated with BC, the skull-bone shows rigid body motion as well as wave transmission. Hence, the stimulation of the cochlea with BC stimulation can differ between a whole head and the specimens used here and, consequently, the vibration pattern of the RW membrane may be different as well. There were similarities between the vibration patterns obtained when AC and BC stimulations were used. For frequencies below 1.5 kHz, the entire RW membrane moved almost in phase; indication of some traveling wave on the membrane was also seen. The place of maximum displacement differed between the specimens but was close to the center with a general tendency towards the antero-superior position. There were also differences between the maximum displacement amplitude among the specimens. Although specimen AC1 had both the greatest area and displacement amplitude at 1 kHz of the specimens stimulated by AC, the general trend was that the RW membranes of small area had greater displacement amplitudes than the RW membranes with large areas. This was observed for the entire frequency range whether the stimulation was by AC or BC. Above 1.5 kHz, the RW membrane vibrated in two sections that moved with almost 180
phase difference, where one section was usually dominating containing more displaced fluid. A tendency of traveling waves was seen at these frequencies as well. The division into two sections became less obvious above 2.5 kHz and

at around 3 kHz, the RW membrane began to move in several sections without any clear pattern. The sections that moved independently of each other seemed to have a maximum around 6–7 kHz. Above 7 kHz, the RWs showed less distinct maximum and the membrane moved more as a whole while containing fine structure giving variations in both amplitude and phase over the membrane. For AC stimulation and at the highest frequencies (above 7 kHz), the vibration pattern of the RW membrane gave an impression of a traveling wave rolling over the RW when the three-dimensional animations of the RW membranes were analyzed. Such distinct traveling wave pattern was not seen in the three-dimensional animations of the specimens stimulated by BC, even though the phase data in Fig. 9 indicates traveling wave motion of the membrane. A traveling wave is defined by gradual spatial phase variation whereas modal vibration is defined by spatial areas of constant phase separated by small regions with great phase gradients. When examining the iso-phase contours in Figs. 4 and 9, indications of both modal and traveling waves can be seen in the results at all frequencies. This means that both types of RW motion is present through the whole frequency range measured. However, when visualizing the motion, one of the motion modes was dominating at some frequency areas: modal vibration at the low frequencies for both AC and BC stimulations and traveling wave motion at the high frequencies when stimulation is by AC. Between 4 and 7 kHz with AC stimulation and above 4 kHz with BC stimulation, no clear pattern of either modal or traveling wave motion was seen when the RW membrane motion was visualized. 4.2. Comparison with previous data To our knowledge, no information regarding the vibration pattern of the human RW membrane has been reported for AC and BC stimulations. By using timeaveraged holography, Khanna and Tonndorf (1971) and Nomura (1984) measured the RW membrane vibration with AC stimulation in live cats and fresh animal cadaver specimens. Khanna and Tonndorf (1971) reported that at frequencies as low as 125 Hz, the RW membrane appeared to move in several separate sections. That was not seen in this study at those low frequencies. Phase opposition is the only phase information available using a holographic technique; they did not find any clear indication of phase opposition between the sections on the RW membrane, except, possibly, at the high frequencies. Both Khanna and Tonndorf (1971) and Nomura (1984) found the area of maximal displacement at the low frequencies to be the anterosuperior region of the RW, which is similar to our findings. They further reported large intersubject variations in both vibration pattern and magnitude. Both also

S. Stenfelt et al. / Hearing Research 198 (2004) 10–24

reported complicated vibration patterns of the RW membrane without any clear indication of a displacement maximum at the high frequencies. The method used here was to create a matrix of reflective targets and measure their vibration on the RW membrane. There are other methods to obtain the vibration pattern of a surface. These different methods have, in research of the hearing function, primarily been used to measure TM vibrations; for the RW membrane measurements, time-averaged holography was used (Khanna and Tonndorf, 1971; Nomura, 1984). Time-averaged holography requires displacements of more than 100 nm and needs high stimulation levels in order to record the fringes. Further, the only phase information available is phase opposition. Recently, Wada et al. (2002) reported vibration measurements of the TM in guinea pig temporal bone specimens using time-averaged speckle pattern interferometry. By combining time-averaged speckle pattern interferometry with sinusoidal phase modulation and using digital image processing, they were able to increase the amplitude sensitivity as well as extract phase information of the TM vibration. Another method is to use an automatic scanning laser Doppler vibrometer or laser interferometer. This method has also been used when measuring the TM and middle ear ossicles vibration (Konradsson et al., 1987; Ball et al., 1997). Time-average holographic techniques has the advantage of measuring the entire surface area at once but require a sinusoidal stimulation, whereas laser Doppler or interferometer techniques only measure one point at the time but can obtain information of the entire frequency range using broad-band stimulation. For a relatively small area as the RW membrane, the scanning laser, or as here, the manual scanning laser method is preferable whereas for larger areas such as the TM, time-average holographic technique would be less time consuming.

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and the other end of the piston attached to the lenticular process of the incus. After this was done, the velocity of the nine central targets (3 · 3 matrix) was remeasured with AC stimulation. It was found that the vibration pattern of the RW membrane changed for the entire frequency range measured (0.1–10 kHz). At the lower frequencies where the RW membrane moves in a single mode (below 1.5 kHz) the phase of the targets shows the same alteration while the amplitudes of the targets were altered (Fig. 6). Although the amplitude change of the targets differed, they showed similar trend with frequency up to 1.5 kHz. Above 1.5 kHz, where the RW membrane showed more complex vibration pattern, the amplitude and phase of the nine targets changes dramatically and there seem to be no correlation of the alterations of the target velocities. This means that the vibration pattern of the RW membrane altered for the entire frequency range 0.1–10 kHz when the mode of stimulation at the OW was altered. The motion of the RW membrane has been used to measure the cochlear stimulation for evaluation middle ear ossicle reconstructions (Asai et al., 1999). This method has some merit as the RW fluid displacement is close to the OW fluid displacement for AC stimulation (Kringlebotn, 1995; Stenfelt et al., 2004). However, in the study of Asai et al. (1999), only the vibration at the center of the RW membrane was measured. Consequently, those results were affected by the vibration pattern alteration when the stimulation mode at the OW altered. If the RW membrane is used as a measure of the input to the cochlea at the OW, the fluid volume displacement at the RW should be measured directly on the RW membrane as in Stenfelt et al. (2004) or by measuring the sound radiated from the RW membrane as in Kringlebotn (1995).

5. Conclusions 4.3. Changes of the RW membrane vibration pattern When the stimulation level was increased by 10 dB, the same vibration pattern was observed on the RW membrane as before the increase with both AC and BC stimulations. The exception was with BC stimulation below 0.3 kHz where differences in the amplitude response were observed. This change of vibration pattern with BC stimulation at the lowest frequencies was attributed to measurement inaccuracies and not to a real change of the vibration pattern of the RW membrane. Nomura (1984) found, similar to the present study, that an increase in sound pressure did not change the vibration pattern but increased the vibration amplitude. A stapedotomy was conducted in two specimens by gluing the stapes footplate to the OW annulus, the stapes superstructure removed, a hole in the footplate drilled, a 0.6 mm teflon piston positioned in the hole

The RW membrane vibration pattern was assessed by manually scanning the membrane in human temporal bone specimens with an LDV aimed at reflecting targets placed on the surface with an approximate spacing of 0.2 mm. The analysis was conducted in four specimens stimulated with AC sound and in four specimens stimulated with BC sound. The overall vibration pattern of the RW membranes was similar whether AC or BC stimulation was used. At frequencies below 1.5 kHz, the membrane moves nearly in-phase in an in-and-out motion. Between 1.5 and 3 kHz the membrane vibrates primarily in two sections moving almost 180
out of phase. Above 3 kHz the membrane motion is irregular with a mixture of modal and traveling wave motion. There was no alteration in the vibration pattern of the RW membrane after the stimulation level was increased by 10 dB; only an increase of the vibration am-

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S. Stenfelt et al. / Hearing Research 198 (2004) 10–24

plitude corresponding to the stimulation increase. This was found with both AC and BC stimulations. By placing one end of a piston in a drilled hole in the stapes footplate and attach the other end to the incus, the mode of stimulation was altered when AC stimulation was used. This led to a change in the vibration pattern of the RW membrane for the entire frequency range 0.1– 10 kHz. Consequently, measuring RW membrane vibration at a single point for evaluation of middle ear ossicle reconstructions can give erroneous results.

Acknowledgements This work was supported in part by a V.A. merit review grant (GDE0010ARG), the Swedish Institute, and the Swedish Research Council for Engineering Sciences (TFR 299-2000-576). References Asai, M., Huber, A.M., Goode, R.L., 1999. Analysis of the best site on the stapes footplate for ossicular chain reconstruction. Acta Otolaryngol. 119, 356–361. Ball, G.R, Huber, A., Goode, R.L., 1997. Scanning laser Doppler vibrometry of the middle ear ossicles. Ear Nose Throat J. 76, 213– 216 218, 220, 222. Be´ke´sy, G. von, 1932. Zur theorie des ho¨rens bei der schallaufnahme durch knochenleitung. Ann. Phys. 13, 111–136. Be´ke´sy, G. von, 1948. The vibration of the cochlear partition in anatomical preparations and in models of the inner ear. J. Acoust. Soc. Am. 20, 227–241.

Be´ke´sy, G. von, 1955. Paradoxical direction of wave travel along the cochlear partition. J. Acoust. Soc. Am. 27, 137–145. Hato, N., Welsh, J., Goode, R.L., Stenfelt, S., 2001. Acoustic role of the buttress and posterior incudal ligament in human temporal bones. Otolaryngol. Head Neck Sur. 124, 274–278. Khanna, S.M., Tonndorf, J., 1971. The vibratory pattern of the round window in cats. J. Acoust. Soc. Am. 50, 1475–1483. Khanna, S.M., Tonndorf, J., Queller, J., 1976. Mechanical parameters of hearing by bone conduction. J. Acoust. Soc. Am. 60, 139–154. Konradsson, K.S., Ivarsson, A., Bank, G., 1987. Computerized laser Doppler interferometric scanning of the vibrating membrane. Scand. Audiol. 16, 159–166. Kringlebotn, M., 1995. The equality of volume displacement in the inner ear windows. J. Acoust. Soc. Am. 98, 192–196. Nomura, Y., 1984. Otological significance of the round window. Adv. Oto. Rhino. Laryngol. 33, 1–162. Puria, S., Peake, W.T., Rosowski, J.J., 1997. Sound–pressure measurements in the cochlear vestibule of human-cadaver ears. J. Acoust. Soc. Am. 101, 2754–2770. Stenfelt, S., Hato, N., Goode, R.L., 2002. Factors contributing to bone conduction: the middle ear. J. Acoust. Soc. Am. 111, 947–959. Stenfelt, S., Hato, N., Goode, R.L., 2004. Fluid volume displacement at the oval and round windows with air and bone conduction stimulation. J. Acoust. Soc. Am. 115, 797–812. Stenfelt, S., Puria, S., Hato, N., Goode, R.L., 2003. Basilar membrane and osseous spiral lamina motion in human cadavers with air and bone conduction stimuli. Hear. Res. 181, 131–143. Tonndorf, J., 1972. Bone conduction. In: Tobias, J. (Ed.), Foundations of Modern Auditory Theory, second ed. Academic Press, New York, pp. 197–237. Wada, H., Ando, M., Takeuchi, M., Sugawara, H., Koike, T., Kobayashi, T., Hozawa, K., Gemma, T., Nara, M., 2002. Vibration measurement of the tympanic membrane of guinea pig temporal bones using time-averaged speckle pattern interferometry. J. Acoust. Soc. Am. 111, 2189–2199. Wever, E.G., Lawrence, M., 1954. Physiological Acoustics. Princeton University Press, Princeton, NJ.