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8. University of Zurich, Zurich, Switzerland. 9. 2Department of Clinical and ... 12. 13. Corresponding Author: 14. Christof Roosli, MD. 15. Department of ...

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Intracranial Pressure and Promontory Vibration with Soft Tissue Stimulation in

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Cadaveric Human Whole Heads

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Christof Roosli, MD1, Ivo Dobrev, PhD1, Jae Hoon Sim, PhD1, Rahel Gerig1, Flurin Pfiffner,

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PhD1, Stefan Stenfelt, PhD2, Alexander M. Huber, MD1

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University of Zurich, Zurich, Switzerland

Department of Otorhinolaryngology, Head and Neck Surgery, University Hospital Zurich,

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Sweden.

Department of Clinical and Experimental Medicine, Linköping University, Linköping,

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Corresponding Author:

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Christof Roosli, MD

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Department of Otorhinolaryngology, Head and Neck Surgery, University Hospital Zurich

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Frauenklinikstrasse 24

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CH-8091 Zurich, Switzerland

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Telephone:

++41 44 255 47 67

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Fax:

++41 44 255 41 64

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E-Mail: [email protected]

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Running title: intracranial pressure with soft tissue stimulation

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Conflicts of Interest and Source of Founding: Author SS is supported by the Swedish

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Research Council. Fore the remaining authors none were declared.

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ABSTRACT

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Hypothesis: Soft tissue stimulation induces bone vibration to a similar extent like bone

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conduction (BC) stimulation.

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Background: A hearing sensation can be elicited by vibratory stimulation on the skin

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covered skull, or by stimulation on soft tissue such as the neck. It is not fully understood

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whether all these different stimulation sites induce skull vibration or whether other

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transmission pathways are dominant. The aim of this study is to assess the correlation

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between intracranial pressure and skull vibration on the promontory for different stimulation

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sites.

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Methods: Measurements were performed on 4 human cadaver heads. A BC hearing aid was

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held in place with a 5-Newton steel headband at four locations (mastoid, forehead, eye, and

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neck). While stimulating in the frequency range of 0.3 – 10 kHz, acceleration of the cochlear

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promontory were measured with a Laser Doppler Vibrometer, and intracranial pressure at the

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center of the head with a hydrophone.

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Results: Promontory acceleration and intracranial pressure was measurable for all stimulation

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sites. Its ratio is comparable between all stimulation sites.

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Conclusions: These findings indicate that promontory acceleration and intracranial pressure

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are involved to a similar extent for stimulation on the sites investigated. The transmission

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pathway of sound energy is comparable for these four stimulation sites.

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Key words: bone conduction, soft tissue stimulation, intracranial pressure, promontory

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vibration

 

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INTRODUCTION

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Bone conduction (BC) is an alternative pathway to air conduction (AC) for sound to

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reach the cochlea. It is widely used in clinical audiometry as it is used to classify conductive

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and sensorineural hearing loss. However, the exact mechanism of BC hearing has not been

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completely understood, neither in normal hearing conditions nor in pathologic situations of

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the middle ear. It is thought that a complex interaction of several different pathways causes

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the hearing sensation with BC sound. The importance of the different pathways depends on

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the stimulation frequency and on pathologies of the middle ear. Most of the pathways are

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agreed on to involve bone vibrations: 1) Distortional vibrations of the cochlear shell cause

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small deformations of the cochlear walls (1). These deformities cause fluid flow in the

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cochlea that excites the basilar membrane. 2) Vibrations of the skull induce inertial forces of

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cochlear fluid that result in pressure change in the inner ear exciting the basilar membrane (2,

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3). A similar phenomenon is the relative motion of the skull and middle ear ossicles caused

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by the inertia of the ossicles (2, 4, 5), which stimulates the inner ear through motion of the

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stapes footplate in the oval window. 3) And finally, skull vibration causes vibration of the

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osseous and cartilaginous external ear canal, resulting in a sound pressure in the external ear

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canal and motion of the tympanic membrane and ossicular chain similar to AC stimulation.

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This pathway is affected by changing the state of the ear canal from open to closed (occlusion

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effect) (6-8).

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Another suggested pathway is dynamic sound pressure transmission from the skull

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interior (brain tissue and cerebrospinal fluid) to the cochlea. Sohmer (9) coupled in an

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experimental study the cranial cavities of two animals by a saline filled plastic tube. A bone

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conduction click stimulus was applied to animal 1, while the brainstem evoked response

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auditory (BERA) was recorded from the second animal. They found a correlation between

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stimulation in animal 1 and BERA response in animal 2, and concluded that sound pressure

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can be transmitted by a fluid pathway to the cochlea and stimulate it. In other experiments,

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the acceleration of the bone was measured for stimulation at the forehead, eye or directly on

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the brain. While BERA could be clearly recorded for all simulation sites, no acceleration of

 

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the bone was measured for stimulation at the eye in human (9) or at the brain in animals (10).

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On the contrary, others found bone vibration when measured directly at the teeth for

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stimulation at the eye. Even so, they found no direct correlation between the BC threshold

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and vibration of the teeth (11). However, it is not certain that the vibration of the teeth

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corresponds to the vibrations of the bone surrounding the cochlea.

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The aim of this study is to compare the relation between intracranial sound pressure

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and bone vibrations measured at the cochlear promontory for stimulation on skin covered

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bone (mastoid and forehead) and on soft tissue (eye and neck). We hypothesize that

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intracranial pressure and skull vibrations are correlated and depend on the stimulation

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position and frequency.

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METHODS

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The experiments were reviewed and approved by the institutional Ethic Committee

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(KEK-ZH-Nr. 2012-0136). In this study, four cadaveric human whole heads that were

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conserved using a technique described by Thiel (12) were used. An endaural incision was

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performed between the helix and the tragus to achieve access to the promontory. Then, a

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tympanomeatal flap was elevated to expose the middle ear (13). Two self-retaining retractors

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were placed to allow good visualization of both the endaural surgery and the later LDV

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measurement. To enhance reflectivity of the laser beam, a small piece of retro-reflective foil

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(1 x 1 mm) was placed onto the cochlear promontory near to the round window on the

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measurement position. The skull was opened at the vertex and a tube of 5 mm diameter was

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tightly sealed to the opening. Details regarding surgical preparation are described in our

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previous work (14).

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Measurements were performed on a stainless steel table to minimize vibrations from

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unwanted sources. A hydrophone (Type 8103, Brüel & Kjær, Denmark) was inserted into the

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intracranial space through the tube. The hydrophone was positioned at the center of the

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cranial hemisphere and its position controlled by X-ray (Figure 1). The physiologic

 

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intracranial pressure of 15cm H2O2 was maintained by a water column in the tube attached to

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the skull of 15 cm (15).

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The transducer of a BAHA Cordell II (Cochlear Company, Australia) was attached to

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the head at 4 positions (mastoid, forehead, eye, and neck) using a 5-Newton steel-headband.

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The coupling forces were controlled with a spring gauge (Light Line, Pesola, Switzerland).

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The stimulus was directly routed to the transducer with a stimulus intensity of 1 Volt, that

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was generated by the measurement system Audio Precision System One (Audio Precision

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Inc., USA). The sound stimulus consisted of a stepped sine measurement procedure in the

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frequency range of 0.3 – 10 kHz. The measurement frequencies were equally spaced on a

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logarithm scale (50 frequency points per decade), resulting in 78 frequencies in the frequency

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range used.

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All motions of the cochlear promontory were measured at a single point using an

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OFV-3001 Scanning Laser Doppler Vibrometry (SLDV) system (Polytec GmbH, Germany).

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The sampling frequency was set at 51.2 kHz. The output of the SLDV was coupled to the

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Audio Precision System One for further data processing. All of the measurement procedures

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were controlled by the Audio Precision software (AP 2700 Control software) installed on a

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personal computer. The acceleration of the cochlear promontory was calculated from the

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recorded velocity. Simultaneously, intracranial pressure was recorded using the hydrophone

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positioned in the cranial space (see above). The recorded pressures were routed to the Audio

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Precision System One via a charge amplifier (Type 2635, Brüel & Kjær, Denmark).

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The stimulation forces with the BAHA Cordell II transducer placed on the skin by the

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steel-headband were calibrated using an artificial mastoid (Type 4930, Brüel & Kjær), and the

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measured cochlear promontory accelerations and intracranial pressure changes were

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normalized by the stimulation force. During the calibration of the transducer on the artificial

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mastoid, the mechanical impedance of the artificial mastoid was measured, and the static

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force between the transducer and the surface of the artificial mastoid was maintained at

 

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approximately 5 Newton, which corresponds to the coupling force between the skin and the

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transducer in the cadaver heads.

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RESULTS

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The cochlear promontory accelerance, which is defined as acceleration normalized by

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the stimulation force, is shown in figure 2 for all four heads separately and for all stimulation

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sites. The cochlear promontory vibration varied among the skulls and the spread among

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specimens was larger than the differences between different stimulation sites for one

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specimen. For stimulation at the mastoid and forehead, the signal was above noise level for

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most frequencies. There was a tendency for low signal to noise ratio (SNR) for stimulation at

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the neck at frequencies above 2 kHz and for stimulation at the eye for frequencies above 3

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kHz. Generally, acceleration of the cochlear promontory was largest with stimulation at the

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mastoid. Lowest acceleration of the promontory was measured for stimulation at the neck.

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Intracranial pressure for stimulation at all sites was measured in all four specimens

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(Figure 3). Again, the variability among the heads was larger than the variability between

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stimulation sites in one head. Therefore the results are shown for each head separately. A

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SNR greater than 10 dB was achieved for all stimulation sites for frequencies below 2 kHz.

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The SNR was less than 10 dB at frequencies above 2 kHz for stimulation at the mastoid,

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forehead, and neck, while the signal was close to or in the noise for stimulation at the neck for

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frequencies above 2 kHz. Largest intracranial pressure was measured for stimulation at the

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mastoid and the forehead. Smallest intracranial pressure was measured when the stimulation

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was at the neck.

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The ratio between vibration of the cochlear promontory and intracranial pressure is

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compared for all stimulation sites and for all specimens (Figure 4). For stimulation on the

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neck and eye, this ratio is within the ratio of mastoid and forehead. Above 2 kHz, the ratio for

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stimulation at the neck needs to be interpreted with care, because the promontory motion and

 

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intracranial pressure was close to the noise level. For frequencies below 2 kHz, these

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findings indicate that regardless of the site of stimulation, vibration of the cochlear

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promontory and intracranial pressure was registered. These two components seem to be

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related and are not mutually independent. The larger magnitude of the cochlear promontory

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vibration and intracranial pressure when the stimulation is on the skin covered bone at the

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mastoid and forehead indicates that this stimulation mode is more efficient than stimulating

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on the head or neck.

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DISCUSSION

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This study investigates the relation between vibration of skull measured at the

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cochlear promontory and intracranial pressure for BC stimulation at four different positions:

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mastoid, forehead, eye and neck. The hypothesis is that skull vibration and intracranial

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pressure correlate independent of the position of stimulation resulting in similar frequency

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functions.

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Measurements were performed in four cadaveric whole heads that give a close

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approximation to the in vivo situation for the following reasons: the heads were stored

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according to a technique described by Thiel (12) which shows no significant difference in

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biomechanical testing as compared to fresh frozen material (16, 17). For measurements on

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BC pathways, dry skulls, temporal bones, and animals have been used in previous studies (4,

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5, 9, 18). Using cadaveric whole heads has the advantage of the presence of soft tissue

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remaining attached to the head and a fluid filled intracranial space as compared to

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measurements on dry skulls or temporal bones. Additionally, the presence of the whole

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circumference of the head may model the complexity of BC pathways more adequately than

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temporal bones or measurements on animals. The cochlear promontory vibrations are

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comparable to the measurement of others (17, 19) who also stimulated on the skin covered

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bone on Thiel fixed heads (17), or directly on the skull (19) (Figure 5).

 

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Vibrations of the promontory were only measured in one direction which does not

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exactly address the complexity of the three dimensional motion of the skull in BC

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stimulation. However, cochlear promontory vibration levels in the three perpendicular

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directions are normally within 5 dB (20). Therefore, we assumed that vibration of the skull

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did not significantly differ in the three perpendicular directions and our method is a valid

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approximation.

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One limitation of our measurement is that some data were close to, or below, the

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noise level, especially for stimulation at frequencies above 4 kHz and for stimulation at the

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neck and eye. One reason is the damping of the skin that affects the effective stimulation at

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the frequencies above 4 kHz (21). This corresponds to worse hearing thresholds at these

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positions compared with the mastoid position in normal hearing subjects (11, 22). A greater

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driving voltage of the transducer could have been used but most likely would have caused

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distortions of the stimulation.

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Another finding was the large variability among the four heads. Averaging of the

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measurements of the four cadaver heads was therefore not meaningful. Analysis of the

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cochlear promontory vibration and intracranial pressure was done for each head individually.

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The exact reason for this large variability is unclear. On reason might be differences in

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anatomical structures such as thickness and circumference of the skull, or thickness and

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structure of the soft tissue. Another possible contributor to differences is the coupling and

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attenuation of the skin and soft tissues in the transducer-skull interface. This influence was

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attempted to be minimized by controlling the static force of the coupling of the headband by a

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force gauge.

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It has been shown that direct stimulation of the soft tissues (i.e. eye or neck)

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stimulates the cochlea and causes a hearing sensation (11, 23, 24). In the current

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measurements, the absolute magnitude for both the cochlear promontory vibration and

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intracranial pressure tended to be smaller for stimulation at the eye or neck compared with the

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mastoid or the forehead. Such findings are consistent with worse hearing threshold for

 

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stimulation at these locations as compared to stimulation at the mastoid. The lower magnitude

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of promontory vibration by up to 10 dB for stimulation at the eye compared to stimulation at

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the mastoid is consistent with the 10 to 15 dB lower hearing threshold for stimulation at the

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eye (11, 22).

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The results presented in this study indicate that the ratio of the cochlear promontory

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vibration and intracranial pressure is comparable for stimulation on skin covered bone and

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soft tissue without direct contact to bone. These findings can be explained by an interaction

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between soft tissue, skull content and skull that results in vibration of the bone surrounding

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the cochlea, and the intracranial space. It’s controversially discussed in the literature whether

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vibration of the soft tissue is independent from bone vibration or not. Some reports claim that

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soft tissue conduction does not involve bone vibration (9, 10, 24, 25). In an animal model,

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Chordekar et al. (24) measured auditory brainstem responses (ABR) and vibrations of the

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bony vestibule with an LDV for BC and soft tissue stimulation. For BC stimulation, ABR and

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bone vibrations were measured, while for soft tissue stimulation only ABR were recorded for

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low intensities. One possible reason for the difference to our findings is that vibrations may

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have been too low to be detected, because low intensity stimulation was used. If bone

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vibration did not contribute to BC hearing for stimulation at the neck, the ratio between

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promontory vibration and intracranial pressure change is expected to be much lower than for

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direct stimulation of the bone. Our data do not show such a difference in ratio, suggesting that

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soft tissue stimulation involves bone vibration similarly to direct stimulation on the bone.

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CONCLUSIONS

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This similar ratio for stimulation on bone and on soft tissue indicates that the stimulation sites

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investigated involve promontory vibration and intracranial pressure to a same extent, meaning

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that bone vibration is considerably involved in soft tissue stimulation.

 

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References

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1) Tonndorf J. Compressional bone conduction in cochlear models. J Acoust Soc Am

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1962;34:1127-31.

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2) Wever EG, Lawrence M. Physiological Acoustics. Princeton University Press,

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3) Stenfelt S, Goode RL. Bone-conducted sound: physiological and clinical aspects. Otol

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Neurotol 2005;26:1245-61.

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4) Barany E. A contribution to the physiology of bone conduction. Acta Otolaryngol

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5) Stenfelt S, Hato N, Goode RL. Factors contributing to bone conduction: the middle ear. J

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Acoust Soc Am 2002;111(2):947-59.

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6) Tonndorf J. Bone conduction. In: Tobias JV ed. Foundations of Auditory Theory, vol. II.

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New York: Academic Press, 1972;197-237.

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7) Khanna SM, Tonndorf J, Queller JE. Mechanical parameters of hearing by bone

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conduction. J Acoust Soc Am 1976;60:139-54.

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8) Stenfelt S, Reinfeldt S. A model of the occlusion effect with bone conduction stimulation.

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Int J Audiol 2007;46:595-608.

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9) Sohmer H, Freeman S. Further evidence for a fluid pathway during bone conduction

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auditory stimulation. Hear Res 2004;193:105-10.

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10) Freeman S, Sichel JY, Sohmer H. Bone conduction experiments in animals - evidence for

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a non-osseous mechanism. Hear Res 2000;146(1-2):72-80.

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11) Ito T, Röösli C, Kim CJ, Sim JH, Huber AM, Probst R. Bone conduction thresholds and

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skull vibration measured on the teeth during stimulation at different sites on the human head.

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Audiol Neurootol 2011;16(1):12-22.

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12) Thiel W. Die Konservierung ganzer Leichen in natürlichen Farben. Ann Anat

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1992;174:185–95.

 

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13) Fisch U, May J, Linder T. Tympanoplasty, Mastoidectomy and Stapes Surgery, 2nd ed.

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Stuttgart, Germany: Georg Thieme Verlag, 2008. 8-11.

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14) Huber AM, Sim JH, Xie YZ, Chatzimichalis M, Ullrich O, Röösli C. The Bonebridge:

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Preclinical evaluation of a new transcutaneously-activated bone anchored hearing device.

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Hear Res 2013;301:93-9.

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15) Steiner LA, Andrews PJ. Monitoring the injured brain: ICP and CBF. British Journal of

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Anaesthesia 2006;97(1):26–38.

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16) Boryor A, Hohmann A, Wunderlich A, Geiger M, Kilic F, Sander M, Sander C, Böckers

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T, Günter Sander F. In-vitro results of rapid maxillary expansion on adults compared with

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finite element simulations. J Biomechan 2010;43:1237–42.

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17) Guignard J, Stieger C, Kompis M, Caversaccio M, Arnold A. Bone conduction in Thiel-

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embalmed cadaver heads. Hear Res 2013;306:115-22.

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18) Stenfelt S, Wild T, Hato N, Goode RL. Factors contributing to bone conduction: the outer

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ear. J Acoust Soc Am 2003;113,:902-13.

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19) Eeg-Olofsson M, Stenfelt S, Granström G. Implications for contralateral bone-conducted

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transmission as measured by cochlear vibrations. Otol Neurotol 2011;32:192-8.

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20) Stenfelt S, Goode RL. Transmission properties of bone conducted sound: measurements

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in cadaver heads. J Acoust Soc Am 2005;118(4):2373-91.

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21) Stenfelt SP, Hakansson BE: Sensitivity to boneconducted sound: excitation of the mastoid

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vs the teeth. Scand Audiol 1999;28:190–8.

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22) Adelman C, Sohmer H. Thresholds to soft tissue conduction stimulation compared to

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bone conduction stimulation. Audiol Neurootol 2013;18(1):31-5.

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23) Watanabe T, Bertoli S, Probst R. Transmission pathways of vibratory stimulation as

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measured by subjective thresholds and distortion-product otoacoustic emissions. Ear Hear

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2008;29(5):667-73.

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24) Chordekar S, Kriksunov L, Kishon-Rabin L, Adelman C, Sohmer H. Mutual cancellation

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between tones presented by air conduction, by bone conduction and by non-osseous (soft

 

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tissue) bone conduction. Hear Res 2012;283(1-2):180-4.

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25) Perez R, Adelman C, Sohmer H. Bone conduction activation through soft tissues

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following complete immobilization of the ossicular chain, stapes footplate and round window.

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Hear Res 2011;280(1-2):82-5.

 

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Figures Captions

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Figure 1

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The position of the hydrophone was checked by X-ray in two planes, lateral view (A), frontal

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view (B) to make sure it is positioned in the center of the cranial space not touching the skull.

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Figure 2

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Promontory motion for all four heads (A-D).

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Figure 3.

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Intracranial pressure for all four heads (A-D).

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Figure 4.

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Ratio of promontory motion and intracranial pressure for all four heads (A-D).

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Figure 5.

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Magnitude of promontory motion for all four heads compared to magnitude of promontory

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motion with direct stimulation on the skull bone (19).

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