Accepted Manuscript Interaction between osseous and non-osseous vibratory stimulation of the human cadaveric head J.H. Sim, I. Dobrev, R. Gerig, F. Pfiffner, S. Stenfelt, A.M. Huber, C. Röösli, MD PII:
S0378-5955(15)30093-9
DOI:
10.1016/j.heares.2016.01.013
Reference:
HEARES 7102
To appear in:
Hearing Research
Received Date: 31 July 2015 Revised Date:
18 January 2016
Accepted Date: 20 January 2016
Please cite this article as: Sim, J., Dobrev, I, Gerig, R, Pfiffner, F, Stenfelt, S, Huber, A., Röösli, C, Interaction between osseous and non-osseous vibratory stimulation of the human cadaveric head, Hearing Research (2016), doi: 10.1016/j.heares.2016.01.013. This is a PDF file of an unedited manuscript that has been accepted for publication. As a service to our customers we are providing this early version of the manuscript. The manuscript will undergo copyediting, typesetting, and review of the resulting proof before it is published in its final form. Please note that during the production process errors may be discovered which could affect the content, and all legal disclaimers that apply to the journal pertain.
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Interaction between osseous and non-osseous vibratory stimulation of the human
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cadaveric head
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Sim JH , Dobrev I , Gerig R , Pfiffner F , Stenfelt S , Huber AM
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and Röösli C
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Department of Otolaryngology, Head and Neck Surgery, University Hospital Zürich,
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Switzerland 2
University of Zurich, Switzerland
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Department of Clinical and Experimental Medicine, Linköping University, Linköping,
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Sweden.
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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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ACCEPTED MANUSCRIPT ABSTRACT
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Bone conduction (BC) stimulation can be applied by vibration to the bony or skin covered
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skull (osseous BC), or on soft tissue such as the neck (non-osseous BC). The interaction
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between osseous and non-osseous bone conduction pathways is assessed in this study. The
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relation between bone vibrations measured at the cochlear promontory and the intracranial
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sound pressure for stimulation directly on the dura and for stimulation at the mastoid
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between 0.2 – 10 kHz was compared. First, for stimulation on the dura, varying the static
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coupling force of the BC transducer on the dura had only a small effect on promontory
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vibration. Second, the presence or absence of intracranial fluid did not affect promontory
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vibration for stimulation on the dura. Third, stimulation on the mastoid elicited both
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promontory vibration and intracranial sound pressure. Stimulation on the dura caused
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intracranial sound pressure to a similar extent above 0.5 kHz compared to stimulation on the
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mastoid, while promontory vibration was less by 20-40 dB. From these findings, we conclude
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that intracranial sound pressure (non-osseous BC) only marginally affects bone vibrations
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measured on the promontory (osseous BC), whereas skull vibrations affect intracranial
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sound pressure.
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KEY WORDS: Bone conduction, intracranial sound pressure, promontory vibration, dura
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stimulation, mastoid stimulation.
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HIGHLIGHTS:
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- Promontory vibration (osseous bone conduction) and intracranial sound pressure (non-
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osseous bone conduction) were measured in human cadaveric whole heads in response to
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vibrational stimulation of the bone or dura.
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- A bone conduction stimulator was attached either to the mastoid or placed on the dura
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“without contacting surrounding bone”.
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- This enabled two modes of stimulation: 1) osseous stimulation on the mastoid and 2) non-
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osseous stimulation on the dura
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- Intracranial sound pressure was comparable >500 Hz for both modes of stimulation.
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- Promontory vibration was less by 20-40 dB for stimulation on the dura compared to bone.
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- Dura stimulation only marginally affected bone vibrations as measured on the promontory,
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whereas stimulation on the mastoid affected intracranial sound pressure.
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ABBREVIATIONS: AC, air conduction; BC, bone conduction; MRI, magnetic resonance
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imaging; BERA, brainstem evoked response audiometry; LDV, laser Doppler vibrometry;
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SNR, signal-to-noise ratio.
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1. INTRODUCTION
A hearing sensation can be elicited when a stimulus is presented not only by air
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conduction (AC) but also by bone conduction (BC), or by a combination of the two. Several
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different pathways and their interactions have been demonstrated to contribute to BC hearing
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(Stenfelt, 2006; Stenfelt and Goode, 2005; Tonndorf, 1966). The importance of these
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pathways depends on frequency and the state of the middle ear ossicles (Stenfelt, 2014).
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Both osseous and non-osseous pathways contribute to the final sensation of hearing. Four
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osseous BC pathways have been identified: a) pathways involving bone vibration
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(compression and expansion of the otic capsule (Stenfelt, 2014; Tonndorf, 1966; von
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Bekesy, 1960); b) sound radiated in the external auditory canal (Brummund et al., 2014;
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Stenfelt et al., 2003); c) inertia of the ossicles (Homma et al., 2010; Stenfelt, 2006; Stenfelt et
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al., 2002); d) inertia of the inner ear fluid (Kim et al., 2011; Stenfelt, 2014). One non-osseous
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BC pathway has been documented (Sohmer et al., 2004). The non-osseous pathway may
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involve a possible mechanism that includes dynamic sound pressure transmission from the
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contents of the skull, such as brain tissue and cerebrospinal fluid via the internal auditory
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canal, cochlear aqueduct and/or vestibular aqueduct to the cochlea. Evidence for the non-
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osseous mechanism has come from studies both on experimental animals (Sohmer and
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Freeman, 2004) and humans (Sohmer et al., 2000).
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In order to induce a hearing sensation, a BC transducer can be placed at various
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soft tissue (soft-tissue stimulation) such as the eye, neck or thorax can cause a hearing
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sensation. For example, distortion product otoacoustic emissions can be elicited by a
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combination of an air conducted stimulus using an earphone in the ear canal and a stimulus
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on the eye delivered via a BC transducer (Watanabe et al., 2008). Further, soft-tissue
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stimulation is an additional pathway of sound transmission in a high-energy sound field. For
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example, during an explosion, limiting the air conduction pathway to the ear with earplugs
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and earmuffs does not offer complete protection against damage. Protection is limited to 38-
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43 dB from 1 - 1.4 kHz (Ravicz et al., 2000), or it may be frequency dependent, ranging from
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40 to 60 dB (Reinfeldt et al., 2007).
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It has been proposed that soft-tissue stimulation by a BC transducer induces an
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auditory response via a predominantly non-osseous pathway (Adelman et al., 2015;
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Freeman et al., 2000; Sohmer et al., 2000). Evidence for this assumption comes from
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experimental studies using clicks as stimuli during brainstem evoked response audiometry
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(BERA). Such studies found no acceleration of the bone measured for stimulation of the eye
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in human (Sohmer et al., 2000) or for stimulation of the brain in experimental animals
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(Freeman et al., 2000). In amphibians, similar mechanisms have been described and
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although concurrent bone vibrations could not be ruled out completely, they were deemed to
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be unlikely (Seaman, 2002). In contrast, skull vibrations, as measured on the teeth following
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stimulation on the eye have been described on normally hearing humans (Ito et al., 2011).
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While vibration of the teeth was clearly measureable, no direct correlation between the BC
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threshold and vibration of the teeth was found, suggesting that non-osseous pathways
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contribute to hearing for this mode of stimulation. One caveat is that vibration of the teeth
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may not directly correspond to vibrations of the bone surrounding the cochlea.
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Osseous pathways can be investigated by measuring bone vibrations at the cochlear
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promontory (Eeg-Olofsson et al., 2013), and non-osseous pathways can be assessed by
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measuring intracranial sound pressure in the head. The aim of this study was to investigate
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the interaction between non-osseous and osseous pathways following stimulation with a BC
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promontory and intracranial sound pressure for stimulation on the dura and on the mastoid
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(Figure 1). We hypothesized that intracranial sound pressure and skull vibrations would be
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correlated for the two stimulation modalities depending on stimulation frequency and the
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presence or absence of cranial fluid in the cadaver heads.
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2. MATERIALS AND METHODS
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2.1 Preparation of specimen
The experiments were reviewed and approved by the institutional Ethics Committee
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(KEK-ZH-Nr. 2012-0136). Measurements were made on four cadaveric whole human heads
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that were conserved using a technique described by Thiel (Thiel, 1992).This method does
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not significantly change the properties of the soft tissue (Guignard et al., 2013). An endaural
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incision was performed between the helix and the tragus. Next, the tympanomeatal flap was
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elevated to expose the middle ear to gain direct access to the promontory (Fisch et al.,
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2008). Two self-retaining retractors were placed to allow good visualization of the promontory
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and access for the Laser Doppler Vibrometry (LDV) beam, which was used to measure
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promontory vibrations. To enhance reflectivity of the laser beam, a small piece of retro-
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reflective foil (i.e., 10dB for all frequencies for stimulation with the BC transducer fixed to the
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mastoid. For direct stimulation on the dura, an SNR >10 dB was obtained in the frequency
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range of 0.2-5kHz, with the exception of the 0.5-0.7 kHz range as noted by the dotted lines in
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all relevant figures.
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3.1. Effects of varying the experimental conditions
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3.1.1. Promontory vibration and intracranial sound pressure for stimulation on mastoid
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Promontory vibration for stimulation on the mastoid (MastStim) was comparable among all four specimens across the measured frequency range. The variation remained
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within 5 dB, indicating that the attachment of the device and the location of stimulation were
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uniform (Figure 3). The response curves were smoother than the corresponding curves (I-4
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on Occiput) in Stenfelt and Goode (2005), where the BAHA transducer mounted on dry skulls
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was used for stimulation and the promontory motion was measured using an accelerometer
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and a LDV system. Greater variability was observed for intracranial sound pressure, which
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was around 10 dB across the measured frequency range. The increased variability in
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intracranial sound pressure may be attributed to variation in the position of the hydrophone,
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and/or to differences of the material properties of the intracranial content, meaning that the
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brain substance was more liquid (less viscous) in some heads whereas it remained more
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solid in others.
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3.1.2. Increasing coupling force for stimulation on dura Effects of altering the coupling force of the BC stimulator on the dura (DuraStim) were analyzed in two heads (Figure 4). Generally, little effect was observed on promontory
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vibration for varying the coupling force. In head CH4 14-9, the frequency location of a local
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peak in magnitude of the promontory vibration response at around 0.4 kHz shifted to higher
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frequencies (i.e., 0.6 kHz) with increased coupling force. No effect in the other frequencies
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was seen, especially not on the highest peak around 1.5 kHz, and no clear trend was seen in
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head CH6 8-10. In general, intracranial sound pressure tended to have its highest peak
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between 1 – 2 kHz in all heads. Head CH4 14-09 showed increased intracranial pressure
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that corresponded with increased coupling force below 1 kHz, which indicates a rigid
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coupling of the BC stimulator to the dura. However, the higher coupling force only lead to an
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increase in bone vibration in one head between 0.4 – 0.5 kHz, indicating that the interaction
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between intracranial sound pressure and bone vibration is minimal.
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3.1.3. Influence of intracranial fluid on promontory motion for stimulation on dura
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To assess the effect of intracranial fluid on bone vibration, stimulation on the dura
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(DuraStim) was compared in two heads under two conditions. In the first, the heads were
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fluid filled and an intracranial sound pressure of 15 cm water column was maintained while
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the coupling force was set at 5 N. In the second, the fluid was removed from the skull by
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passively allowing it to flow out of the head (drained head), however the brain tissue was
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retained. The amount of remaining tissue or fluid was not controlled objectively. Intracranial
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sound pressure and promontory vibration were compared for the two conditions. Intracranial
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sound pressure was greater for the fluid filled condition. The differences between the two
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heads may be explained by differences in the amount of remaining fluid. Promontory
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vibration only showed an increase in magnitude around 0.3 kHz and 1.5 kHz, whereas
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differences were small at the other frequencies (Figure 5).
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3.2. Comparison of stimulation on mastoid versus on dura
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The magnitude of promontory vibration was larger by 10 to 40 dB for the MastStim as compared to DuraStim (Figure 6). Differences were smallest (i.e., 10 dB) for the low
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frequencies and increased above 0.5 kHz. Intracranial sound pressure was larger (i.e., 20
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dB) for DuraStim between 0.2 and 0.5 kHz while the differences were smaller (i.e., 10dB, with the BC transducer attached to the mastoid (MastStim) and to the dura
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(DuraStim). Promontory vibrations with DuraStim were 10-40 dB smaller at all frequencies
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than promontory vibrations with MastStim, and the difference increased with frequency. This
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is consistent with previous measurements (Stenfelt and Goode, 2005) of promontory
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vibration with bone stimulation at the skull’s vertex versus at the mastoid. Intracranial sound
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pressure was comparable for both stimulation methods above 0.5 kHz. This suggests that
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the coupling between the BC transducer and the skull, for stimulation on the dura (DuraStim),
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through the band is not significant for frequencies above 0.5 kHz. Further reduction of the
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possible coupling variability for the dura stimulation (DuraStim) could potentially be achieved
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by supporting the BC transducer independently of the head, which could allow for better and
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easier control of the coupling force, area and location, while avoiding direct coupling with the
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skull. These findings suggest that sound transfer from bone to intracranial contents is more
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efficient above 0.5 kHz than vice versa. Therefore, sound transfer from intracranial fluid to
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bone is not a major pathway to elicit auditory vibrations. The question of whether intracranial
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sound pressure can evoke a hearing sensation cannot be answered by our measurement
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setup on cadaver heads. In the literature, findings are contradictory. Chordekar et al. ( 2013)
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observed recordings of the auditory brainstem response in sand fat rats for stimulation on
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soft tissue without recording bone vibrations above the noise level, claiming that bone
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vibrations are not involved in this mode of stimulation, while auditory brainstem response and
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bone vibrations were recorded for stimulation on the bone. In contrast, Ito et al. (2011) were
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able to measure bone vibration for stimulation on soft tissue (eye) in human. The difference
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may come from differences between species or from differences of measurement techniques
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for bone vibrations. While Chordekar et al. (2013) used an LDV, Ito et al. (2011) used an
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accelerometer, which may result in differences of sensitivity and SNR. In our measurements,
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SNR was improved by attaching a retro-reflective foil on the bone and stimulating with supra-
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threshold sound pressure, while Chordekar et al. (2013) stimulated at hearing threshold.
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Intracranial sound pressure affects bone vibrations measured on the promontory only
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marginally. This statement is supported by three of our findings: 1) increases in applied
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contact pressure between the BC transducer and the dura increases intracranial sound
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pressure but does not affect bone vibration; 2) the presence or absence of intracranial fluid
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does not significantly affect bone vibration for stimulation on the dura (DuraStim) while the
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intracranial sound pressure is significantly affected; 3) stimulation on the dura (DuraStim)
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evokes increases in intracranial sound pressure more than does mastoid stimulation
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(MastStim) below 0.5 kHz, but only limited promontory vibration. Stimulation on the mastoid
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(MastStim) evokes intracranial sound pressure as well as promontory vibration for
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frequencies above 0.5 kHz. It is possible that hybrid stimulation may be beneficial in some
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situations.
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Figure 1
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Fig. 1. A simplified scheme of the human head, with corresponding interface boundaries and
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interaction types among all components. Each stimulation type DuraStim (A) and MastStim
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(B) provides stimulation to the inner ear via different BC pathways. Indicated are stimulation
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locations (Dura, Skull) and measured parameters (ICF pressure, Promontory motion) for all
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experiments.
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Fig. 2. Overview of the measurement system (A), experimental setup (B), hydrophone (C)
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and BC transducer (D) location. The measurement system (A) provided a unified user
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interface for control over the excitation signal generation and the data acquisition. The
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experimental setup (B) for each measurement included an LDV, measuring the promontory
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motion, as well as hydrophone in central or temporal position to measure fluid pressure. The
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excitation was provided via a BC transducer (Bonebridge) (D) attached either to the mastoid
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(MastStim) with screws, or placed on the dura (DuraStim) with headband.
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Fig. 3. Variability of promontory motion and intracranial pressure for mastoid stimulation.
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Promontory motion, due to mastoid stimulation (MastStim), shows small variations (i.e., < 5
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dB variation) among all four cadaver heads, while intracranial sound pressure variations are
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larger (i.e., 10 dB variation). The noise floor for each measurement is noted with a
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corresponding dotted line. Data with SNR
