Research ArticleExperimental Analysis of the Mechanism ofHearing under Water

Shai Chordekar1 Liat Kishon-Rabin1 Leonid Kriksunov23

Cahtia Adelman34 and Haim Sohmer5

1Department of Communication Disorders Sackler Faculty of Medicine Tel Aviv University The Chaim Sheba Medical Center52621 Tel Hashomer Israel2Ozen Kashevet Hearing Clinic 6 Ben Maimon Street 92261 Jerusalem Israel3Department of Communication Disorders Hadassah Academic College 37 Haneviim Street PO Box 1114 91010 Jerusalem Israel4Speech amp Hearing Center Hebrew University School of Medicine Hadassah Medical Center Kiryat Hadassah PO Box 1200091120 Jerusalem Israel5Department of Medical Neurobiology (Physiology) Institute for Medical Research Israel-Canada Hebrew UniversityHadassah Medical School PO Box 12272 91120 Jerusalem Israel

Correspondence should be addressed to Haim Sohmer haimsekmdhujiacil

Received 26 August 2015 Revised 11 November 2015 Accepted 24 November 2015

Academic Editor Jareen K Meinzen-Derr

Copyright copy 2015 Shai Chordekar et alThis is an open access article distributed under the Creative Commons Attribution Licensewhich permits unrestricted use distribution and reproduction in any medium provided the original work is properly cited

The mechanism of human hearing under water is debated Some suggest it is by air conduction (AC) others by bone conduction(BC) and others by a combination of AC and BC A clinical bone vibrator applied to soft tissue sites on the head neck and thoraxalso elicits hearing by a mechanism called soft tissue conduction (STC) or nonosseous BC The present study was designed to testwhether underwater hearing at low intensities is by AC or by osseous BC based on bone vibrations or by nonosseous BC (STC)Thresholds of normal hearing participants to bone vibrator stimulation with their forehead in air were recorded and again whenforehead and bone vibrator were under water A vibrometer detected vibrations of a dry human skull in all similar conditions (inair and under water) but not when water was the intermediary between the sound source and the skull forehead Therefore theintensities required to induce vibrations of the dry skull in water were significantly higher than the underwater hearing thresholdsof the participants under conditions when hearing by AC and osseous BC is not likely The results support the hypothesis thathearing under water at low sound intensities may be attributed to nonosseous BC (STC)

1 Introduction

Even though the mammalian ear is adapted mainly for hear-ing in an air environment that is by air conduction (AC)involving the tympanicmembrane and themiddle ear ossicu-lar chain mammals including humans also hear under water[1ndash5] However themechanism responsible for the hearing ofsound inwater is still not clear Some studies support the tym-panic theory which suggests that when under water soundwaves are conducted to the inner ear via the middle ear as inAC hearing [3] That is a passive traveling wave is inducedleading to activation of the outer hair cells [6] Other studiesprovided evidence supporting an osseous bone conduction

(BC)mechanism for underwater hearing in which the soundfield in the water surrounding the head induces skull bonevibrations that are necessary for eliciting BC hearing [1 2 5]These bone vibrations lead to ossicular chain inertia cochlearcompression-distortion cochlear fluid inertia and radiationto the external canal if occluded (occlusion effect) [7] Someresearchers have suggested a dual path theory of underwaterhearing which assumes that both mechanisms AC and BCare involved in underwater hearing [2 3]

Recently further analysis of the mechanisms of BC hasled to the suggestion that during low intensity BC stimulationhearing can result from transmission of sound waves to theinner ear via soft tissue and fluid pathways for example by

Hindawi Publishing CorporationBioMed Research InternationalVolume 2015 Article ID 526708 7 pageshttpdxdoiorg1011552015526708

2 BioMed Research International

delivering vibratory stimulation to sites on the head neckand thorax not overlying skull bone [8ndash10] This mode ofhearing has been referred to as soft tissue conduction (STC)[11] or nonosseous BC [12] and both terms will be used hereinterchangeablyThe sound field in water is actually in initialdirect contact with the skin and other soft tissues (subcuta-neous fat muscle etc) overlying skull bone Therefore therecan be a possible contribution of a nonosseous BC mecha-nism to underwater hearing at low sound levels Since theestablished view of BC is based on the induction of actualvibrations of skull bone [7] the latter mode is called hereosseous BC

The present studywas therefore designed to test the hypo-thesis that underwater hearing at low sound intensities canbe elicited by a mechanism which does not involve osseousBC or AC (ie the external auditory meatus and middle ear)but rather by nonosseous BC For this purpose two com-plementary experiments were conducted and their resultsare compared The first experiment on human subjectswas designed to assess the intensity levels required to elicithearing thresholds under water (while AC hearing is com-promised) and in air The second experiment was designedto assess with a vibrometer the intensity levels required toinduce detectable skull vibrations under water and in airThissecond experimentwas conducted on a dry human skull sinceit has been shown that the presence of soft tissues over andin the skull attenuates skull bone vibrations [13ndash16] so thata dry human skull represents a more sensitive model of thehuman head if vibrations could not be detected on a dryskull then they surely would not be found on an intact headwith overlying attenuating soft tissues

2 Methods and Results

21 Experiment 1 Air and Underwater HearingThresholds of Normal Hearing Participants

211 Participants This experiment was conducted on sixhealthy participants (2 males 4 females) with age rangingbetween 22 and 30 years (mean = 273 SD = 29) All partici-pants had normal hearingAC and BC thresholds 15 dBHL orbetter at frequencies 05 kHz 10 kHz 20 kHz and 40 kHzDuring all experiments the participants were equipped withdeeply inserted earplugs in both ears (Classic Superfit-30Aero Co E-A-R USA) having a 30 dB noise reduction ratingas one of the ways used in this study to reduce the possibilitythat air conducted (AC) sound coming from the bone vibra-tor would excite the ear through the external auditorymeatusand middle ear

The entire experimental protocol was reviewed andapproved by the Tel AvivUniversity Institutional Ethics Com-mittee All participants gave their informed written consentto take part in the study

212 Apparatus A standard clinical B-71 (Radioear) bonevibrator was used as the sound source for assessing BChearing thresholds to forehead stimulation in air and underwater A clinical audiometer (MAICO 41) generated stimuliat 05 kHz 10 kHz 20 kHz and 40 kHz delivered to the bone

vibrator Initially the BC thresholds were assessed with theforehead of the participants in air with the bone vibratorpressed directly to the center of the forehead with anapplication force of 500 gram (approximately 5N) providedby the P3333 Radioear headband as in clinical audiometryIn the underwater stage of the experiment the bone vibratorwas tightly wrapped in a waterproof surgical rubber gloveand then submerged in a water-filled round basin (diameter48 cm height 20 cm with water to a depth of 14 cm) In orderto ensure that the bone vibrator did not touch the walls ofthe basin the bone vibrator was suspended by a string in afixed position at a constant distance from the forehead BCthresholdswhen the forehead was in air and under water wereexpressed in dB HL settings of the audiometer in BC modeHowever the bone vibrator and audiometer in BC mode hadbeen calibrated in accordance with ANSI specification (ANSIS36-2010) for delivering BC stimulation to the skin over themastoid or forehead in the clinic and not for inducing a soundfield when in contact with water Therefore the differencebetween the dB HL settings of the audiometer at threshold inair and under water of the participants was also calculated

213 Procedure Hearing thresholds for all tested conditions(in air and in water) were obtained using an adaptive seekingthreshold procedure following the 5 dB-up 10 dB-down rulesimilar to that used in clinical audiometry The order ofthe tested frequencies was randomized between and withinparticipants

In order to determine underwater thresholds of the par-ticipants the head was tilted so that only the forehead wasimmersed in water and the clinical bone vibrator was sub-merged not touching the foreheadThe forehead was chosenfor immersion because it is the most convenient site to sub-merge while at the same time the eyes nose and the externalears (equipped with earplugs) of the tilted head were stillabove water The nose in air also enabled the participantsto breath normally The center of the segment of the fore-head under water was the same site to which bone vibra-tor had been pressed (with 5N force) in air The participantsimmersed their forehead by tilting their head into the basinof water while the back of the head (inion) and the top of thehead (parietal region) remained in air As the forehead wasgradually immersed in the water the participants reportedthat the loudness of the sound gradually increased reaching amaximum at a particular depth Loudness sensation reachedmaximum when the forehead was about 4-5 cm under waterat which time the diameter of the segment of the immersedforehead was about 8 cm and the forehead in water was13 cm from the submerged bone vibratorThis latter conditionwas the one used for the remainder of this experiment Thehearing thresholds of the participants were also assessed atthe same frequencies using an ldquoin air controlrdquo that is with theforehead lifted from the water into air 2 cm above the surfaceof the water while the bone vibrator remained in water Thiswas done in order to further confirm that participants werenot responding to air conducted sounds coming from thebone vibrator in water by AC hearing through the externalauditory canals in air (even though they were equipped withearplugs)

BioMed Research International 3

0

10

20

30

40

50

60

70

80

500 1000 2000 4000

Mea

n th

resh

old

(dB

HL)

Frequency (Hz)

Figure 1Mean (plusmnSD) intensities eliciting threshold of normal hear-ing participants in the following conditions [e] bone vibrator inwater forehead in air [I] bone vibrator and forehead under waternot touching [998771] bone vibrator directly on forehead both in air

In order to avoid order effects testing conditions wererandomized between participants The tests were conductedat least twice for each condition to ensure repeatability

Results Experiment 1 Thresholds The mean (and standarddeviation) thresholds of the same participants in air andunder water are shown in Figure 1 It can be seen thatbetter (ie lower) thresholds (mean 8ndash13 dB HL dependingon frequency) were obtained when the bone vibrator wasdirectly applied to the forehead in air with a force of about5N Higher thresholds (33ndash50 dB HL) were obtained underwater when water was the intervening medium between thebone vibrator and the forehead 13 cm apart The differencebetween these underwater-air thresholds ranged from 24to 42 dB depending on frequency Even higher (poorer)thresholds (60ndash70 dB HL) were obtained in the controlprocedure in which the head with earplugs was just abovethe water while bone vibrator was still under water A 2-way repeated measures ANOVA separating main effects oftest condition and frequency confirmed these observations[119865(1 71) = 737927 119901 lt 0001 119865(3 71) = 8566 119901 = 0001resp] Pairwise multiple comparisons (Tukey test) found asignificant difference between all tested conditions (119901 lt0001) Also a significant interaction between frequency andtest condition was found [119865(6 71) = 7605 119901 lt 0001] Thesignificant interaction resulted from better threshold at10 kHz in the underwater condition (119901 lt 0001)

22 Experiment 2 Dry Skull Vibrations in Air and underWater In order to assess the intensity levels of the stimuliwhich induce skull bone vibrations the vibrations of a dryskull were measured using a Laser Doppler Vibrometer(LDV) in the two conditions similar to those in experiment 1on the live participants that is when the bone vibrator andskull were both in water and when the bone vibrator wasdirectly applied with 5N force to the skull forehead in air

221 Apparatus The vibration measurements were con-ducted on a dry adult skull using a LDV VibroMet model

500V single point vibrometer (MetroLaser Inc Irvine CAUSA) with a frequency range DC to 70 kHz velocity range2 120583ms to 1ms Recordings were conducted using theMetro-lab software with a sampling rate of 40 kHz and frequencyresolution of 10Hz To improve the signal-to-noise ratio eachmeasurement was averaged 100 times at each stimulationfrequency and the noise floorwas carefullymonitored duringthe entire procedure In order to enhance laser beam reflec-tion and reduce the noise floor aluminum foil reflecting tapewas pasted to all target areas and the laser beam was focusedon this reflector A clinical audiometer (Interacoustics AC-33) was used in order to generate stimuli at 05 kHz 10 kHz20 kHz and 40 kHz delivered to a B-71 (radio ear) bonevibrator

222 Sensitivity Validation of the LDVSystem Thesensitivityof the LDV system was initially assessed by focusing the laserbeam directly on a reflector applied to the center of the bonevibrator without any application force that is ldquounloadedrdquoAssessing the sensitivity of the vibrometer on the unloadedbone vibrator would provide its optimal sensitivity sinceloading (pressing) the bone vibrator onto some surface (egthe forehead) would reduce the vibrations and lead to anelevation of the intensity required to elicit them Vibrations ofthe bone vibrator were assessed for the same four frequenciesin order to determine the lowest vibration velocity whichcould be detected by the LDV and the stimulus intensityrequired to induce it The LDV detected vibrations at thesame four frequencies directly on the bone vibrator with amagnitude ranging from 002 to 005mmsec at 0 dB HLThe noise floor in these measurements was 8 to 12 120583msecdepending on frequency and all were recorded with a signal-to-noise ratio (SNR) of at least 6 dB

223 Procedure The vibrations of the dry skull were mea-sured when it was entirely in air and the bone vibratorwas applied to the forehead of the skull using the standardbone vibrator headband (direct application force equivalentto approximately 5N) as during the hearing thresholddeterminations of the participants in experiment 1 The skullwas placed on a spongy surface to avoid sound and vibrationreflection from the table to the skull when delivering boneconduction stimuli to the skull The LDV laser beam wasfocused at a reflector pasted on the back of the skull (inion-occipital protuberance) perpendicular to the surface of theskull and pure-tones were delivered by the bone vibrator

Skull bone vibrations under water were assessed underthe same conditions as in experiment 1 in which humanthresholds were determined (ie skull suspended tiltedfrom above skull forehead under water inion in air samewater-protected bone vibrator under water at a distance of13 cm from the tilted skull forehead under water stimulidelivered by the bone vibrator under water LDV laser beamfocused to the inion of the skull in air and LDV measuringskull vibrations at that site) In addition vibrations were alsoassessed with the LDV beam focused on the parietal regionof the skull which was also still in air above the water butmuch closer to the surface of the water than the assessmentat the inion The top of the parietal region of the skull is

4 BioMed Research International

perpendicular to a line between the forehead and the inionFurthermore to confirm that the LDV could indeed measureskull vibrations induced under water LDV recordings wereconducted while the bone vibrator was manually pressed indirect underwater contact with the forehead of the immersedskull In this latter condition 13 cm of water no longerintervened between the sound source in the water and theskull forehead in water and the LDV beam was directed tothe inion LDV recordings were conducted at least two timesfor each condition to confirm repeatability Throughout allmeasurements in air and in water vibrations were assessedwhen the stimulus intensities delivered began with the maxi-mumoutput of the audiometer at each frequency down to thelowest intensity at which bone vibrations could still be clearlydetected by the LDV Throughout all LDV measurements(directly on the bone vibrator and on the skull both in airand in water) the noise floor was consistently between 8 to12 120583msec and the signal-to-noise ratio was at least 6 dB

Results Experiment 2 Skull VibrationsThe magnitude of thevibrations of the skull (expressed as velocity mmsec) wasmeasured by the LDV at the inion of the skull (in air) inresponse to stimulation by the bone vibrator pressed directlyto the forehead (in air) with an application force of approx-imately 5N (headband) The lowest stimulus intensities atwhich vibrations could be detected (6 dB above the noisefloor) on the skull in air were 10 dB HL at 05 kHz 30 dB HLat 10 kHz 20 dB HL at 20 kHz and 25 dB HL at 40 kHzAt lower intensities the LDV could not detect any vibrationsabove the noise floor (which was 8 to 12 120583msec dependingon frequency) The magnitude of the vibrations increasedlinearly with stimulus intensity at each frequency reachinghighest levels at the maximal output of the audiometer

When the forehead of the skull was suspended fromabove in the water basin with the bone vibrator also in water13 cm distant bone vibrations above the noise floor weredetected only at 10 kHz and then only at 65ndash70 dB HL (themaximumoutput of the audiometer at 10 kHzwas 70 dBHL)At all other frequencies and intensities vibrations could notbe detected above the noise floor (8 to 12120583msec) even atmaximum output of the audiometer (which was 60 dB HLat 05 kHz 70 dB HL at 20 kHz and 80 dB HL at 40 kHz)Similar results (absence of vibrations with forehead underwater at 05 kHz 20 kHz and 40 kHz present at 10 kHzbut only at maximum intensities) were obtained when theLDV was focused at the top of the parietal region in airabove water Bone vibrations were also determined whenthe bone vibrator in the water bath was manually pressedin direct contact with the forehead of the immersed tiltedskull without intervening water In that situation vibrationswere clearly detected at the inion in air by the LDV with thesame order of magnitude as those seen when the skull wasin air with the bone vibrator applied to the forehead with theheadband

3 Discussion

The present study was designed to test the hypothesis thatunderwater hearing is elicited by a nonosseous BC (STC)mechanism and not by AC and not by osseous BC This

was achieved by determining the thresholds of normal partic-ipants in air and under water (experiment 1) and comparingthem to theminimal intensities required to induce skull bonevibrations in air and under water (experiment 2)

31 Absence of AC Hearing under Water Several aspects ofthe experimental design confirm that AC hearing was notinvolved the ears were occluded by earplugs having a noisereduction rating (NRR) of 30 dB the external ear canals of theparticipants were above water while the sound source wasunder water Since there is a large difference in the acousticimpedances of air and of water the sound pressures inducedby the bone vibrator in water would be largely reflected atits boundary with air and therefore not transmitted to theair above [17ndash19] Furthermore when the forehead of theparticipants was just above the surface of the water and thebone vibrator was still submerged in water (in air control)the thresholds were even higher compared to the condition inwhich the bone vibrator and forehead were both submergedin water but not touching

32 Absence of Osseous BC Hearing under Water When thebone vibrator was pressed to the forehead of the skull directlywith a 5N force in air the lowest intensities at which skullvibrationswere clearly detected at the inion and at the parietalregionwere 10 to 30 dBHL (depending on frequency) On theother hand the thresholds of the participants obtained whentheir foreheads and the bone vibrator were both under waterabout 13 cm apart were 24 to 42 dB (depending on frequency)higher than the thresholds obtained when the bone vibratorwas pressed in air directly to the forehead of the participantswith a 5N force (experiment 1) Note that in the underwatercondition water served as the intermediary between thebone vibrator and the skull and vibrations were detected atthe inion only at 10 kHz and then only at the maximumoutput at that frequency (65 to 70 dB HL) No vibrationswere detected at the other frequencies even at the maximumintensities available However when the bone vibrator waspressed under water directly to the skull forehead (withoutwater serving as the intermediary) vibrations were detectedat the same frequencies and intensities as those obtainedwhen the bone vibrator was applied to the forehead in air

In both underwater parts of the experiments (thresholdsof participants and skull vibrations) the test conditions forthe determination of human thresholds and the assessmentof dry skull vibrations were identical the same water baththe same bone vibrator wrapped with the same rubber glovethe immersion of the forehead in the same position the bonevibrator in contact with water and the same distance (13 cm)between the forehead and the submerged bone vibratorTherefore results of these two experiments can be comparedand it was seen that the thresholds of the participants underwater were much lower than the dB HL settings required forinduction of vibrations at the inion of the skull in air while theskull forehead was under water However the BC thresholdsof the participants with their forehead under water expressedin dB HL audiometer settings in BCmode of the audiometercould not be directly compared to those when the bonevibrator was pressed (5N) to the forehead in air This is due

BioMed Research International 5

01020304050607080

500 1000 2000 4000

Inte

nsity

diff

eren

ce (d

B)

Frequency (Hz)

Behavioral threshold differences in air and under waterVibration detection level differences in air and under water

Figure 2 Bar graphs showing the air-underwater intensity differ-ences in dB which elicited threshold in normal participants andwhich induced vibrations of skull bone at the 4 stimulus frequenciesSince the intensities delivered under water to the skull at 05 20and 40 kHz even at the maximum output of the audiometer didnot induce skull vibrations the maximal output was used in thecalculation of the intensity differences for skull vibration with anupward pointing arrow to indicate that the intensity differences atthese frequencies were even greater For 10 kHz the intensity usedin this calculation is that which induced skull vibrations

to the audiometer and bone vibrator having been calibratedfor BC stimulation when pressed to head sites (mastoid orforehead) and not for inducing a sound field in water Themechanical impedances of the forehead and that of water arevery different However this limitation can be overcome bycomparing in addition the air-water threshold differences tothe air-water intensity differences required to induce skullbone vibrations If one assumes that only an osseous BCmechanism was involved in underwater hearing then thedifference between the intensity levels in air compared to thatunder water between experiments 1 (thresholds) and 2 (vibra-tions) would have been similar In other words if in bothexperiments only an osseous BC mechanism was involvedin underwater hearing then the same difference (between inair and under water see Figure 2) would have been expectedin experiments 1 and 2 However as shown in Figure 2 alarger difference was found in experiment 2 (skull vibrations)than in experiment 1 (threshold of participants) suggestingthe involvement of a different physiological mechanism ineach of the two experiments In fact the exact differencewith respect to the skull vibrations under water could noteven be directly calculated for 05 20 and 40 kHz since novibrations were detected at these frequencies on the inion ofthe skull when the skull forehead was under water even withstimulation at the maximum output level of the audiometerVibrations on the skull under water were detected only at10 kHz at 65ndash70 dB HL Therefore in Figure 2 at the otherfrequencies at which skull vibrations were not detected themaximum output of the audiometer was used for calculationof the intensity difference shown in the bar graph Anarrow pointing upward indicates that the intensity differencesrequired for eliciting skull vibrations at these frequencieswere

even greater As can be clearly seen in Figure 2 the intensitydifferences between those in air and in water required toinduce skull bone vibrations were much greater than thoseneeded to elicit threshold in the participants

The possibility that the LDV system was not sensitiveenough to detect vibrations of bone induced by the soundfield in water at 05 20 and 40 kHz is refuted by severalfindings Among these vibrations at 0 dB HL were detectedby the LDV at these frequencies when focused directly onthe bone vibrator under optimal conditions (bone vibratorunloaded) for sensitivity assessment of the vibrometer (seeMethods experiment 2 sensitivity) In addition the LDVwas able to detect skull vibrations at the inion in air at thesefrequencies only when the stimuli were delivered by thebone vibrator applied in direct contact and pressed to theforehead in air using the headband Skull vibrations werealso detected by the LDV on the inion of the skull in air atthese frequencies when the skull was tilted in water and thebone vibrator was pressed in direct contact under water tothe forehead In this situation water was not serving as theintermediary between the sound field in water and the softtissues over the bone at the forehead Also the noise floorduring all LDV measurements was 10 to 11120583msec and aSNR of at least 6 dB was considered as the criterion for thepresence of vibrations On the other hand the only situationat which the LDV did not detect vibrations of the skull atthe inion and parietal region at 05 20 and 40 kHz evenat the maximum output in air at this SNR was when waterserved as the intervening medium between the bone vibratorand the skull forehead 13 cm apart When water served asthe intervening medium vibrations were detected only at10 kHz but only at maximum output (65 and 70 dB HL)These findings lead to the suggestion that the sound fieldintensities induced by the bone vibrator in water at 05 20and 40 kHz (and at 10 kHz at intensities below 65ndash70 dBHL) were insufficient to induce skull bone vibrations Thistogether with the fact that our participants were able to hear(threshold) sounds under water at intensities below thosewhich induce skull bone vibrations leads to the suggestionthat other sound transmitting mechanisms (eg nonosseousBC) are likely involved at low sound intensities Osseous BCmay be involved in underwater hearing at higher stimulusintensities at sites on the head overlying bone (foreheadinion)

33 Nonosseous BC (STC) in Underwater Hearing at LowIntensities The results of the present study therefore do notsupport the involvement of AC nor of osseous BC (at leastnot at low sound intensities) in underwater hearing Since thesound field in water was actually in direct contact with theskin and the underlying additional soft tissues (muscle adi-pose tissue connective tissue etc of the forehead) overlyingskull bone it is suggested therefore that nonosseous BC canbe considered an alternative mechanism for hearing in suchconditions without inducing skull vibrations that is withoutosseous BC [12] In this mechanism the sound field inducedin the water can elicit vibrations in the soft tissues (STC) [11]since water and each of the soft tissues have similar acousticimpedances (defined as the product of the density of each

6 BioMed Research International

tissue and the velocity of sound in that tissue the acousticimpedance of water = 152 times 106 kgm2 sec and of typical softtissues = 162 times 106 kgm2 sec) Therefore acoustic frequencyvibrations can be transmitted from thewater to the soft tissuesof the body (similar to that during ultrasound diagnosticimaging [18]) to the inner ear fluids [17ndash19] Thus as a resultof the similarity of acoustic impedances between water andthe soft tissues of the head the sound field pressure waves inwater would be transmitted to the soft tissues and from thereto the inner ear (ie low threshold stimulation by nonosseousBC-STC) Moreover as the intensity of the sound field inwater is gradually increased beginning at very low levels forexample during threshold determinations the nonosseousBC (STC) threshold would be reached at a lower intensitythan the osseous BC threshold On the other hand whenthe acoustic impedances of adjacent tissues are very differentfrom each other for example skin or soft tissue to bone (theacoustic impedance of bone = 78times 106 kgm2 sec)most of thevibratory energy (60ndash69) would be reflected at the water-bone interface and not transmitted [17ndash19] and would notinduce skull vibrations (osseous BC) at low intensities Thusdue to the large differences in acoustic impedance betweenwater and bone the sound field in water and soft tissues atlow intensities would be reflected at the bone and would notinduce skull bone vibrations so that osseous BC thresholdswould be elevated Thus it is not likely that the sound fieldinduced in water at threshold intensities would be able toinduce vibrations of skull bone This is similar to the consid-erations of the transmission of sound vibrations from an airenvironment in the external ear to the fluid environment inthe inner ear where the transmission loss is reduced by theimpedance matching functions of the middle ear (tympanicmembranestapes footplate area and lever ratios) [17 19]Furthermore the presence of soft tissues overlying andwithinthe skull actually attenuates the sound levels reaching thebone by about 20 dB [13ndash16] (such attenuation has also beenshown when the magnitude of bone vibrations was evaluatedwith single point LDVs [15 16]) This is likely a result ofthe differences in acoustic impedance between that of softtissues and the underlying bone so that a dry skull may beconsidered to provide a more sensitive measure of possibleskull bone vibrations If vibrations could not be detected on adry skull then they would surely not be detected on an intacthead The finding however that our participants (humanhead with soft tissues) reported threshold hearing at lowerintensities than those required to induce skull vibrationssupports the hypothesis that vibrations in the water and softtissues which did not induce skull bone vibrations at mostfrequencies were nevertheless transmitted via nonosseous(STC) BC to the inner ear

Additional support for a nonosseous BC (STC) mecha-nism can be derived from recent studies showing that hearingsensations can be elicited when the bone vibrator is appliedto water or gel on the skin without any real contact or appli-cation force similar to the situation in underwater hearing[20] Similarly it has been suggested that a major part of thepathway for the transmission of water borne sounds to theinner ear of dolphins and other marine mammals when theyare totally under water is through a soft tissue conduction

pathway In the dolphin this pathway is a fat filled channel inthe mandible [21]

This nonosseous-soft tissue mechanism for underwaterhearingmay also explain the hearing of the 20weeks gestationfetus The fetus is completely enveloped in amniotic fluidwith a softer skull and wider sutures between the skull bonesconditions in which actual skull vibrations (osseous BC) arenot likely Nonosseous BC (STC) therefore probably plays asignificant role in hearing in a fluid environment at thresholdlevels

4 Conclusion

It seems that underwater hearing at low sound intensities ismediated by a nonosseous BC (STC) mechanism At higherintensities there is likely a transition to osseous BC mecha-nisms which involves actual skull bone vibrations

Conflict of Interests

The authors declare that there is no conflict of interestsregarding the publication of this paper

Acknowledgments

The authors wish to express their sincere gratitude to thephysicist Benjamin Gavish PhD for his assistance to thestudy The intensive in-depth discussions with him con-tributed greatly to the interpretation of the results especiallyconcerning the nature of the energy interactions at the inter-face between water or soft tissues with bone Ronen PerezMD otologist provided input to the planning of the studyThe authors wish to thank Vocalzoom Systems Israel forallowing use of their Laser Doppler Vibrometer

References

[1] H Hollien and S Feinstein ldquoContribution of the externalauditory meatus to auditory sensitivity underwaterrdquo Journal ofthe Acoustical Society of America vol 57 no 6 pp 1488ndash14921975

[2] A Shupak Z Sharoni Y Yanir Y Keynan Y Alfie and P Halp-ern ldquoUnderwater hearing and sound localization with andwithout an air interfacerdquo Otology amp Neurotology vol 26 no 1pp 127ndash130 2005

[3] H W Pau M Warkentin O Specht H Krentz A Herrmannand K Ehrt ldquoExperiments on the mechanism of underwaterhearingrdquoActa Oto-Laryngologica vol 131 no 12 pp 1279ndash12852011

[4] M K Qin D Schwaller M Babina and E Cudahy ldquoHumanunderwater and bone conduction hearing in the sonic andultrasonic rangerdquoThe Journal of the Acoustical Society of Amer-ica vol 129 no 4 article 2485 2011

[5] J F Brandt and H Hollien ldquoUnderwater hearing thresholds inmanrdquo Journal of the Acoustical Society of America vol 42 no 5pp 966ndash971 1967

[6] J S Oghalai ldquoThe cochlear amplifier augmentation of the trav-eling wave within the inner earrdquo Current Opinion in Otolaryn-gology amp Head and Neck Surgery vol 12 no 5 pp 431ndash4382004

BioMed Research International 7

[7] S Stenfelt ldquoAcoustic and physiologic aspects of bone conduc-tion hearingrdquo Advances in Oto-Rhino-Laryngology vol 71 pp10ndash21 2011

[8] S Freeman J-Y Sichel and H Sohmer ldquoBone conductionexperiments in animalsmdashevidence for a non-osseous mecha-nismrdquo Hearing Research vol 146 no 1-2 pp 72ndash80 2000

[9] T Ito C Roosli C J Kim J H Sim AMHuber and R ProbstldquoBone conduction thresholds and skull vibration measured onthe teeth during stimulation at different sites on the humanheadrdquo Audiology and Neurotology vol 16 no 1 pp 12ndash22 2010

[10] T Watanabe S Bertoli and R Probst ldquoTransmission pathwaysof vibratory stimulation as measured by subjective thresholdsand distortion-product otoacoustic emissionsrdquo Ear and Hear-ing vol 29 no 5 pp 667ndash673 2008

[11] C Adelman M Kaufmann Yehezkely S Chordekar and HSohmer ldquoRelation between body structure and hearing duringsoft tissue auditory stimulationrdquoBioMedResearch Internationalvol 2015 Article ID 172026 6 pages 2015

[12] B A Vento and J D Durrant ldquoAssessing bone conductionthresholds in clinical practicerdquo in Handbook of Clinical Audi-ology J Katz R Burkard L Hood and L Medwetsky EdsLippincott Williams amp Wilkins Baltimore Md USA 6thedition 2009

[13] A Tjellstrom B Hakansson J Lindstrom et al ldquoAnalysis of themechanical impedance of bone-anchored hearing aidsrdquo ActaOto-Laryngologica vol 89 no 1-2 pp 85ndash92 1980

[14] B Hakansson A Tjellstrom and U Rosenhall ldquoAccelerationlevels at hearing threshold with direct bone conduction versusconventional bone conductionrdquo Acta Oto-Laryngologica vol100 no 3-4 pp 240ndash252 1985

[15] M Eeg-Olofsson S Stenfelt H Taghavi et al ldquoTransmission ofbone conducted soundmdashcorrelation between hearing percep-tion and cochlear vibrationrdquo Hearing Research vol 306 pp 11ndash20 2013

[16] J K Mattingly N T Greene H A Jenkins D J Tollin J REaster and S P Cass ldquoEffects of skin thickness on cochlearinput signal using transcutaneous bone conduction implantsrdquoOtology amp Neurotology vol 36 no 8 pp 1403ndash1411 2015

[17] E G Wever and M Lawrence ldquoThe function of the middleearrdquo in Physiological Acoustics pp 69ndash78 Princeton UniversityPress Princeton NJ USA 1954

[18] J Baun Physical Principles of General and Vascular SonographyCalifornia Publishing San Fransisco Calif USA 2004

[19] B W Blakley and S Siddique ldquoA qualitative explanation of theWeber testrdquo OtolaryngologymdashHead and Neck Surgery vol 120no 1 pp 1ndash4 1999

[20] M Geal-Dor S Chordekar C Adelman andH Sohmer ldquoBoneconduction thresholds without bone vibrator application forcerdquoJournal of the American Academy of Audiology vol 26 no 7 pp645ndash651 2015

[21] S Hemila S Nummela and T Reuter ldquoAnatomy and physicsof the exceptional sensitivity of dolphin hearing (OdontocetiCetacea)rdquo Journal of Comparative Physiology A NeuroethologySensory Neural and Behavioral Physiology vol 196 no 3 pp165ndash179 2010

Submit your manuscripts athttpwwwhindawicom

Stem CellsInternational

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

MEDIATORSINFLAMMATION

of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Behavioural Neurology

EndocrinologyInternational Journal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Disease Markers

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

BioMed Research International

OncologyJournal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Oxidative Medicine and Cellular Longevity

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PPAR Research

The Scientific World JournalHindawi Publishing Corporation httpwwwhindawicom Volume 2014

Immunology ResearchHindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Journal of

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Research and TreatmentAIDS

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Parkinsonrsquos Disease

Evidence-Based Complementary and Alternative Medicine

Volume 2014Hindawi Publishing Corporationhttpwwwhindawicom

2 BioMed Research International

delivering vibratory stimulation to sites on the head neckand thorax not overlying skull bone [8ndash10] This mode ofhearing has been referred to as soft tissue conduction (STC)[11] or nonosseous BC [12] and both terms will be used hereinterchangeablyThe sound field in water is actually in initialdirect contact with the skin and other soft tissues (subcuta-neous fat muscle etc) overlying skull bone Therefore therecan be a possible contribution of a nonosseous BC mecha-nism to underwater hearing at low sound levels Since theestablished view of BC is based on the induction of actualvibrations of skull bone [7] the latter mode is called hereosseous BC

The present studywas therefore designed to test the hypo-thesis that underwater hearing at low sound intensities canbe elicited by a mechanism which does not involve osseousBC or AC (ie the external auditory meatus and middle ear)but rather by nonosseous BC For this purpose two com-plementary experiments were conducted and their resultsare compared The first experiment on human subjectswas designed to assess the intensity levels required to elicithearing thresholds under water (while AC hearing is com-promised) and in air The second experiment was designedto assess with a vibrometer the intensity levels required toinduce detectable skull vibrations under water and in airThissecond experimentwas conducted on a dry human skull sinceit has been shown that the presence of soft tissues over andin the skull attenuates skull bone vibrations [13ndash16] so thata dry human skull represents a more sensitive model of thehuman head if vibrations could not be detected on a dryskull then they surely would not be found on an intact headwith overlying attenuating soft tissues

2 Methods and Results

21 Experiment 1 Air and Underwater HearingThresholds of Normal Hearing Participants

211 Participants This experiment was conducted on sixhealthy participants (2 males 4 females) with age rangingbetween 22 and 30 years (mean = 273 SD = 29) All partici-pants had normal hearingAC and BC thresholds 15 dBHL orbetter at frequencies 05 kHz 10 kHz 20 kHz and 40 kHzDuring all experiments the participants were equipped withdeeply inserted earplugs in both ears (Classic Superfit-30Aero Co E-A-R USA) having a 30 dB noise reduction ratingas one of the ways used in this study to reduce the possibilitythat air conducted (AC) sound coming from the bone vibra-tor would excite the ear through the external auditorymeatusand middle ear

The entire experimental protocol was reviewed andapproved by the Tel AvivUniversity Institutional Ethics Com-mittee All participants gave their informed written consentto take part in the study

212 Apparatus A standard clinical B-71 (Radioear) bonevibrator was used as the sound source for assessing BChearing thresholds to forehead stimulation in air and underwater A clinical audiometer (MAICO 41) generated stimuliat 05 kHz 10 kHz 20 kHz and 40 kHz delivered to the bone

vibrator Initially the BC thresholds were assessed with theforehead of the participants in air with the bone vibratorpressed directly to the center of the forehead with anapplication force of 500 gram (approximately 5N) providedby the P3333 Radioear headband as in clinical audiometryIn the underwater stage of the experiment the bone vibratorwas tightly wrapped in a waterproof surgical rubber gloveand then submerged in a water-filled round basin (diameter48 cm height 20 cm with water to a depth of 14 cm) In orderto ensure that the bone vibrator did not touch the walls ofthe basin the bone vibrator was suspended by a string in afixed position at a constant distance from the forehead BCthresholdswhen the forehead was in air and under water wereexpressed in dB HL settings of the audiometer in BC modeHowever the bone vibrator and audiometer in BC mode hadbeen calibrated in accordance with ANSI specification (ANSIS36-2010) for delivering BC stimulation to the skin over themastoid or forehead in the clinic and not for inducing a soundfield when in contact with water Therefore the differencebetween the dB HL settings of the audiometer at threshold inair and under water of the participants was also calculated

213 Procedure Hearing thresholds for all tested conditions(in air and in water) were obtained using an adaptive seekingthreshold procedure following the 5 dB-up 10 dB-down rulesimilar to that used in clinical audiometry The order ofthe tested frequencies was randomized between and withinparticipants

In order to determine underwater thresholds of the par-ticipants the head was tilted so that only the forehead wasimmersed in water and the clinical bone vibrator was sub-merged not touching the foreheadThe forehead was chosenfor immersion because it is the most convenient site to sub-merge while at the same time the eyes nose and the externalears (equipped with earplugs) of the tilted head were stillabove water The nose in air also enabled the participantsto breath normally The center of the segment of the fore-head under water was the same site to which bone vibra-tor had been pressed (with 5N force) in air The participantsimmersed their forehead by tilting their head into the basinof water while the back of the head (inion) and the top of thehead (parietal region) remained in air As the forehead wasgradually immersed in the water the participants reportedthat the loudness of the sound gradually increased reaching amaximum at a particular depth Loudness sensation reachedmaximum when the forehead was about 4-5 cm under waterat which time the diameter of the segment of the immersedforehead was about 8 cm and the forehead in water was13 cm from the submerged bone vibratorThis latter conditionwas the one used for the remainder of this experiment Thehearing thresholds of the participants were also assessed atthe same frequencies using an ldquoin air controlrdquo that is with theforehead lifted from the water into air 2 cm above the surfaceof the water while the bone vibrator remained in water Thiswas done in order to further confirm that participants werenot responding to air conducted sounds coming from thebone vibrator in water by AC hearing through the externalauditory canals in air (even though they were equipped withearplugs)

BioMed Research International 3

0

10

20

30

40

50

60

70

80

500 1000 2000 4000

Mea

n th

resh

old

(dB

HL)

Frequency (Hz)

Figure 1Mean (plusmnSD) intensities eliciting threshold of normal hear-ing participants in the following conditions [e] bone vibrator inwater forehead in air [I] bone vibrator and forehead under waternot touching [998771] bone vibrator directly on forehead both in air

In order to avoid order effects testing conditions wererandomized between participants The tests were conductedat least twice for each condition to ensure repeatability

Results Experiment 1 Thresholds The mean (and standarddeviation) thresholds of the same participants in air andunder water are shown in Figure 1 It can be seen thatbetter (ie lower) thresholds (mean 8ndash13 dB HL dependingon frequency) were obtained when the bone vibrator wasdirectly applied to the forehead in air with a force of about5N Higher thresholds (33ndash50 dB HL) were obtained underwater when water was the intervening medium between thebone vibrator and the forehead 13 cm apart The differencebetween these underwater-air thresholds ranged from 24to 42 dB depending on frequency Even higher (poorer)thresholds (60ndash70 dB HL) were obtained in the controlprocedure in which the head with earplugs was just abovethe water while bone vibrator was still under water A 2-way repeated measures ANOVA separating main effects oftest condition and frequency confirmed these observations[119865(1 71) = 737927 119901 lt 0001 119865(3 71) = 8566 119901 = 0001resp] Pairwise multiple comparisons (Tukey test) found asignificant difference between all tested conditions (119901 lt0001) Also a significant interaction between frequency andtest condition was found [119865(6 71) = 7605 119901 lt 0001] Thesignificant interaction resulted from better threshold at10 kHz in the underwater condition (119901 lt 0001)

22 Experiment 2 Dry Skull Vibrations in Air and underWater In order to assess the intensity levels of the stimuliwhich induce skull bone vibrations the vibrations of a dryskull were measured using a Laser Doppler Vibrometer(LDV) in the two conditions similar to those in experiment 1on the live participants that is when the bone vibrator andskull were both in water and when the bone vibrator wasdirectly applied with 5N force to the skull forehead in air

221 Apparatus The vibration measurements were con-ducted on a dry adult skull using a LDV VibroMet model

500V single point vibrometer (MetroLaser Inc Irvine CAUSA) with a frequency range DC to 70 kHz velocity range2 120583ms to 1ms Recordings were conducted using theMetro-lab software with a sampling rate of 40 kHz and frequencyresolution of 10Hz To improve the signal-to-noise ratio eachmeasurement was averaged 100 times at each stimulationfrequency and the noise floorwas carefullymonitored duringthe entire procedure In order to enhance laser beam reflec-tion and reduce the noise floor aluminum foil reflecting tapewas pasted to all target areas and the laser beam was focusedon this reflector A clinical audiometer (Interacoustics AC-33) was used in order to generate stimuli at 05 kHz 10 kHz20 kHz and 40 kHz delivered to a B-71 (radio ear) bonevibrator

222 Sensitivity Validation of the LDVSystem Thesensitivityof the LDV system was initially assessed by focusing the laserbeam directly on a reflector applied to the center of the bonevibrator without any application force that is ldquounloadedrdquoAssessing the sensitivity of the vibrometer on the unloadedbone vibrator would provide its optimal sensitivity sinceloading (pressing) the bone vibrator onto some surface (egthe forehead) would reduce the vibrations and lead to anelevation of the intensity required to elicit them Vibrations ofthe bone vibrator were assessed for the same four frequenciesin order to determine the lowest vibration velocity whichcould be detected by the LDV and the stimulus intensityrequired to induce it The LDV detected vibrations at thesame four frequencies directly on the bone vibrator with amagnitude ranging from 002 to 005mmsec at 0 dB HLThe noise floor in these measurements was 8 to 12 120583msecdepending on frequency and all were recorded with a signal-to-noise ratio (SNR) of at least 6 dB

223 Procedure The vibrations of the dry skull were mea-sured when it was entirely in air and the bone vibratorwas applied to the forehead of the skull using the standardbone vibrator headband (direct application force equivalentto approximately 5N) as during the hearing thresholddeterminations of the participants in experiment 1 The skullwas placed on a spongy surface to avoid sound and vibrationreflection from the table to the skull when delivering boneconduction stimuli to the skull The LDV laser beam wasfocused at a reflector pasted on the back of the skull (inion-occipital protuberance) perpendicular to the surface of theskull and pure-tones were delivered by the bone vibrator

Skull bone vibrations under water were assessed underthe same conditions as in experiment 1 in which humanthresholds were determined (ie skull suspended tiltedfrom above skull forehead under water inion in air samewater-protected bone vibrator under water at a distance of13 cm from the tilted skull forehead under water stimulidelivered by the bone vibrator under water LDV laser beamfocused to the inion of the skull in air and LDV measuringskull vibrations at that site) In addition vibrations were alsoassessed with the LDV beam focused on the parietal regionof the skull which was also still in air above the water butmuch closer to the surface of the water than the assessmentat the inion The top of the parietal region of the skull is

4 BioMed Research International

perpendicular to a line between the forehead and the inionFurthermore to confirm that the LDV could indeed measureskull vibrations induced under water LDV recordings wereconducted while the bone vibrator was manually pressed indirect underwater contact with the forehead of the immersedskull In this latter condition 13 cm of water no longerintervened between the sound source in the water and theskull forehead in water and the LDV beam was directed tothe inion LDV recordings were conducted at least two timesfor each condition to confirm repeatability Throughout allmeasurements in air and in water vibrations were assessedwhen the stimulus intensities delivered began with the maxi-mumoutput of the audiometer at each frequency down to thelowest intensity at which bone vibrations could still be clearlydetected by the LDV Throughout all LDV measurements(directly on the bone vibrator and on the skull both in airand in water) the noise floor was consistently between 8 to12 120583msec and the signal-to-noise ratio was at least 6 dB

Results Experiment 2 Skull VibrationsThe magnitude of thevibrations of the skull (expressed as velocity mmsec) wasmeasured by the LDV at the inion of the skull (in air) inresponse to stimulation by the bone vibrator pressed directlyto the forehead (in air) with an application force of approx-imately 5N (headband) The lowest stimulus intensities atwhich vibrations could be detected (6 dB above the noisefloor) on the skull in air were 10 dB HL at 05 kHz 30 dB HLat 10 kHz 20 dB HL at 20 kHz and 25 dB HL at 40 kHzAt lower intensities the LDV could not detect any vibrationsabove the noise floor (which was 8 to 12 120583msec dependingon frequency) The magnitude of the vibrations increasedlinearly with stimulus intensity at each frequency reachinghighest levels at the maximal output of the audiometer

When the forehead of the skull was suspended fromabove in the water basin with the bone vibrator also in water13 cm distant bone vibrations above the noise floor weredetected only at 10 kHz and then only at 65ndash70 dB HL (themaximumoutput of the audiometer at 10 kHzwas 70 dBHL)At all other frequencies and intensities vibrations could notbe detected above the noise floor (8 to 12120583msec) even atmaximum output of the audiometer (which was 60 dB HLat 05 kHz 70 dB HL at 20 kHz and 80 dB HL at 40 kHz)Similar results (absence of vibrations with forehead underwater at 05 kHz 20 kHz and 40 kHz present at 10 kHzbut only at maximum intensities) were obtained when theLDV was focused at the top of the parietal region in airabove water Bone vibrations were also determined whenthe bone vibrator in the water bath was manually pressedin direct contact with the forehead of the immersed tiltedskull without intervening water In that situation vibrationswere clearly detected at the inion in air by the LDV with thesame order of magnitude as those seen when the skull wasin air with the bone vibrator applied to the forehead with theheadband

3 Discussion

The present study was designed to test the hypothesis thatunderwater hearing is elicited by a nonosseous BC (STC)mechanism and not by AC and not by osseous BC This

was achieved by determining the thresholds of normal partic-ipants in air and under water (experiment 1) and comparingthem to theminimal intensities required to induce skull bonevibrations in air and under water (experiment 2)

31 Absence of AC Hearing under Water Several aspects ofthe experimental design confirm that AC hearing was notinvolved the ears were occluded by earplugs having a noisereduction rating (NRR) of 30 dB the external ear canals of theparticipants were above water while the sound source wasunder water Since there is a large difference in the acousticimpedances of air and of water the sound pressures inducedby the bone vibrator in water would be largely reflected atits boundary with air and therefore not transmitted to theair above [17ndash19] Furthermore when the forehead of theparticipants was just above the surface of the water and thebone vibrator was still submerged in water (in air control)the thresholds were even higher compared to the condition inwhich the bone vibrator and forehead were both submergedin water but not touching

32 Absence of Osseous BC Hearing under Water When thebone vibrator was pressed to the forehead of the skull directlywith a 5N force in air the lowest intensities at which skullvibrationswere clearly detected at the inion and at the parietalregionwere 10 to 30 dBHL (depending on frequency) On theother hand the thresholds of the participants obtained whentheir foreheads and the bone vibrator were both under waterabout 13 cm apart were 24 to 42 dB (depending on frequency)higher than the thresholds obtained when the bone vibratorwas pressed in air directly to the forehead of the participantswith a 5N force (experiment 1) Note that in the underwatercondition water served as the intermediary between thebone vibrator and the skull and vibrations were detected atthe inion only at 10 kHz and then only at the maximumoutput at that frequency (65 to 70 dB HL) No vibrationswere detected at the other frequencies even at the maximumintensities available However when the bone vibrator waspressed under water directly to the skull forehead (withoutwater serving as the intermediary) vibrations were detectedat the same frequencies and intensities as those obtainedwhen the bone vibrator was applied to the forehead in air

In both underwater parts of the experiments (thresholdsof participants and skull vibrations) the test conditions forthe determination of human thresholds and the assessmentof dry skull vibrations were identical the same water baththe same bone vibrator wrapped with the same rubber glovethe immersion of the forehead in the same position the bonevibrator in contact with water and the same distance (13 cm)between the forehead and the submerged bone vibratorTherefore results of these two experiments can be comparedand it was seen that the thresholds of the participants underwater were much lower than the dB HL settings required forinduction of vibrations at the inion of the skull in air while theskull forehead was under water However the BC thresholdsof the participants with their forehead under water expressedin dB HL audiometer settings in BCmode of the audiometercould not be directly compared to those when the bonevibrator was pressed (5N) to the forehead in air This is due

BioMed Research International 5

01020304050607080

500 1000 2000 4000

Inte

nsity

diff

eren

ce (d

B)

Frequency (Hz)

Behavioral threshold differences in air and under waterVibration detection level differences in air and under water

Figure 2 Bar graphs showing the air-underwater intensity differ-ences in dB which elicited threshold in normal participants andwhich induced vibrations of skull bone at the 4 stimulus frequenciesSince the intensities delivered under water to the skull at 05 20and 40 kHz even at the maximum output of the audiometer didnot induce skull vibrations the maximal output was used in thecalculation of the intensity differences for skull vibration with anupward pointing arrow to indicate that the intensity differences atthese frequencies were even greater For 10 kHz the intensity usedin this calculation is that which induced skull vibrations

to the audiometer and bone vibrator having been calibratedfor BC stimulation when pressed to head sites (mastoid orforehead) and not for inducing a sound field in water Themechanical impedances of the forehead and that of water arevery different However this limitation can be overcome bycomparing in addition the air-water threshold differences tothe air-water intensity differences required to induce skullbone vibrations If one assumes that only an osseous BCmechanism was involved in underwater hearing then thedifference between the intensity levels in air compared to thatunder water between experiments 1 (thresholds) and 2 (vibra-tions) would have been similar In other words if in bothexperiments only an osseous BC mechanism was involvedin underwater hearing then the same difference (between inair and under water see Figure 2) would have been expectedin experiments 1 and 2 However as shown in Figure 2 alarger difference was found in experiment 2 (skull vibrations)than in experiment 1 (threshold of participants) suggestingthe involvement of a different physiological mechanism ineach of the two experiments In fact the exact differencewith respect to the skull vibrations under water could noteven be directly calculated for 05 20 and 40 kHz since novibrations were detected at these frequencies on the inion ofthe skull when the skull forehead was under water even withstimulation at the maximum output level of the audiometerVibrations on the skull under water were detected only at10 kHz at 65ndash70 dB HL Therefore in Figure 2 at the otherfrequencies at which skull vibrations were not detected themaximum output of the audiometer was used for calculationof the intensity difference shown in the bar graph Anarrow pointing upward indicates that the intensity differencesrequired for eliciting skull vibrations at these frequencieswere

even greater As can be clearly seen in Figure 2 the intensitydifferences between those in air and in water required toinduce skull bone vibrations were much greater than thoseneeded to elicit threshold in the participants

The possibility that the LDV system was not sensitiveenough to detect vibrations of bone induced by the soundfield in water at 05 20 and 40 kHz is refuted by severalfindings Among these vibrations at 0 dB HL were detectedby the LDV at these frequencies when focused directly onthe bone vibrator under optimal conditions (bone vibratorunloaded) for sensitivity assessment of the vibrometer (seeMethods experiment 2 sensitivity) In addition the LDVwas able to detect skull vibrations at the inion in air at thesefrequencies only when the stimuli were delivered by thebone vibrator applied in direct contact and pressed to theforehead in air using the headband Skull vibrations werealso detected by the LDV on the inion of the skull in air atthese frequencies when the skull was tilted in water and thebone vibrator was pressed in direct contact under water tothe forehead In this situation water was not serving as theintermediary between the sound field in water and the softtissues over the bone at the forehead Also the noise floorduring all LDV measurements was 10 to 11120583msec and aSNR of at least 6 dB was considered as the criterion for thepresence of vibrations On the other hand the only situationat which the LDV did not detect vibrations of the skull atthe inion and parietal region at 05 20 and 40 kHz evenat the maximum output in air at this SNR was when waterserved as the intervening medium between the bone vibratorand the skull forehead 13 cm apart When water served asthe intervening medium vibrations were detected only at10 kHz but only at maximum output (65 and 70 dB HL)These findings lead to the suggestion that the sound fieldintensities induced by the bone vibrator in water at 05 20and 40 kHz (and at 10 kHz at intensities below 65ndash70 dBHL) were insufficient to induce skull bone vibrations Thistogether with the fact that our participants were able to hear(threshold) sounds under water at intensities below thosewhich induce skull bone vibrations leads to the suggestionthat other sound transmitting mechanisms (eg nonosseousBC) are likely involved at low sound intensities Osseous BCmay be involved in underwater hearing at higher stimulusintensities at sites on the head overlying bone (foreheadinion)

33 Nonosseous BC (STC) in Underwater Hearing at LowIntensities The results of the present study therefore do notsupport the involvement of AC nor of osseous BC (at leastnot at low sound intensities) in underwater hearing Since thesound field in water was actually in direct contact with theskin and the underlying additional soft tissues (muscle adi-pose tissue connective tissue etc of the forehead) overlyingskull bone it is suggested therefore that nonosseous BC canbe considered an alternative mechanism for hearing in suchconditions without inducing skull vibrations that is withoutosseous BC [12] In this mechanism the sound field inducedin the water can elicit vibrations in the soft tissues (STC) [11]since water and each of the soft tissues have similar acousticimpedances (defined as the product of the density of each

6 BioMed Research International

tissue and the velocity of sound in that tissue the acousticimpedance of water = 152 times 106 kgm2 sec and of typical softtissues = 162 times 106 kgm2 sec) Therefore acoustic frequencyvibrations can be transmitted from thewater to the soft tissuesof the body (similar to that during ultrasound diagnosticimaging [18]) to the inner ear fluids [17ndash19] Thus as a resultof the similarity of acoustic impedances between water andthe soft tissues of the head the sound field pressure waves inwater would be transmitted to the soft tissues and from thereto the inner ear (ie low threshold stimulation by nonosseousBC-STC) Moreover as the intensity of the sound field inwater is gradually increased beginning at very low levels forexample during threshold determinations the nonosseousBC (STC) threshold would be reached at a lower intensitythan the osseous BC threshold On the other hand whenthe acoustic impedances of adjacent tissues are very differentfrom each other for example skin or soft tissue to bone (theacoustic impedance of bone = 78times 106 kgm2 sec)most of thevibratory energy (60ndash69) would be reflected at the water-bone interface and not transmitted [17ndash19] and would notinduce skull vibrations (osseous BC) at low intensities Thusdue to the large differences in acoustic impedance betweenwater and bone the sound field in water and soft tissues atlow intensities would be reflected at the bone and would notinduce skull bone vibrations so that osseous BC thresholdswould be elevated Thus it is not likely that the sound fieldinduced in water at threshold intensities would be able toinduce vibrations of skull bone This is similar to the consid-erations of the transmission of sound vibrations from an airenvironment in the external ear to the fluid environment inthe inner ear where the transmission loss is reduced by theimpedance matching functions of the middle ear (tympanicmembranestapes footplate area and lever ratios) [17 19]Furthermore the presence of soft tissues overlying andwithinthe skull actually attenuates the sound levels reaching thebone by about 20 dB [13ndash16] (such attenuation has also beenshown when the magnitude of bone vibrations was evaluatedwith single point LDVs [15 16]) This is likely a result ofthe differences in acoustic impedance between that of softtissues and the underlying bone so that a dry skull may beconsidered to provide a more sensitive measure of possibleskull bone vibrations If vibrations could not be detected on adry skull then they would surely not be detected on an intacthead The finding however that our participants (humanhead with soft tissues) reported threshold hearing at lowerintensities than those required to induce skull vibrationssupports the hypothesis that vibrations in the water and softtissues which did not induce skull bone vibrations at mostfrequencies were nevertheless transmitted via nonosseous(STC) BC to the inner ear

Additional support for a nonosseous BC (STC) mecha-nism can be derived from recent studies showing that hearingsensations can be elicited when the bone vibrator is appliedto water or gel on the skin without any real contact or appli-cation force similar to the situation in underwater hearing[20] Similarly it has been suggested that a major part of thepathway for the transmission of water borne sounds to theinner ear of dolphins and other marine mammals when theyare totally under water is through a soft tissue conduction

pathway In the dolphin this pathway is a fat filled channel inthe mandible [21]

This nonosseous-soft tissue mechanism for underwaterhearingmay also explain the hearing of the 20weeks gestationfetus The fetus is completely enveloped in amniotic fluidwith a softer skull and wider sutures between the skull bonesconditions in which actual skull vibrations (osseous BC) arenot likely Nonosseous BC (STC) therefore probably plays asignificant role in hearing in a fluid environment at thresholdlevels

4 Conclusion

It seems that underwater hearing at low sound intensities ismediated by a nonosseous BC (STC) mechanism At higherintensities there is likely a transition to osseous BC mecha-nisms which involves actual skull bone vibrations

Conflict of Interests

The authors declare that there is no conflict of interestsregarding the publication of this paper

Acknowledgments

The authors wish to express their sincere gratitude to thephysicist Benjamin Gavish PhD for his assistance to thestudy The intensive in-depth discussions with him con-tributed greatly to the interpretation of the results especiallyconcerning the nature of the energy interactions at the inter-face between water or soft tissues with bone Ronen PerezMD otologist provided input to the planning of the studyThe authors wish to thank Vocalzoom Systems Israel forallowing use of their Laser Doppler Vibrometer

References

[1] H Hollien and S Feinstein ldquoContribution of the externalauditory meatus to auditory sensitivity underwaterrdquo Journal ofthe Acoustical Society of America vol 57 no 6 pp 1488ndash14921975

[2] A Shupak Z Sharoni Y Yanir Y Keynan Y Alfie and P Halp-ern ldquoUnderwater hearing and sound localization with andwithout an air interfacerdquo Otology amp Neurotology vol 26 no 1pp 127ndash130 2005

[3] H W Pau M Warkentin O Specht H Krentz A Herrmannand K Ehrt ldquoExperiments on the mechanism of underwaterhearingrdquoActa Oto-Laryngologica vol 131 no 12 pp 1279ndash12852011

[4] M K Qin D Schwaller M Babina and E Cudahy ldquoHumanunderwater and bone conduction hearing in the sonic andultrasonic rangerdquoThe Journal of the Acoustical Society of Amer-ica vol 129 no 4 article 2485 2011

[5] J F Brandt and H Hollien ldquoUnderwater hearing thresholds inmanrdquo Journal of the Acoustical Society of America vol 42 no 5pp 966ndash971 1967

[6] J S Oghalai ldquoThe cochlear amplifier augmentation of the trav-eling wave within the inner earrdquo Current Opinion in Otolaryn-gology amp Head and Neck Surgery vol 12 no 5 pp 431ndash4382004

BioMed Research International 7

[7] S Stenfelt ldquoAcoustic and physiologic aspects of bone conduc-tion hearingrdquo Advances in Oto-Rhino-Laryngology vol 71 pp10ndash21 2011

[8] S Freeman J-Y Sichel and H Sohmer ldquoBone conductionexperiments in animalsmdashevidence for a non-osseous mecha-nismrdquo Hearing Research vol 146 no 1-2 pp 72ndash80 2000

[9] T Ito C Roosli C J Kim J H Sim AMHuber and R ProbstldquoBone conduction thresholds and skull vibration measured onthe teeth during stimulation at different sites on the humanheadrdquo Audiology and Neurotology vol 16 no 1 pp 12ndash22 2010

[10] T Watanabe S Bertoli and R Probst ldquoTransmission pathwaysof vibratory stimulation as measured by subjective thresholdsand distortion-product otoacoustic emissionsrdquo Ear and Hear-ing vol 29 no 5 pp 667ndash673 2008

[11] C Adelman M Kaufmann Yehezkely S Chordekar and HSohmer ldquoRelation between body structure and hearing duringsoft tissue auditory stimulationrdquoBioMedResearch Internationalvol 2015 Article ID 172026 6 pages 2015

[12] B A Vento and J D Durrant ldquoAssessing bone conductionthresholds in clinical practicerdquo in Handbook of Clinical Audi-ology J Katz R Burkard L Hood and L Medwetsky EdsLippincott Williams amp Wilkins Baltimore Md USA 6thedition 2009

[13] A Tjellstrom B Hakansson J Lindstrom et al ldquoAnalysis of themechanical impedance of bone-anchored hearing aidsrdquo ActaOto-Laryngologica vol 89 no 1-2 pp 85ndash92 1980

[14] B Hakansson A Tjellstrom and U Rosenhall ldquoAccelerationlevels at hearing threshold with direct bone conduction versusconventional bone conductionrdquo Acta Oto-Laryngologica vol100 no 3-4 pp 240ndash252 1985

[15] M Eeg-Olofsson S Stenfelt H Taghavi et al ldquoTransmission ofbone conducted soundmdashcorrelation between hearing percep-tion and cochlear vibrationrdquo Hearing Research vol 306 pp 11ndash20 2013

[16] J K Mattingly N T Greene H A Jenkins D J Tollin J REaster and S P Cass ldquoEffects of skin thickness on cochlearinput signal using transcutaneous bone conduction implantsrdquoOtology amp Neurotology vol 36 no 8 pp 1403ndash1411 2015

[17] E G Wever and M Lawrence ldquoThe function of the middleearrdquo in Physiological Acoustics pp 69ndash78 Princeton UniversityPress Princeton NJ USA 1954

[18] J Baun Physical Principles of General and Vascular SonographyCalifornia Publishing San Fransisco Calif USA 2004

[19] B W Blakley and S Siddique ldquoA qualitative explanation of theWeber testrdquo OtolaryngologymdashHead and Neck Surgery vol 120no 1 pp 1ndash4 1999

[20] M Geal-Dor S Chordekar C Adelman andH Sohmer ldquoBoneconduction thresholds without bone vibrator application forcerdquoJournal of the American Academy of Audiology vol 26 no 7 pp645ndash651 2015

[21] S Hemila S Nummela and T Reuter ldquoAnatomy and physicsof the exceptional sensitivity of dolphin hearing (OdontocetiCetacea)rdquo Journal of Comparative Physiology A NeuroethologySensory Neural and Behavioral Physiology vol 196 no 3 pp165ndash179 2010

Submit your manuscripts athttpwwwhindawicom

Stem CellsInternational

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

MEDIATORSINFLAMMATION

of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Behavioural Neurology

EndocrinologyInternational Journal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Disease Markers

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

BioMed Research International

OncologyJournal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Oxidative Medicine and Cellular Longevity

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

PPAR Research

The Scientific World JournalHindawi Publishing Corporation httpwwwhindawicom Volume 2014

Immunology ResearchHindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Journal of

ObesityJournal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Computational and Mathematical Methods in Medicine

OphthalmologyJournal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Diabetes ResearchJournal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

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Research and TreatmentAIDS

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

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Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Parkinsonrsquos Disease

Evidence-Based Complementary and Alternative Medicine

Volume 2014Hindawi Publishing Corporationhttpwwwhindawicom

BioMed Research International 3

0

10

20

30

40

50

60

70

80

500 1000 2000 4000

Mea

n th

resh

old

(dB

HL)

Frequency (Hz)

Figure 1Mean (plusmnSD) intensities eliciting threshold of normal hear-ing participants in the following conditions [e] bone vibrator inwater forehead in air [I] bone vibrator and forehead under waternot touching [998771] bone vibrator directly on forehead both in air

In order to avoid order effects testing conditions wererandomized between participants The tests were conductedat least twice for each condition to ensure repeatability

Results Experiment 1 Thresholds The mean (and standarddeviation) thresholds of the same participants in air andunder water are shown in Figure 1 It can be seen thatbetter (ie lower) thresholds (mean 8ndash13 dB HL dependingon frequency) were obtained when the bone vibrator wasdirectly applied to the forehead in air with a force of about5N Higher thresholds (33ndash50 dB HL) were obtained underwater when water was the intervening medium between thebone vibrator and the forehead 13 cm apart The differencebetween these underwater-air thresholds ranged from 24to 42 dB depending on frequency Even higher (poorer)thresholds (60ndash70 dB HL) were obtained in the controlprocedure in which the head with earplugs was just abovethe water while bone vibrator was still under water A 2-way repeated measures ANOVA separating main effects oftest condition and frequency confirmed these observations[119865(1 71) = 737927 119901 lt 0001 119865(3 71) = 8566 119901 = 0001resp] Pairwise multiple comparisons (Tukey test) found asignificant difference between all tested conditions (119901 lt0001) Also a significant interaction between frequency andtest condition was found [119865(6 71) = 7605 119901 lt 0001] Thesignificant interaction resulted from better threshold at10 kHz in the underwater condition (119901 lt 0001)

22 Experiment 2 Dry Skull Vibrations in Air and underWater In order to assess the intensity levels of the stimuliwhich induce skull bone vibrations the vibrations of a dryskull were measured using a Laser Doppler Vibrometer(LDV) in the two conditions similar to those in experiment 1on the live participants that is when the bone vibrator andskull were both in water and when the bone vibrator wasdirectly applied with 5N force to the skull forehead in air

221 Apparatus The vibration measurements were con-ducted on a dry adult skull using a LDV VibroMet model

500V single point vibrometer (MetroLaser Inc Irvine CAUSA) with a frequency range DC to 70 kHz velocity range2 120583ms to 1ms Recordings were conducted using theMetro-lab software with a sampling rate of 40 kHz and frequencyresolution of 10Hz To improve the signal-to-noise ratio eachmeasurement was averaged 100 times at each stimulationfrequency and the noise floorwas carefullymonitored duringthe entire procedure In order to enhance laser beam reflec-tion and reduce the noise floor aluminum foil reflecting tapewas pasted to all target areas and the laser beam was focusedon this reflector A clinical audiometer (Interacoustics AC-33) was used in order to generate stimuli at 05 kHz 10 kHz20 kHz and 40 kHz delivered to a B-71 (radio ear) bonevibrator

222 Sensitivity Validation of the LDVSystem Thesensitivityof the LDV system was initially assessed by focusing the laserbeam directly on a reflector applied to the center of the bonevibrator without any application force that is ldquounloadedrdquoAssessing the sensitivity of the vibrometer on the unloadedbone vibrator would provide its optimal sensitivity sinceloading (pressing) the bone vibrator onto some surface (egthe forehead) would reduce the vibrations and lead to anelevation of the intensity required to elicit them Vibrations ofthe bone vibrator were assessed for the same four frequenciesin order to determine the lowest vibration velocity whichcould be detected by the LDV and the stimulus intensityrequired to induce it The LDV detected vibrations at thesame four frequencies directly on the bone vibrator with amagnitude ranging from 002 to 005mmsec at 0 dB HLThe noise floor in these measurements was 8 to 12 120583msecdepending on frequency and all were recorded with a signal-to-noise ratio (SNR) of at least 6 dB

223 Procedure The vibrations of the dry skull were mea-sured when it was entirely in air and the bone vibratorwas applied to the forehead of the skull using the standardbone vibrator headband (direct application force equivalentto approximately 5N) as during the hearing thresholddeterminations of the participants in experiment 1 The skullwas placed on a spongy surface to avoid sound and vibrationreflection from the table to the skull when delivering boneconduction stimuli to the skull The LDV laser beam wasfocused at a reflector pasted on the back of the skull (inion-occipital protuberance) perpendicular to the surface of theskull and pure-tones were delivered by the bone vibrator

Skull bone vibrations under water were assessed underthe same conditions as in experiment 1 in which humanthresholds were determined (ie skull suspended tiltedfrom above skull forehead under water inion in air samewater-protected bone vibrator under water at a distance of13 cm from the tilted skull forehead under water stimulidelivered by the bone vibrator under water LDV laser beamfocused to the inion of the skull in air and LDV measuringskull vibrations at that site) In addition vibrations were alsoassessed with the LDV beam focused on the parietal regionof the skull which was also still in air above the water butmuch closer to the surface of the water than the assessmentat the inion The top of the parietal region of the skull is

4 BioMed Research International

perpendicular to a line between the forehead and the inionFurthermore to confirm that the LDV could indeed measureskull vibrations induced under water LDV recordings wereconducted while the bone vibrator was manually pressed indirect underwater contact with the forehead of the immersedskull In this latter condition 13 cm of water no longerintervened between the sound source in the water and theskull forehead in water and the LDV beam was directed tothe inion LDV recordings were conducted at least two timesfor each condition to confirm repeatability Throughout allmeasurements in air and in water vibrations were assessedwhen the stimulus intensities delivered began with the maxi-mumoutput of the audiometer at each frequency down to thelowest intensity at which bone vibrations could still be clearlydetected by the LDV Throughout all LDV measurements(directly on the bone vibrator and on the skull both in airand in water) the noise floor was consistently between 8 to12 120583msec and the signal-to-noise ratio was at least 6 dB

Results Experiment 2 Skull VibrationsThe magnitude of thevibrations of the skull (expressed as velocity mmsec) wasmeasured by the LDV at the inion of the skull (in air) inresponse to stimulation by the bone vibrator pressed directlyto the forehead (in air) with an application force of approx-imately 5N (headband) The lowest stimulus intensities atwhich vibrations could be detected (6 dB above the noisefloor) on the skull in air were 10 dB HL at 05 kHz 30 dB HLat 10 kHz 20 dB HL at 20 kHz and 25 dB HL at 40 kHzAt lower intensities the LDV could not detect any vibrationsabove the noise floor (which was 8 to 12 120583msec dependingon frequency) The magnitude of the vibrations increasedlinearly with stimulus intensity at each frequency reachinghighest levels at the maximal output of the audiometer

When the forehead of the skull was suspended fromabove in the water basin with the bone vibrator also in water13 cm distant bone vibrations above the noise floor weredetected only at 10 kHz and then only at 65ndash70 dB HL (themaximumoutput of the audiometer at 10 kHzwas 70 dBHL)At all other frequencies and intensities vibrations could notbe detected above the noise floor (8 to 12120583msec) even atmaximum output of the audiometer (which was 60 dB HLat 05 kHz 70 dB HL at 20 kHz and 80 dB HL at 40 kHz)Similar results (absence of vibrations with forehead underwater at 05 kHz 20 kHz and 40 kHz present at 10 kHzbut only at maximum intensities) were obtained when theLDV was focused at the top of the parietal region in airabove water Bone vibrations were also determined whenthe bone vibrator in the water bath was manually pressedin direct contact with the forehead of the immersed tiltedskull without intervening water In that situation vibrationswere clearly detected at the inion in air by the LDV with thesame order of magnitude as those seen when the skull wasin air with the bone vibrator applied to the forehead with theheadband

3 Discussion

The present study was designed to test the hypothesis thatunderwater hearing is elicited by a nonosseous BC (STC)mechanism and not by AC and not by osseous BC This

was achieved by determining the thresholds of normal partic-ipants in air and under water (experiment 1) and comparingthem to theminimal intensities required to induce skull bonevibrations in air and under water (experiment 2)

31 Absence of AC Hearing under Water Several aspects ofthe experimental design confirm that AC hearing was notinvolved the ears were occluded by earplugs having a noisereduction rating (NRR) of 30 dB the external ear canals of theparticipants were above water while the sound source wasunder water Since there is a large difference in the acousticimpedances of air and of water the sound pressures inducedby the bone vibrator in water would be largely reflected atits boundary with air and therefore not transmitted to theair above [17ndash19] Furthermore when the forehead of theparticipants was just above the surface of the water and thebone vibrator was still submerged in water (in air control)the thresholds were even higher compared to the condition inwhich the bone vibrator and forehead were both submergedin water but not touching

32 Absence of Osseous BC Hearing under Water When thebone vibrator was pressed to the forehead of the skull directlywith a 5N force in air the lowest intensities at which skullvibrationswere clearly detected at the inion and at the parietalregionwere 10 to 30 dBHL (depending on frequency) On theother hand the thresholds of the participants obtained whentheir foreheads and the bone vibrator were both under waterabout 13 cm apart were 24 to 42 dB (depending on frequency)higher than the thresholds obtained when the bone vibratorwas pressed in air directly to the forehead of the participantswith a 5N force (experiment 1) Note that in the underwatercondition water served as the intermediary between thebone vibrator and the skull and vibrations were detected atthe inion only at 10 kHz and then only at the maximumoutput at that frequency (65 to 70 dB HL) No vibrationswere detected at the other frequencies even at the maximumintensities available However when the bone vibrator waspressed under water directly to the skull forehead (withoutwater serving as the intermediary) vibrations were detectedat the same frequencies and intensities as those obtainedwhen the bone vibrator was applied to the forehead in air

In both underwater parts of the experiments (thresholdsof participants and skull vibrations) the test conditions forthe determination of human thresholds and the assessmentof dry skull vibrations were identical the same water baththe same bone vibrator wrapped with the same rubber glovethe immersion of the forehead in the same position the bonevibrator in contact with water and the same distance (13 cm)between the forehead and the submerged bone vibratorTherefore results of these two experiments can be comparedand it was seen that the thresholds of the participants underwater were much lower than the dB HL settings required forinduction of vibrations at the inion of the skull in air while theskull forehead was under water However the BC thresholdsof the participants with their forehead under water expressedin dB HL audiometer settings in BCmode of the audiometercould not be directly compared to those when the bonevibrator was pressed (5N) to the forehead in air This is due

BioMed Research International 5

01020304050607080

500 1000 2000 4000

Inte

nsity

diff

eren

ce (d

B)

Frequency (Hz)

Behavioral threshold differences in air and under waterVibration detection level differences in air and under water

Figure 2 Bar graphs showing the air-underwater intensity differ-ences in dB which elicited threshold in normal participants andwhich induced vibrations of skull bone at the 4 stimulus frequenciesSince the intensities delivered under water to the skull at 05 20and 40 kHz even at the maximum output of the audiometer didnot induce skull vibrations the maximal output was used in thecalculation of the intensity differences for skull vibration with anupward pointing arrow to indicate that the intensity differences atthese frequencies were even greater For 10 kHz the intensity usedin this calculation is that which induced skull vibrations

to the audiometer and bone vibrator having been calibratedfor BC stimulation when pressed to head sites (mastoid orforehead) and not for inducing a sound field in water Themechanical impedances of the forehead and that of water arevery different However this limitation can be overcome bycomparing in addition the air-water threshold differences tothe air-water intensity differences required to induce skullbone vibrations If one assumes that only an osseous BCmechanism was involved in underwater hearing then thedifference between the intensity levels in air compared to thatunder water between experiments 1 (thresholds) and 2 (vibra-tions) would have been similar In other words if in bothexperiments only an osseous BC mechanism was involvedin underwater hearing then the same difference (between inair and under water see Figure 2) would have been expectedin experiments 1 and 2 However as shown in Figure 2 alarger difference was found in experiment 2 (skull vibrations)than in experiment 1 (threshold of participants) suggestingthe involvement of a different physiological mechanism ineach of the two experiments In fact the exact differencewith respect to the skull vibrations under water could noteven be directly calculated for 05 20 and 40 kHz since novibrations were detected at these frequencies on the inion ofthe skull when the skull forehead was under water even withstimulation at the maximum output level of the audiometerVibrations on the skull under water were detected only at10 kHz at 65ndash70 dB HL Therefore in Figure 2 at the otherfrequencies at which skull vibrations were not detected themaximum output of the audiometer was used for calculationof the intensity difference shown in the bar graph Anarrow pointing upward indicates that the intensity differencesrequired for eliciting skull vibrations at these frequencieswere

even greater As can be clearly seen in Figure 2 the intensitydifferences between those in air and in water required toinduce skull bone vibrations were much greater than thoseneeded to elicit threshold in the participants

The possibility that the LDV system was not sensitiveenough to detect vibrations of bone induced by the soundfield in water at 05 20 and 40 kHz is refuted by severalfindings Among these vibrations at 0 dB HL were detectedby the LDV at these frequencies when focused directly onthe bone vibrator under optimal conditions (bone vibratorunloaded) for sensitivity assessment of the vibrometer (seeMethods experiment 2 sensitivity) In addition the LDVwas able to detect skull vibrations at the inion in air at thesefrequencies only when the stimuli were delivered by thebone vibrator applied in direct contact and pressed to theforehead in air using the headband Skull vibrations werealso detected by the LDV on the inion of the skull in air atthese frequencies when the skull was tilted in water and thebone vibrator was pressed in direct contact under water tothe forehead In this situation water was not serving as theintermediary between the sound field in water and the softtissues over the bone at the forehead Also the noise floorduring all LDV measurements was 10 to 11120583msec and aSNR of at least 6 dB was considered as the criterion for thepresence of vibrations On the other hand the only situationat which the LDV did not detect vibrations of the skull atthe inion and parietal region at 05 20 and 40 kHz evenat the maximum output in air at this SNR was when waterserved as the intervening medium between the bone vibratorand the skull forehead 13 cm apart When water served asthe intervening medium vibrations were detected only at10 kHz but only at maximum output (65 and 70 dB HL)These findings lead to the suggestion that the sound fieldintensities induced by the bone vibrator in water at 05 20and 40 kHz (and at 10 kHz at intensities below 65ndash70 dBHL) were insufficient to induce skull bone vibrations Thistogether with the fact that our participants were able to hear(threshold) sounds under water at intensities below thosewhich induce skull bone vibrations leads to the suggestionthat other sound transmitting mechanisms (eg nonosseousBC) are likely involved at low sound intensities Osseous BCmay be involved in underwater hearing at higher stimulusintensities at sites on the head overlying bone (foreheadinion)

33 Nonosseous BC (STC) in Underwater Hearing at LowIntensities The results of the present study therefore do notsupport the involvement of AC nor of osseous BC (at leastnot at low sound intensities) in underwater hearing Since thesound field in water was actually in direct contact with theskin and the underlying additional soft tissues (muscle adi-pose tissue connective tissue etc of the forehead) overlyingskull bone it is suggested therefore that nonosseous BC canbe considered an alternative mechanism for hearing in suchconditions without inducing skull vibrations that is withoutosseous BC [12] In this mechanism the sound field inducedin the water can elicit vibrations in the soft tissues (STC) [11]since water and each of the soft tissues have similar acousticimpedances (defined as the product of the density of each

6 BioMed Research International

tissue and the velocity of sound in that tissue the acousticimpedance of water = 152 times 106 kgm2 sec and of typical softtissues = 162 times 106 kgm2 sec) Therefore acoustic frequencyvibrations can be transmitted from thewater to the soft tissuesof the body (similar to that during ultrasound diagnosticimaging [18]) to the inner ear fluids [17ndash19] Thus as a resultof the similarity of acoustic impedances between water andthe soft tissues of the head the sound field pressure waves inwater would be transmitted to the soft tissues and from thereto the inner ear (ie low threshold stimulation by nonosseousBC-STC) Moreover as the intensity of the sound field inwater is gradually increased beginning at very low levels forexample during threshold determinations the nonosseousBC (STC) threshold would be reached at a lower intensitythan the osseous BC threshold On the other hand whenthe acoustic impedances of adjacent tissues are very differentfrom each other for example skin or soft tissue to bone (theacoustic impedance of bone = 78times 106 kgm2 sec)most of thevibratory energy (60ndash69) would be reflected at the water-bone interface and not transmitted [17ndash19] and would notinduce skull vibrations (osseous BC) at low intensities Thusdue to the large differences in acoustic impedance betweenwater and bone the sound field in water and soft tissues atlow intensities would be reflected at the bone and would notinduce skull bone vibrations so that osseous BC thresholdswould be elevated Thus it is not likely that the sound fieldinduced in water at threshold intensities would be able toinduce vibrations of skull bone This is similar to the consid-erations of the transmission of sound vibrations from an airenvironment in the external ear to the fluid environment inthe inner ear where the transmission loss is reduced by theimpedance matching functions of the middle ear (tympanicmembranestapes footplate area and lever ratios) [17 19]Furthermore the presence of soft tissues overlying andwithinthe skull actually attenuates the sound levels reaching thebone by about 20 dB [13ndash16] (such attenuation has also beenshown when the magnitude of bone vibrations was evaluatedwith single point LDVs [15 16]) This is likely a result ofthe differences in acoustic impedance between that of softtissues and the underlying bone so that a dry skull may beconsidered to provide a more sensitive measure of possibleskull bone vibrations If vibrations could not be detected on adry skull then they would surely not be detected on an intacthead The finding however that our participants (humanhead with soft tissues) reported threshold hearing at lowerintensities than those required to induce skull vibrationssupports the hypothesis that vibrations in the water and softtissues which did not induce skull bone vibrations at mostfrequencies were nevertheless transmitted via nonosseous(STC) BC to the inner ear

Additional support for a nonosseous BC (STC) mecha-nism can be derived from recent studies showing that hearingsensations can be elicited when the bone vibrator is appliedto water or gel on the skin without any real contact or appli-cation force similar to the situation in underwater hearing[20] Similarly it has been suggested that a major part of thepathway for the transmission of water borne sounds to theinner ear of dolphins and other marine mammals when theyare totally under water is through a soft tissue conduction

pathway In the dolphin this pathway is a fat filled channel inthe mandible [21]

This nonosseous-soft tissue mechanism for underwaterhearingmay also explain the hearing of the 20weeks gestationfetus The fetus is completely enveloped in amniotic fluidwith a softer skull and wider sutures between the skull bonesconditions in which actual skull vibrations (osseous BC) arenot likely Nonosseous BC (STC) therefore probably plays asignificant role in hearing in a fluid environment at thresholdlevels

4 Conclusion

It seems that underwater hearing at low sound intensities ismediated by a nonosseous BC (STC) mechanism At higherintensities there is likely a transition to osseous BC mecha-nisms which involves actual skull bone vibrations

Conflict of Interests

The authors declare that there is no conflict of interestsregarding the publication of this paper

Acknowledgments

The authors wish to express their sincere gratitude to thephysicist Benjamin Gavish PhD for his assistance to thestudy The intensive in-depth discussions with him con-tributed greatly to the interpretation of the results especiallyconcerning the nature of the energy interactions at the inter-face between water or soft tissues with bone Ronen PerezMD otologist provided input to the planning of the studyThe authors wish to thank Vocalzoom Systems Israel forallowing use of their Laser Doppler Vibrometer

References

[1] H Hollien and S Feinstein ldquoContribution of the externalauditory meatus to auditory sensitivity underwaterrdquo Journal ofthe Acoustical Society of America vol 57 no 6 pp 1488ndash14921975

[2] A Shupak Z Sharoni Y Yanir Y Keynan Y Alfie and P Halp-ern ldquoUnderwater hearing and sound localization with andwithout an air interfacerdquo Otology amp Neurotology vol 26 no 1pp 127ndash130 2005

[3] H W Pau M Warkentin O Specht H Krentz A Herrmannand K Ehrt ldquoExperiments on the mechanism of underwaterhearingrdquoActa Oto-Laryngologica vol 131 no 12 pp 1279ndash12852011

[4] M K Qin D Schwaller M Babina and E Cudahy ldquoHumanunderwater and bone conduction hearing in the sonic andultrasonic rangerdquoThe Journal of the Acoustical Society of Amer-ica vol 129 no 4 article 2485 2011

[5] J F Brandt and H Hollien ldquoUnderwater hearing thresholds inmanrdquo Journal of the Acoustical Society of America vol 42 no 5pp 966ndash971 1967

[6] J S Oghalai ldquoThe cochlear amplifier augmentation of the trav-eling wave within the inner earrdquo Current Opinion in Otolaryn-gology amp Head and Neck Surgery vol 12 no 5 pp 431ndash4382004

BioMed Research International 7

[7] S Stenfelt ldquoAcoustic and physiologic aspects of bone conduc-tion hearingrdquo Advances in Oto-Rhino-Laryngology vol 71 pp10ndash21 2011

[8] S Freeman J-Y Sichel and H Sohmer ldquoBone conductionexperiments in animalsmdashevidence for a non-osseous mecha-nismrdquo Hearing Research vol 146 no 1-2 pp 72ndash80 2000

[9] T Ito C Roosli C J Kim J H Sim AMHuber and R ProbstldquoBone conduction thresholds and skull vibration measured onthe teeth during stimulation at different sites on the humanheadrdquo Audiology and Neurotology vol 16 no 1 pp 12ndash22 2010

[10] T Watanabe S Bertoli and R Probst ldquoTransmission pathwaysof vibratory stimulation as measured by subjective thresholdsand distortion-product otoacoustic emissionsrdquo Ear and Hear-ing vol 29 no 5 pp 667ndash673 2008

[11] C Adelman M Kaufmann Yehezkely S Chordekar and HSohmer ldquoRelation between body structure and hearing duringsoft tissue auditory stimulationrdquoBioMedResearch Internationalvol 2015 Article ID 172026 6 pages 2015

[12] B A Vento and J D Durrant ldquoAssessing bone conductionthresholds in clinical practicerdquo in Handbook of Clinical Audi-ology J Katz R Burkard L Hood and L Medwetsky EdsLippincott Williams amp Wilkins Baltimore Md USA 6thedition 2009

[13] A Tjellstrom B Hakansson J Lindstrom et al ldquoAnalysis of themechanical impedance of bone-anchored hearing aidsrdquo ActaOto-Laryngologica vol 89 no 1-2 pp 85ndash92 1980

[14] B Hakansson A Tjellstrom and U Rosenhall ldquoAccelerationlevels at hearing threshold with direct bone conduction versusconventional bone conductionrdquo Acta Oto-Laryngologica vol100 no 3-4 pp 240ndash252 1985

[15] M Eeg-Olofsson S Stenfelt H Taghavi et al ldquoTransmission ofbone conducted soundmdashcorrelation between hearing percep-tion and cochlear vibrationrdquo Hearing Research vol 306 pp 11ndash20 2013

[16] J K Mattingly N T Greene H A Jenkins D J Tollin J REaster and S P Cass ldquoEffects of skin thickness on cochlearinput signal using transcutaneous bone conduction implantsrdquoOtology amp Neurotology vol 36 no 8 pp 1403ndash1411 2015

[17] E G Wever and M Lawrence ldquoThe function of the middleearrdquo in Physiological Acoustics pp 69ndash78 Princeton UniversityPress Princeton NJ USA 1954

[18] J Baun Physical Principles of General and Vascular SonographyCalifornia Publishing San Fransisco Calif USA 2004

[19] B W Blakley and S Siddique ldquoA qualitative explanation of theWeber testrdquo OtolaryngologymdashHead and Neck Surgery vol 120no 1 pp 1ndash4 1999

[20] M Geal-Dor S Chordekar C Adelman andH Sohmer ldquoBoneconduction thresholds without bone vibrator application forcerdquoJournal of the American Academy of Audiology vol 26 no 7 pp645ndash651 2015

[21] S Hemila S Nummela and T Reuter ldquoAnatomy and physicsof the exceptional sensitivity of dolphin hearing (OdontocetiCetacea)rdquo Journal of Comparative Physiology A NeuroethologySensory Neural and Behavioral Physiology vol 196 no 3 pp165ndash179 2010

Submit your manuscripts athttpwwwhindawicom

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Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

MEDIATORSINFLAMMATION

of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Behavioural Neurology

EndocrinologyInternational Journal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Disease Markers

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

BioMed Research International

OncologyJournal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Oxidative Medicine and Cellular Longevity

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

PPAR Research

The Scientific World JournalHindawi Publishing Corporation httpwwwhindawicom Volume 2014

Immunology ResearchHindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Journal of

ObesityJournal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Computational and Mathematical Methods in Medicine

OphthalmologyJournal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Diabetes ResearchJournal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Research and TreatmentAIDS

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Gastroenterology Research and Practice

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Parkinsonrsquos Disease

Evidence-Based Complementary and Alternative Medicine

Volume 2014Hindawi Publishing Corporationhttpwwwhindawicom

4 BioMed Research International

perpendicular to a line between the forehead and the inionFurthermore to confirm that the LDV could indeed measureskull vibrations induced under water LDV recordings wereconducted while the bone vibrator was manually pressed indirect underwater contact with the forehead of the immersedskull In this latter condition 13 cm of water no longerintervened between the sound source in the water and theskull forehead in water and the LDV beam was directed tothe inion LDV recordings were conducted at least two timesfor each condition to confirm repeatability Throughout allmeasurements in air and in water vibrations were assessedwhen the stimulus intensities delivered began with the maxi-mumoutput of the audiometer at each frequency down to thelowest intensity at which bone vibrations could still be clearlydetected by the LDV Throughout all LDV measurements(directly on the bone vibrator and on the skull both in airand in water) the noise floor was consistently between 8 to12 120583msec and the signal-to-noise ratio was at least 6 dB

Results Experiment 2 Skull VibrationsThe magnitude of thevibrations of the skull (expressed as velocity mmsec) wasmeasured by the LDV at the inion of the skull (in air) inresponse to stimulation by the bone vibrator pressed directlyto the forehead (in air) with an application force of approx-imately 5N (headband) The lowest stimulus intensities atwhich vibrations could be detected (6 dB above the noisefloor) on the skull in air were 10 dB HL at 05 kHz 30 dB HLat 10 kHz 20 dB HL at 20 kHz and 25 dB HL at 40 kHzAt lower intensities the LDV could not detect any vibrationsabove the noise floor (which was 8 to 12 120583msec dependingon frequency) The magnitude of the vibrations increasedlinearly with stimulus intensity at each frequency reachinghighest levels at the maximal output of the audiometer

When the forehead of the skull was suspended fromabove in the water basin with the bone vibrator also in water13 cm distant bone vibrations above the noise floor weredetected only at 10 kHz and then only at 65ndash70 dB HL (themaximumoutput of the audiometer at 10 kHzwas 70 dBHL)At all other frequencies and intensities vibrations could notbe detected above the noise floor (8 to 12120583msec) even atmaximum output of the audiometer (which was 60 dB HLat 05 kHz 70 dB HL at 20 kHz and 80 dB HL at 40 kHz)Similar results (absence of vibrations with forehead underwater at 05 kHz 20 kHz and 40 kHz present at 10 kHzbut only at maximum intensities) were obtained when theLDV was focused at the top of the parietal region in airabove water Bone vibrations were also determined whenthe bone vibrator in the water bath was manually pressedin direct contact with the forehead of the immersed tiltedskull without intervening water In that situation vibrationswere clearly detected at the inion in air by the LDV with thesame order of magnitude as those seen when the skull wasin air with the bone vibrator applied to the forehead with theheadband

3 Discussion

The present study was designed to test the hypothesis thatunderwater hearing is elicited by a nonosseous BC (STC)mechanism and not by AC and not by osseous BC This

was achieved by determining the thresholds of normal partic-ipants in air and under water (experiment 1) and comparingthem to theminimal intensities required to induce skull bonevibrations in air and under water (experiment 2)

31 Absence of AC Hearing under Water Several aspects ofthe experimental design confirm that AC hearing was notinvolved the ears were occluded by earplugs having a noisereduction rating (NRR) of 30 dB the external ear canals of theparticipants were above water while the sound source wasunder water Since there is a large difference in the acousticimpedances of air and of water the sound pressures inducedby the bone vibrator in water would be largely reflected atits boundary with air and therefore not transmitted to theair above [17ndash19] Furthermore when the forehead of theparticipants was just above the surface of the water and thebone vibrator was still submerged in water (in air control)the thresholds were even higher compared to the condition inwhich the bone vibrator and forehead were both submergedin water but not touching

32 Absence of Osseous BC Hearing under Water When thebone vibrator was pressed to the forehead of the skull directlywith a 5N force in air the lowest intensities at which skullvibrationswere clearly detected at the inion and at the parietalregionwere 10 to 30 dBHL (depending on frequency) On theother hand the thresholds of the participants obtained whentheir foreheads and the bone vibrator were both under waterabout 13 cm apart were 24 to 42 dB (depending on frequency)higher than the thresholds obtained when the bone vibratorwas pressed in air directly to the forehead of the participantswith a 5N force (experiment 1) Note that in the underwatercondition water served as the intermediary between thebone vibrator and the skull and vibrations were detected atthe inion only at 10 kHz and then only at the maximumoutput at that frequency (65 to 70 dB HL) No vibrationswere detected at the other frequencies even at the maximumintensities available However when the bone vibrator waspressed under water directly to the skull forehead (withoutwater serving as the intermediary) vibrations were detectedat the same frequencies and intensities as those obtainedwhen the bone vibrator was applied to the forehead in air

In both underwater parts of the experiments (thresholdsof participants and skull vibrations) the test conditions forthe determination of human thresholds and the assessmentof dry skull vibrations were identical the same water baththe same bone vibrator wrapped with the same rubber glovethe immersion of the forehead in the same position the bonevibrator in contact with water and the same distance (13 cm)between the forehead and the submerged bone vibratorTherefore results of these two experiments can be comparedand it was seen that the thresholds of the participants underwater were much lower than the dB HL settings required forinduction of vibrations at the inion of the skull in air while theskull forehead was under water However the BC thresholdsof the participants with their forehead under water expressedin dB HL audiometer settings in BCmode of the audiometercould not be directly compared to those when the bonevibrator was pressed (5N) to the forehead in air This is due

BioMed Research International 5

01020304050607080

500 1000 2000 4000

Inte

nsity

diff

eren

ce (d

B)

Frequency (Hz)

Behavioral threshold differences in air and under waterVibration detection level differences in air and under water

Figure 2 Bar graphs showing the air-underwater intensity differ-ences in dB which elicited threshold in normal participants andwhich induced vibrations of skull bone at the 4 stimulus frequenciesSince the intensities delivered under water to the skull at 05 20and 40 kHz even at the maximum output of the audiometer didnot induce skull vibrations the maximal output was used in thecalculation of the intensity differences for skull vibration with anupward pointing arrow to indicate that the intensity differences atthese frequencies were even greater For 10 kHz the intensity usedin this calculation is that which induced skull vibrations

to the audiometer and bone vibrator having been calibratedfor BC stimulation when pressed to head sites (mastoid orforehead) and not for inducing a sound field in water Themechanical impedances of the forehead and that of water arevery different However this limitation can be overcome bycomparing in addition the air-water threshold differences tothe air-water intensity differences required to induce skullbone vibrations If one assumes that only an osseous BCmechanism was involved in underwater hearing then thedifference between the intensity levels in air compared to thatunder water between experiments 1 (thresholds) and 2 (vibra-tions) would have been similar In other words if in bothexperiments only an osseous BC mechanism was involvedin underwater hearing then the same difference (between inair and under water see Figure 2) would have been expectedin experiments 1 and 2 However as shown in Figure 2 alarger difference was found in experiment 2 (skull vibrations)than in experiment 1 (threshold of participants) suggestingthe involvement of a different physiological mechanism ineach of the two experiments In fact the exact differencewith respect to the skull vibrations under water could noteven be directly calculated for 05 20 and 40 kHz since novibrations were detected at these frequencies on the inion ofthe skull when the skull forehead was under water even withstimulation at the maximum output level of the audiometerVibrations on the skull under water were detected only at10 kHz at 65ndash70 dB HL Therefore in Figure 2 at the otherfrequencies at which skull vibrations were not detected themaximum output of the audiometer was used for calculationof the intensity difference shown in the bar graph Anarrow pointing upward indicates that the intensity differencesrequired for eliciting skull vibrations at these frequencieswere

even greater As can be clearly seen in Figure 2 the intensitydifferences between those in air and in water required toinduce skull bone vibrations were much greater than thoseneeded to elicit threshold in the participants

The possibility that the LDV system was not sensitiveenough to detect vibrations of bone induced by the soundfield in water at 05 20 and 40 kHz is refuted by severalfindings Among these vibrations at 0 dB HL were detectedby the LDV at these frequencies when focused directly onthe bone vibrator under optimal conditions (bone vibratorunloaded) for sensitivity assessment of the vibrometer (seeMethods experiment 2 sensitivity) In addition the LDVwas able to detect skull vibrations at the inion in air at thesefrequencies only when the stimuli were delivered by thebone vibrator applied in direct contact and pressed to theforehead in air using the headband Skull vibrations werealso detected by the LDV on the inion of the skull in air atthese frequencies when the skull was tilted in water and thebone vibrator was pressed in direct contact under water tothe forehead In this situation water was not serving as theintermediary between the sound field in water and the softtissues over the bone at the forehead Also the noise floorduring all LDV measurements was 10 to 11120583msec and aSNR of at least 6 dB was considered as the criterion for thepresence of vibrations On the other hand the only situationat which the LDV did not detect vibrations of the skull atthe inion and parietal region at 05 20 and 40 kHz evenat the maximum output in air at this SNR was when waterserved as the intervening medium between the bone vibratorand the skull forehead 13 cm apart When water served asthe intervening medium vibrations were detected only at10 kHz but only at maximum output (65 and 70 dB HL)These findings lead to the suggestion that the sound fieldintensities induced by the bone vibrator in water at 05 20and 40 kHz (and at 10 kHz at intensities below 65ndash70 dBHL) were insufficient to induce skull bone vibrations Thistogether with the fact that our participants were able to hear(threshold) sounds under water at intensities below thosewhich induce skull bone vibrations leads to the suggestionthat other sound transmitting mechanisms (eg nonosseousBC) are likely involved at low sound intensities Osseous BCmay be involved in underwater hearing at higher stimulusintensities at sites on the head overlying bone (foreheadinion)

33 Nonosseous BC (STC) in Underwater Hearing at LowIntensities The results of the present study therefore do notsupport the involvement of AC nor of osseous BC (at leastnot at low sound intensities) in underwater hearing Since thesound field in water was actually in direct contact with theskin and the underlying additional soft tissues (muscle adi-pose tissue connective tissue etc of the forehead) overlyingskull bone it is suggested therefore that nonosseous BC canbe considered an alternative mechanism for hearing in suchconditions without inducing skull vibrations that is withoutosseous BC [12] In this mechanism the sound field inducedin the water can elicit vibrations in the soft tissues (STC) [11]since water and each of the soft tissues have similar acousticimpedances (defined as the product of the density of each

6 BioMed Research International

tissue and the velocity of sound in that tissue the acousticimpedance of water = 152 times 106 kgm2 sec and of typical softtissues = 162 times 106 kgm2 sec) Therefore acoustic frequencyvibrations can be transmitted from thewater to the soft tissuesof the body (similar to that during ultrasound diagnosticimaging [18]) to the inner ear fluids [17ndash19] Thus as a resultof the similarity of acoustic impedances between water andthe soft tissues of the head the sound field pressure waves inwater would be transmitted to the soft tissues and from thereto the inner ear (ie low threshold stimulation by nonosseousBC-STC) Moreover as the intensity of the sound field inwater is gradually increased beginning at very low levels forexample during threshold determinations the nonosseousBC (STC) threshold would be reached at a lower intensitythan the osseous BC threshold On the other hand whenthe acoustic impedances of adjacent tissues are very differentfrom each other for example skin or soft tissue to bone (theacoustic impedance of bone = 78times 106 kgm2 sec)most of thevibratory energy (60ndash69) would be reflected at the water-bone interface and not transmitted [17ndash19] and would notinduce skull vibrations (osseous BC) at low intensities Thusdue to the large differences in acoustic impedance betweenwater and bone the sound field in water and soft tissues atlow intensities would be reflected at the bone and would notinduce skull bone vibrations so that osseous BC thresholdswould be elevated Thus it is not likely that the sound fieldinduced in water at threshold intensities would be able toinduce vibrations of skull bone This is similar to the consid-erations of the transmission of sound vibrations from an airenvironment in the external ear to the fluid environment inthe inner ear where the transmission loss is reduced by theimpedance matching functions of the middle ear (tympanicmembranestapes footplate area and lever ratios) [17 19]Furthermore the presence of soft tissues overlying andwithinthe skull actually attenuates the sound levels reaching thebone by about 20 dB [13ndash16] (such attenuation has also beenshown when the magnitude of bone vibrations was evaluatedwith single point LDVs [15 16]) This is likely a result ofthe differences in acoustic impedance between that of softtissues and the underlying bone so that a dry skull may beconsidered to provide a more sensitive measure of possibleskull bone vibrations If vibrations could not be detected on adry skull then they would surely not be detected on an intacthead The finding however that our participants (humanhead with soft tissues) reported threshold hearing at lowerintensities than those required to induce skull vibrationssupports the hypothesis that vibrations in the water and softtissues which did not induce skull bone vibrations at mostfrequencies were nevertheless transmitted via nonosseous(STC) BC to the inner ear

Additional support for a nonosseous BC (STC) mecha-nism can be derived from recent studies showing that hearingsensations can be elicited when the bone vibrator is appliedto water or gel on the skin without any real contact or appli-cation force similar to the situation in underwater hearing[20] Similarly it has been suggested that a major part of thepathway for the transmission of water borne sounds to theinner ear of dolphins and other marine mammals when theyare totally under water is through a soft tissue conduction

pathway In the dolphin this pathway is a fat filled channel inthe mandible [21]

This nonosseous-soft tissue mechanism for underwaterhearingmay also explain the hearing of the 20weeks gestationfetus The fetus is completely enveloped in amniotic fluidwith a softer skull and wider sutures between the skull bonesconditions in which actual skull vibrations (osseous BC) arenot likely Nonosseous BC (STC) therefore probably plays asignificant role in hearing in a fluid environment at thresholdlevels

4 Conclusion

It seems that underwater hearing at low sound intensities ismediated by a nonosseous BC (STC) mechanism At higherintensities there is likely a transition to osseous BC mecha-nisms which involves actual skull bone vibrations

Conflict of Interests

The authors declare that there is no conflict of interestsregarding the publication of this paper

Acknowledgments

The authors wish to express their sincere gratitude to thephysicist Benjamin Gavish PhD for his assistance to thestudy The intensive in-depth discussions with him con-tributed greatly to the interpretation of the results especiallyconcerning the nature of the energy interactions at the inter-face between water or soft tissues with bone Ronen PerezMD otologist provided input to the planning of the studyThe authors wish to thank Vocalzoom Systems Israel forallowing use of their Laser Doppler Vibrometer

References

[1] H Hollien and S Feinstein ldquoContribution of the externalauditory meatus to auditory sensitivity underwaterrdquo Journal ofthe Acoustical Society of America vol 57 no 6 pp 1488ndash14921975

[2] A Shupak Z Sharoni Y Yanir Y Keynan Y Alfie and P Halp-ern ldquoUnderwater hearing and sound localization with andwithout an air interfacerdquo Otology amp Neurotology vol 26 no 1pp 127ndash130 2005

[3] H W Pau M Warkentin O Specht H Krentz A Herrmannand K Ehrt ldquoExperiments on the mechanism of underwaterhearingrdquoActa Oto-Laryngologica vol 131 no 12 pp 1279ndash12852011

[4] M K Qin D Schwaller M Babina and E Cudahy ldquoHumanunderwater and bone conduction hearing in the sonic andultrasonic rangerdquoThe Journal of the Acoustical Society of Amer-ica vol 129 no 4 article 2485 2011

[5] J F Brandt and H Hollien ldquoUnderwater hearing thresholds inmanrdquo Journal of the Acoustical Society of America vol 42 no 5pp 966ndash971 1967

[6] J S Oghalai ldquoThe cochlear amplifier augmentation of the trav-eling wave within the inner earrdquo Current Opinion in Otolaryn-gology amp Head and Neck Surgery vol 12 no 5 pp 431ndash4382004

BioMed Research International 7

[7] S Stenfelt ldquoAcoustic and physiologic aspects of bone conduc-tion hearingrdquo Advances in Oto-Rhino-Laryngology vol 71 pp10ndash21 2011

[8] S Freeman J-Y Sichel and H Sohmer ldquoBone conductionexperiments in animalsmdashevidence for a non-osseous mecha-nismrdquo Hearing Research vol 146 no 1-2 pp 72ndash80 2000

[9] T Ito C Roosli C J Kim J H Sim AMHuber and R ProbstldquoBone conduction thresholds and skull vibration measured onthe teeth during stimulation at different sites on the humanheadrdquo Audiology and Neurotology vol 16 no 1 pp 12ndash22 2010

[10] T Watanabe S Bertoli and R Probst ldquoTransmission pathwaysof vibratory stimulation as measured by subjective thresholdsand distortion-product otoacoustic emissionsrdquo Ear and Hear-ing vol 29 no 5 pp 667ndash673 2008

[11] C Adelman M Kaufmann Yehezkely S Chordekar and HSohmer ldquoRelation between body structure and hearing duringsoft tissue auditory stimulationrdquoBioMedResearch Internationalvol 2015 Article ID 172026 6 pages 2015

[12] B A Vento and J D Durrant ldquoAssessing bone conductionthresholds in clinical practicerdquo in Handbook of Clinical Audi-ology J Katz R Burkard L Hood and L Medwetsky EdsLippincott Williams amp Wilkins Baltimore Md USA 6thedition 2009

[13] A Tjellstrom B Hakansson J Lindstrom et al ldquoAnalysis of themechanical impedance of bone-anchored hearing aidsrdquo ActaOto-Laryngologica vol 89 no 1-2 pp 85ndash92 1980

[14] B Hakansson A Tjellstrom and U Rosenhall ldquoAccelerationlevels at hearing threshold with direct bone conduction versusconventional bone conductionrdquo Acta Oto-Laryngologica vol100 no 3-4 pp 240ndash252 1985

[15] M Eeg-Olofsson S Stenfelt H Taghavi et al ldquoTransmission ofbone conducted soundmdashcorrelation between hearing percep-tion and cochlear vibrationrdquo Hearing Research vol 306 pp 11ndash20 2013

[16] J K Mattingly N T Greene H A Jenkins D J Tollin J REaster and S P Cass ldquoEffects of skin thickness on cochlearinput signal using transcutaneous bone conduction implantsrdquoOtology amp Neurotology vol 36 no 8 pp 1403ndash1411 2015

[17] E G Wever and M Lawrence ldquoThe function of the middleearrdquo in Physiological Acoustics pp 69ndash78 Princeton UniversityPress Princeton NJ USA 1954

[18] J Baun Physical Principles of General and Vascular SonographyCalifornia Publishing San Fransisco Calif USA 2004

[19] B W Blakley and S Siddique ldquoA qualitative explanation of theWeber testrdquo OtolaryngologymdashHead and Neck Surgery vol 120no 1 pp 1ndash4 1999

[20] M Geal-Dor S Chordekar C Adelman andH Sohmer ldquoBoneconduction thresholds without bone vibrator application forcerdquoJournal of the American Academy of Audiology vol 26 no 7 pp645ndash651 2015

[21] S Hemila S Nummela and T Reuter ldquoAnatomy and physicsof the exceptional sensitivity of dolphin hearing (OdontocetiCetacea)rdquo Journal of Comparative Physiology A NeuroethologySensory Neural and Behavioral Physiology vol 196 no 3 pp165ndash179 2010

Submit your manuscripts athttpwwwhindawicom

Stem CellsInternational

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

MEDIATORSINFLAMMATION

of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Behavioural Neurology

EndocrinologyInternational Journal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Disease Markers

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

BioMed Research International

OncologyJournal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Oxidative Medicine and Cellular Longevity

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

PPAR Research

The Scientific World JournalHindawi Publishing Corporation httpwwwhindawicom Volume 2014

Immunology ResearchHindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Journal of

ObesityJournal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Computational and Mathematical Methods in Medicine

OphthalmologyJournal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Diabetes ResearchJournal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Research and TreatmentAIDS

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Gastroenterology Research and Practice

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Parkinsonrsquos Disease

Evidence-Based Complementary and Alternative Medicine

Volume 2014Hindawi Publishing Corporationhttpwwwhindawicom

BioMed Research International 5

01020304050607080

500 1000 2000 4000

Inte

nsity

diff

eren

ce (d

B)

Frequency (Hz)

Behavioral threshold differences in air and under waterVibration detection level differences in air and under water

Figure 2 Bar graphs showing the air-underwater intensity differ-ences in dB which elicited threshold in normal participants andwhich induced vibrations of skull bone at the 4 stimulus frequenciesSince the intensities delivered under water to the skull at 05 20and 40 kHz even at the maximum output of the audiometer didnot induce skull vibrations the maximal output was used in thecalculation of the intensity differences for skull vibration with anupward pointing arrow to indicate that the intensity differences atthese frequencies were even greater For 10 kHz the intensity usedin this calculation is that which induced skull vibrations

to the audiometer and bone vibrator having been calibratedfor BC stimulation when pressed to head sites (mastoid orforehead) and not for inducing a sound field in water Themechanical impedances of the forehead and that of water arevery different However this limitation can be overcome bycomparing in addition the air-water threshold differences tothe air-water intensity differences required to induce skullbone vibrations If one assumes that only an osseous BCmechanism was involved in underwater hearing then thedifference between the intensity levels in air compared to thatunder water between experiments 1 (thresholds) and 2 (vibra-tions) would have been similar In other words if in bothexperiments only an osseous BC mechanism was involvedin underwater hearing then the same difference (between inair and under water see Figure 2) would have been expectedin experiments 1 and 2 However as shown in Figure 2 alarger difference was found in experiment 2 (skull vibrations)than in experiment 1 (threshold of participants) suggestingthe involvement of a different physiological mechanism ineach of the two experiments In fact the exact differencewith respect to the skull vibrations under water could noteven be directly calculated for 05 20 and 40 kHz since novibrations were detected at these frequencies on the inion ofthe skull when the skull forehead was under water even withstimulation at the maximum output level of the audiometerVibrations on the skull under water were detected only at10 kHz at 65ndash70 dB HL Therefore in Figure 2 at the otherfrequencies at which skull vibrations were not detected themaximum output of the audiometer was used for calculationof the intensity difference shown in the bar graph Anarrow pointing upward indicates that the intensity differencesrequired for eliciting skull vibrations at these frequencieswere

even greater As can be clearly seen in Figure 2 the intensitydifferences between those in air and in water required toinduce skull bone vibrations were much greater than thoseneeded to elicit threshold in the participants

The possibility that the LDV system was not sensitiveenough to detect vibrations of bone induced by the soundfield in water at 05 20 and 40 kHz is refuted by severalfindings Among these vibrations at 0 dB HL were detectedby the LDV at these frequencies when focused directly onthe bone vibrator under optimal conditions (bone vibratorunloaded) for sensitivity assessment of the vibrometer (seeMethods experiment 2 sensitivity) In addition the LDVwas able to detect skull vibrations at the inion in air at thesefrequencies only when the stimuli were delivered by thebone vibrator applied in direct contact and pressed to theforehead in air using the headband Skull vibrations werealso detected by the LDV on the inion of the skull in air atthese frequencies when the skull was tilted in water and thebone vibrator was pressed in direct contact under water tothe forehead In this situation water was not serving as theintermediary between the sound field in water and the softtissues over the bone at the forehead Also the noise floorduring all LDV measurements was 10 to 11120583msec and aSNR of at least 6 dB was considered as the criterion for thepresence of vibrations On the other hand the only situationat which the LDV did not detect vibrations of the skull atthe inion and parietal region at 05 20 and 40 kHz evenat the maximum output in air at this SNR was when waterserved as the intervening medium between the bone vibratorand the skull forehead 13 cm apart When water served asthe intervening medium vibrations were detected only at10 kHz but only at maximum output (65 and 70 dB HL)These findings lead to the suggestion that the sound fieldintensities induced by the bone vibrator in water at 05 20and 40 kHz (and at 10 kHz at intensities below 65ndash70 dBHL) were insufficient to induce skull bone vibrations Thistogether with the fact that our participants were able to hear(threshold) sounds under water at intensities below thosewhich induce skull bone vibrations leads to the suggestionthat other sound transmitting mechanisms (eg nonosseousBC) are likely involved at low sound intensities Osseous BCmay be involved in underwater hearing at higher stimulusintensities at sites on the head overlying bone (foreheadinion)

33 Nonosseous BC (STC) in Underwater Hearing at LowIntensities The results of the present study therefore do notsupport the involvement of AC nor of osseous BC (at leastnot at low sound intensities) in underwater hearing Since thesound field in water was actually in direct contact with theskin and the underlying additional soft tissues (muscle adi-pose tissue connective tissue etc of the forehead) overlyingskull bone it is suggested therefore that nonosseous BC canbe considered an alternative mechanism for hearing in suchconditions without inducing skull vibrations that is withoutosseous BC [12] In this mechanism the sound field inducedin the water can elicit vibrations in the soft tissues (STC) [11]since water and each of the soft tissues have similar acousticimpedances (defined as the product of the density of each

6 BioMed Research International

tissue and the velocity of sound in that tissue the acousticimpedance of water = 152 times 106 kgm2 sec and of typical softtissues = 162 times 106 kgm2 sec) Therefore acoustic frequencyvibrations can be transmitted from thewater to the soft tissuesof the body (similar to that during ultrasound diagnosticimaging [18]) to the inner ear fluids [17ndash19] Thus as a resultof the similarity of acoustic impedances between water andthe soft tissues of the head the sound field pressure waves inwater would be transmitted to the soft tissues and from thereto the inner ear (ie low threshold stimulation by nonosseousBC-STC) Moreover as the intensity of the sound field inwater is gradually increased beginning at very low levels forexample during threshold determinations the nonosseousBC (STC) threshold would be reached at a lower intensitythan the osseous BC threshold On the other hand whenthe acoustic impedances of adjacent tissues are very differentfrom each other for example skin or soft tissue to bone (theacoustic impedance of bone = 78times 106 kgm2 sec)most of thevibratory energy (60ndash69) would be reflected at the water-bone interface and not transmitted [17ndash19] and would notinduce skull vibrations (osseous BC) at low intensities Thusdue to the large differences in acoustic impedance betweenwater and bone the sound field in water and soft tissues atlow intensities would be reflected at the bone and would notinduce skull bone vibrations so that osseous BC thresholdswould be elevated Thus it is not likely that the sound fieldinduced in water at threshold intensities would be able toinduce vibrations of skull bone This is similar to the consid-erations of the transmission of sound vibrations from an airenvironment in the external ear to the fluid environment inthe inner ear where the transmission loss is reduced by theimpedance matching functions of the middle ear (tympanicmembranestapes footplate area and lever ratios) [17 19]Furthermore the presence of soft tissues overlying andwithinthe skull actually attenuates the sound levels reaching thebone by about 20 dB [13ndash16] (such attenuation has also beenshown when the magnitude of bone vibrations was evaluatedwith single point LDVs [15 16]) This is likely a result ofthe differences in acoustic impedance between that of softtissues and the underlying bone so that a dry skull may beconsidered to provide a more sensitive measure of possibleskull bone vibrations If vibrations could not be detected on adry skull then they would surely not be detected on an intacthead The finding however that our participants (humanhead with soft tissues) reported threshold hearing at lowerintensities than those required to induce skull vibrationssupports the hypothesis that vibrations in the water and softtissues which did not induce skull bone vibrations at mostfrequencies were nevertheless transmitted via nonosseous(STC) BC to the inner ear

Additional support for a nonosseous BC (STC) mecha-nism can be derived from recent studies showing that hearingsensations can be elicited when the bone vibrator is appliedto water or gel on the skin without any real contact or appli-cation force similar to the situation in underwater hearing[20] Similarly it has been suggested that a major part of thepathway for the transmission of water borne sounds to theinner ear of dolphins and other marine mammals when theyare totally under water is through a soft tissue conduction

pathway In the dolphin this pathway is a fat filled channel inthe mandible [21]

This nonosseous-soft tissue mechanism for underwaterhearingmay also explain the hearing of the 20weeks gestationfetus The fetus is completely enveloped in amniotic fluidwith a softer skull and wider sutures between the skull bonesconditions in which actual skull vibrations (osseous BC) arenot likely Nonosseous BC (STC) therefore probably plays asignificant role in hearing in a fluid environment at thresholdlevels

4 Conclusion

It seems that underwater hearing at low sound intensities ismediated by a nonosseous BC (STC) mechanism At higherintensities there is likely a transition to osseous BC mecha-nisms which involves actual skull bone vibrations

Conflict of Interests

The authors declare that there is no conflict of interestsregarding the publication of this paper

Acknowledgments

The authors wish to express their sincere gratitude to thephysicist Benjamin Gavish PhD for his assistance to thestudy The intensive in-depth discussions with him con-tributed greatly to the interpretation of the results especiallyconcerning the nature of the energy interactions at the inter-face between water or soft tissues with bone Ronen PerezMD otologist provided input to the planning of the studyThe authors wish to thank Vocalzoom Systems Israel forallowing use of their Laser Doppler Vibrometer

References

[1] H Hollien and S Feinstein ldquoContribution of the externalauditory meatus to auditory sensitivity underwaterrdquo Journal ofthe Acoustical Society of America vol 57 no 6 pp 1488ndash14921975

[2] A Shupak Z Sharoni Y Yanir Y Keynan Y Alfie and P Halp-ern ldquoUnderwater hearing and sound localization with andwithout an air interfacerdquo Otology amp Neurotology vol 26 no 1pp 127ndash130 2005

[3] H W Pau M Warkentin O Specht H Krentz A Herrmannand K Ehrt ldquoExperiments on the mechanism of underwaterhearingrdquoActa Oto-Laryngologica vol 131 no 12 pp 1279ndash12852011

[4] M K Qin D Schwaller M Babina and E Cudahy ldquoHumanunderwater and bone conduction hearing in the sonic andultrasonic rangerdquoThe Journal of the Acoustical Society of Amer-ica vol 129 no 4 article 2485 2011

[5] J F Brandt and H Hollien ldquoUnderwater hearing thresholds inmanrdquo Journal of the Acoustical Society of America vol 42 no 5pp 966ndash971 1967

[6] J S Oghalai ldquoThe cochlear amplifier augmentation of the trav-eling wave within the inner earrdquo Current Opinion in Otolaryn-gology amp Head and Neck Surgery vol 12 no 5 pp 431ndash4382004

BioMed Research International 7

[7] S Stenfelt ldquoAcoustic and physiologic aspects of bone conduc-tion hearingrdquo Advances in Oto-Rhino-Laryngology vol 71 pp10ndash21 2011

[8] S Freeman J-Y Sichel and H Sohmer ldquoBone conductionexperiments in animalsmdashevidence for a non-osseous mecha-nismrdquo Hearing Research vol 146 no 1-2 pp 72ndash80 2000

[9] T Ito C Roosli C J Kim J H Sim AMHuber and R ProbstldquoBone conduction thresholds and skull vibration measured onthe teeth during stimulation at different sites on the humanheadrdquo Audiology and Neurotology vol 16 no 1 pp 12ndash22 2010

[10] T Watanabe S Bertoli and R Probst ldquoTransmission pathwaysof vibratory stimulation as measured by subjective thresholdsand distortion-product otoacoustic emissionsrdquo Ear and Hear-ing vol 29 no 5 pp 667ndash673 2008

[11] C Adelman M Kaufmann Yehezkely S Chordekar and HSohmer ldquoRelation between body structure and hearing duringsoft tissue auditory stimulationrdquoBioMedResearch Internationalvol 2015 Article ID 172026 6 pages 2015

[12] B A Vento and J D Durrant ldquoAssessing bone conductionthresholds in clinical practicerdquo in Handbook of Clinical Audi-ology J Katz R Burkard L Hood and L Medwetsky EdsLippincott Williams amp Wilkins Baltimore Md USA 6thedition 2009

[13] A Tjellstrom B Hakansson J Lindstrom et al ldquoAnalysis of themechanical impedance of bone-anchored hearing aidsrdquo ActaOto-Laryngologica vol 89 no 1-2 pp 85ndash92 1980

[14] B Hakansson A Tjellstrom and U Rosenhall ldquoAccelerationlevels at hearing threshold with direct bone conduction versusconventional bone conductionrdquo Acta Oto-Laryngologica vol100 no 3-4 pp 240ndash252 1985

[15] M Eeg-Olofsson S Stenfelt H Taghavi et al ldquoTransmission ofbone conducted soundmdashcorrelation between hearing percep-tion and cochlear vibrationrdquo Hearing Research vol 306 pp 11ndash20 2013

[16] J K Mattingly N T Greene H A Jenkins D J Tollin J REaster and S P Cass ldquoEffects of skin thickness on cochlearinput signal using transcutaneous bone conduction implantsrdquoOtology amp Neurotology vol 36 no 8 pp 1403ndash1411 2015

[17] E G Wever and M Lawrence ldquoThe function of the middleearrdquo in Physiological Acoustics pp 69ndash78 Princeton UniversityPress Princeton NJ USA 1954

[18] J Baun Physical Principles of General and Vascular SonographyCalifornia Publishing San Fransisco Calif USA 2004

[19] B W Blakley and S Siddique ldquoA qualitative explanation of theWeber testrdquo OtolaryngologymdashHead and Neck Surgery vol 120no 1 pp 1ndash4 1999

[20] M Geal-Dor S Chordekar C Adelman andH Sohmer ldquoBoneconduction thresholds without bone vibrator application forcerdquoJournal of the American Academy of Audiology vol 26 no 7 pp645ndash651 2015

[21] S Hemila S Nummela and T Reuter ldquoAnatomy and physicsof the exceptional sensitivity of dolphin hearing (OdontocetiCetacea)rdquo Journal of Comparative Physiology A NeuroethologySensory Neural and Behavioral Physiology vol 196 no 3 pp165ndash179 2010

Submit your manuscripts athttpwwwhindawicom

Stem CellsInternational

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

MEDIATORSINFLAMMATION

of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Behavioural Neurology

EndocrinologyInternational Journal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Disease Markers

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

BioMed Research International

OncologyJournal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Oxidative Medicine and Cellular Longevity

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

PPAR Research

The Scientific World JournalHindawi Publishing Corporation httpwwwhindawicom Volume 2014

Immunology ResearchHindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Journal of

ObesityJournal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Computational and Mathematical Methods in Medicine

OphthalmologyJournal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Diabetes ResearchJournal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Research and TreatmentAIDS

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Gastroenterology Research and Practice

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Parkinsonrsquos Disease

Evidence-Based Complementary and Alternative Medicine

Volume 2014Hindawi Publishing Corporationhttpwwwhindawicom

6 BioMed Research International

tissue and the velocity of sound in that tissue the acousticimpedance of water = 152 times 106 kgm2 sec and of typical softtissues = 162 times 106 kgm2 sec) Therefore acoustic frequencyvibrations can be transmitted from thewater to the soft tissuesof the body (similar to that during ultrasound diagnosticimaging [18]) to the inner ear fluids [17ndash19] Thus as a resultof the similarity of acoustic impedances between water andthe soft tissues of the head the sound field pressure waves inwater would be transmitted to the soft tissues and from thereto the inner ear (ie low threshold stimulation by nonosseousBC-STC) Moreover as the intensity of the sound field inwater is gradually increased beginning at very low levels forexample during threshold determinations the nonosseousBC (STC) threshold would be reached at a lower intensitythan the osseous BC threshold On the other hand whenthe acoustic impedances of adjacent tissues are very differentfrom each other for example skin or soft tissue to bone (theacoustic impedance of bone = 78times 106 kgm2 sec)most of thevibratory energy (60ndash69) would be reflected at the water-bone interface and not transmitted [17ndash19] and would notinduce skull vibrations (osseous BC) at low intensities Thusdue to the large differences in acoustic impedance betweenwater and bone the sound field in water and soft tissues atlow intensities would be reflected at the bone and would notinduce skull bone vibrations so that osseous BC thresholdswould be elevated Thus it is not likely that the sound fieldinduced in water at threshold intensities would be able toinduce vibrations of skull bone This is similar to the consid-erations of the transmission of sound vibrations from an airenvironment in the external ear to the fluid environment inthe inner ear where the transmission loss is reduced by theimpedance matching functions of the middle ear (tympanicmembranestapes footplate area and lever ratios) [17 19]Furthermore the presence of soft tissues overlying andwithinthe skull actually attenuates the sound levels reaching thebone by about 20 dB [13ndash16] (such attenuation has also beenshown when the magnitude of bone vibrations was evaluatedwith single point LDVs [15 16]) This is likely a result ofthe differences in acoustic impedance between that of softtissues and the underlying bone so that a dry skull may beconsidered to provide a more sensitive measure of possibleskull bone vibrations If vibrations could not be detected on adry skull then they would surely not be detected on an intacthead The finding however that our participants (humanhead with soft tissues) reported threshold hearing at lowerintensities than those required to induce skull vibrationssupports the hypothesis that vibrations in the water and softtissues which did not induce skull bone vibrations at mostfrequencies were nevertheless transmitted via nonosseous(STC) BC to the inner ear

Additional support for a nonosseous BC (STC) mecha-nism can be derived from recent studies showing that hearingsensations can be elicited when the bone vibrator is appliedto water or gel on the skin without any real contact or appli-cation force similar to the situation in underwater hearing[20] Similarly it has been suggested that a major part of thepathway for the transmission of water borne sounds to theinner ear of dolphins and other marine mammals when theyare totally under water is through a soft tissue conduction

pathway In the dolphin this pathway is a fat filled channel inthe mandible [21]

This nonosseous-soft tissue mechanism for underwaterhearingmay also explain the hearing of the 20weeks gestationfetus The fetus is completely enveloped in amniotic fluidwith a softer skull and wider sutures between the skull bonesconditions in which actual skull vibrations (osseous BC) arenot likely Nonosseous BC (STC) therefore probably plays asignificant role in hearing in a fluid environment at thresholdlevels

4 Conclusion

It seems that underwater hearing at low sound intensities ismediated by a nonosseous BC (STC) mechanism At higherintensities there is likely a transition to osseous BC mecha-nisms which involves actual skull bone vibrations

Conflict of Interests

The authors declare that there is no conflict of interestsregarding the publication of this paper

Acknowledgments

The authors wish to express their sincere gratitude to thephysicist Benjamin Gavish PhD for his assistance to thestudy The intensive in-depth discussions with him con-tributed greatly to the interpretation of the results especiallyconcerning the nature of the energy interactions at the inter-face between water or soft tissues with bone Ronen PerezMD otologist provided input to the planning of the studyThe authors wish to thank Vocalzoom Systems Israel forallowing use of their Laser Doppler Vibrometer

References

[1] H Hollien and S Feinstein ldquoContribution of the externalauditory meatus to auditory sensitivity underwaterrdquo Journal ofthe Acoustical Society of America vol 57 no 6 pp 1488ndash14921975

[2] A Shupak Z Sharoni Y Yanir Y Keynan Y Alfie and P Halp-ern ldquoUnderwater hearing and sound localization with andwithout an air interfacerdquo Otology amp Neurotology vol 26 no 1pp 127ndash130 2005

[3] H W Pau M Warkentin O Specht H Krentz A Herrmannand K Ehrt ldquoExperiments on the mechanism of underwaterhearingrdquoActa Oto-Laryngologica vol 131 no 12 pp 1279ndash12852011

[4] M K Qin D Schwaller M Babina and E Cudahy ldquoHumanunderwater and bone conduction hearing in the sonic andultrasonic rangerdquoThe Journal of the Acoustical Society of Amer-ica vol 129 no 4 article 2485 2011

[5] J F Brandt and H Hollien ldquoUnderwater hearing thresholds inmanrdquo Journal of the Acoustical Society of America vol 42 no 5pp 966ndash971 1967

[6] J S Oghalai ldquoThe cochlear amplifier augmentation of the trav-eling wave within the inner earrdquo Current Opinion in Otolaryn-gology amp Head and Neck Surgery vol 12 no 5 pp 431ndash4382004

BioMed Research International 7

[7] S Stenfelt ldquoAcoustic and physiologic aspects of bone conduc-tion hearingrdquo Advances in Oto-Rhino-Laryngology vol 71 pp10ndash21 2011

[8] S Freeman J-Y Sichel and H Sohmer ldquoBone conductionexperiments in animalsmdashevidence for a non-osseous mecha-nismrdquo Hearing Research vol 146 no 1-2 pp 72ndash80 2000

[9] T Ito C Roosli C J Kim J H Sim AMHuber and R ProbstldquoBone conduction thresholds and skull vibration measured onthe teeth during stimulation at different sites on the humanheadrdquo Audiology and Neurotology vol 16 no 1 pp 12ndash22 2010

[10] T Watanabe S Bertoli and R Probst ldquoTransmission pathwaysof vibratory stimulation as measured by subjective thresholdsand distortion-product otoacoustic emissionsrdquo Ear and Hear-ing vol 29 no 5 pp 667ndash673 2008

[11] C Adelman M Kaufmann Yehezkely S Chordekar and HSohmer ldquoRelation between body structure and hearing duringsoft tissue auditory stimulationrdquoBioMedResearch Internationalvol 2015 Article ID 172026 6 pages 2015

[12] B A Vento and J D Durrant ldquoAssessing bone conductionthresholds in clinical practicerdquo in Handbook of Clinical Audi-ology J Katz R Burkard L Hood and L Medwetsky EdsLippincott Williams amp Wilkins Baltimore Md USA 6thedition 2009

[13] A Tjellstrom B Hakansson J Lindstrom et al ldquoAnalysis of themechanical impedance of bone-anchored hearing aidsrdquo ActaOto-Laryngologica vol 89 no 1-2 pp 85ndash92 1980

[14] B Hakansson A Tjellstrom and U Rosenhall ldquoAccelerationlevels at hearing threshold with direct bone conduction versusconventional bone conductionrdquo Acta Oto-Laryngologica vol100 no 3-4 pp 240ndash252 1985

[15] M Eeg-Olofsson S Stenfelt H Taghavi et al ldquoTransmission ofbone conducted soundmdashcorrelation between hearing percep-tion and cochlear vibrationrdquo Hearing Research vol 306 pp 11ndash20 2013

[16] J K Mattingly N T Greene H A Jenkins D J Tollin J REaster and S P Cass ldquoEffects of skin thickness on cochlearinput signal using transcutaneous bone conduction implantsrdquoOtology amp Neurotology vol 36 no 8 pp 1403ndash1411 2015

[17] E G Wever and M Lawrence ldquoThe function of the middleearrdquo in Physiological Acoustics pp 69ndash78 Princeton UniversityPress Princeton NJ USA 1954

[18] J Baun Physical Principles of General and Vascular SonographyCalifornia Publishing San Fransisco Calif USA 2004

[19] B W Blakley and S Siddique ldquoA qualitative explanation of theWeber testrdquo OtolaryngologymdashHead and Neck Surgery vol 120no 1 pp 1ndash4 1999

[20] M Geal-Dor S Chordekar C Adelman andH Sohmer ldquoBoneconduction thresholds without bone vibrator application forcerdquoJournal of the American Academy of Audiology vol 26 no 7 pp645ndash651 2015

[21] S Hemila S Nummela and T Reuter ldquoAnatomy and physicsof the exceptional sensitivity of dolphin hearing (OdontocetiCetacea)rdquo Journal of Comparative Physiology A NeuroethologySensory Neural and Behavioral Physiology vol 196 no 3 pp165ndash179 2010

Submit your manuscripts athttpwwwhindawicom

Stem CellsInternational

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

MEDIATORSINFLAMMATION

of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Behavioural Neurology

EndocrinologyInternational Journal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Disease Markers

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

BioMed Research International

OncologyJournal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Oxidative Medicine and Cellular Longevity

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

PPAR Research

The Scientific World JournalHindawi Publishing Corporation httpwwwhindawicom Volume 2014

Immunology ResearchHindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Journal of

ObesityJournal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Computational and Mathematical Methods in Medicine

OphthalmologyJournal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Diabetes ResearchJournal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Research and TreatmentAIDS

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Gastroenterology Research and Practice

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Parkinsonrsquos Disease

Evidence-Based Complementary and Alternative Medicine

Volume 2014Hindawi Publishing Corporationhttpwwwhindawicom

BioMed Research International 7

[7] S Stenfelt ldquoAcoustic and physiologic aspects of bone conduc-tion hearingrdquo Advances in Oto-Rhino-Laryngology vol 71 pp10ndash21 2011

[8] S Freeman J-Y Sichel and H Sohmer ldquoBone conductionexperiments in animalsmdashevidence for a non-osseous mecha-nismrdquo Hearing Research vol 146 no 1-2 pp 72ndash80 2000

[9] T Ito C Roosli C J Kim J H Sim AMHuber and R ProbstldquoBone conduction thresholds and skull vibration measured onthe teeth during stimulation at different sites on the humanheadrdquo Audiology and Neurotology vol 16 no 1 pp 12ndash22 2010

[10] T Watanabe S Bertoli and R Probst ldquoTransmission pathwaysof vibratory stimulation as measured by subjective thresholdsand distortion-product otoacoustic emissionsrdquo Ear and Hear-ing vol 29 no 5 pp 667ndash673 2008

[11] C Adelman M Kaufmann Yehezkely S Chordekar and HSohmer ldquoRelation between body structure and hearing duringsoft tissue auditory stimulationrdquoBioMedResearch Internationalvol 2015 Article ID 172026 6 pages 2015

[12] B A Vento and J D Durrant ldquoAssessing bone conductionthresholds in clinical practicerdquo in Handbook of Clinical Audi-ology J Katz R Burkard L Hood and L Medwetsky EdsLippincott Williams amp Wilkins Baltimore Md USA 6thedition 2009

[13] A Tjellstrom B Hakansson J Lindstrom et al ldquoAnalysis of themechanical impedance of bone-anchored hearing aidsrdquo ActaOto-Laryngologica vol 89 no 1-2 pp 85ndash92 1980

[14] B Hakansson A Tjellstrom and U Rosenhall ldquoAccelerationlevels at hearing threshold with direct bone conduction versusconventional bone conductionrdquo Acta Oto-Laryngologica vol100 no 3-4 pp 240ndash252 1985

[15] M Eeg-Olofsson S Stenfelt H Taghavi et al ldquoTransmission ofbone conducted soundmdashcorrelation between hearing percep-tion and cochlear vibrationrdquo Hearing Research vol 306 pp 11ndash20 2013

[16] J K Mattingly N T Greene H A Jenkins D J Tollin J REaster and S P Cass ldquoEffects of skin thickness on cochlearinput signal using transcutaneous bone conduction implantsrdquoOtology amp Neurotology vol 36 no 8 pp 1403ndash1411 2015

[17] E G Wever and M Lawrence ldquoThe function of the middleearrdquo in Physiological Acoustics pp 69ndash78 Princeton UniversityPress Princeton NJ USA 1954

[18] J Baun Physical Principles of General and Vascular SonographyCalifornia Publishing San Fransisco Calif USA 2004

[19] B W Blakley and S Siddique ldquoA qualitative explanation of theWeber testrdquo OtolaryngologymdashHead and Neck Surgery vol 120no 1 pp 1ndash4 1999

[20] M Geal-Dor S Chordekar C Adelman andH Sohmer ldquoBoneconduction thresholds without bone vibrator application forcerdquoJournal of the American Academy of Audiology vol 26 no 7 pp645ndash651 2015

[21] S Hemila S Nummela and T Reuter ldquoAnatomy and physicsof the exceptional sensitivity of dolphin hearing (OdontocetiCetacea)rdquo Journal of Comparative Physiology A NeuroethologySensory Neural and Behavioral Physiology vol 196 no 3 pp165ndash179 2010

Submit your manuscripts athttpwwwhindawicom

Stem CellsInternational

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

MEDIATORSINFLAMMATION

of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Behavioural Neurology

EndocrinologyInternational Journal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Disease Markers

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

BioMed Research International

OncologyJournal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Oxidative Medicine and Cellular Longevity

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

PPAR Research

The Scientific World JournalHindawi Publishing Corporation httpwwwhindawicom Volume 2014

Immunology ResearchHindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Journal of

ObesityJournal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Computational and Mathematical Methods in Medicine

OphthalmologyJournal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Diabetes ResearchJournal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Research and TreatmentAIDS

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Gastroenterology Research and Practice

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Parkinsonrsquos Disease

Evidence-Based Complementary and Alternative Medicine

Volume 2014Hindawi Publishing Corporationhttpwwwhindawicom

Submit your manuscripts athttpwwwhindawicom

Stem CellsInternational

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

MEDIATORSINFLAMMATION

of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Behavioural Neurology

EndocrinologyInternational Journal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Disease Markers

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

BioMed Research International

OncologyJournal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Oxidative Medicine and Cellular Longevity

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

PPAR Research

The Scientific World JournalHindawi Publishing Corporation httpwwwhindawicom Volume 2014

Immunology ResearchHindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Journal of

ObesityJournal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Computational and Mathematical Methods in Medicine

OphthalmologyJournal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Diabetes ResearchJournal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Research and TreatmentAIDS

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Gastroenterology Research and Practice

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Parkinsonrsquos Disease

Evidence-Based Complementary and Alternative Medicine

Volume 2014Hindawi Publishing Corporationhttpwwwhindawicom