Bilateral bone conduction stimulation provides reliable binaural cues for localization

Bilateral bone conduction stimulation provides reliable binaural cues for localization

Hearing Research 388 (2020) 107881 Contents lists available at ScienceDirect Hearing Research journal homepage: www.elsevier.com/locate/heares Rese...

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Hearing Research 388 (2020) 107881

Contents lists available at ScienceDirect

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

Research Paper

Bilateral bone conduction stimulation provides reliable binaural cues for localization Hillary Snapp a, *, Katharina Vogt b, Martijn J.H. Agterberg b, c a

Department of Otolaryngology, University of Miami, Miami, FL, USA Department of Biophysics, Donders Institute for Brain, Cognition and Behaviour, Radboud University Nijmegen, the Netherlands c Department of Otorhinolaryngology, Donders Institute for Brain, Cognition and Behaviour, Radboud University Medical Centre Nijmegen, the Netherlands b

a r t i c l e i n f o

a b s t r a c t

Article history: Received 26 August 2019 Received in revised form 25 November 2019 Accepted 27 December 2019 Available online 3 January 2020

This study aimed to characterize binaural hearing abilities with bone conduction stimulation in simulated conductive hearing loss. Bone conduction hearing devices (BCDs) are a common method of rehabilitating conductive hearing loss. However, little is known about the access these devices provide to binaural cues. To study the ability of BCDs to restore access to binaural cues in conductive loss, normal hearing listeners were plugged unilaterally and bilaterally and localization ability was assessed using a non-surgical BCD attached to the mastoid/s via an adhesive (MED-EL, Corp). The results demonstrate that 1) application of the BCD in simulated unilateral conductive hearing loss does not restore access to binaural cues, evidenced by poor localization abilities. 2) bilateral application of BCDs in simulated bilateral conductive hearing loss provides access to binaural cues, 2) unilateral application of BCDs in simulated bilateral conductive hearing loss disrupts these cues and impairs localization performance, The transcutaneous stimulation of the adhesive BCD resulted in decreased access to sound compared to the normal open ear, resulting in asymmetries in aided versus non-aided hearing thresholds. Symmetrical hearing results in improved localization abilities, while asymmetric hearing disrupts sound localization abilities. © 2019 Published by Elsevier B.V.

Keywords: Adhear Bilateral conductive hearing loss Bone conduction Sound localization Binaural hearing

1. Introduction In those with irresolvable conductive hearing loss (CHL), stimulation by bone conduction (BC) is a well-accepted form of rehabilitation (Snik et al., 2005). In CHL where the external and/or middle ear are compromised, bone conduction devices (BCDs) can bypass these components to directly stimulate the intact cochlea by way of vibrating the skull. Although it has been established that percutaneous BCDs provide improved audibility and speech perception in subjects with unilateral CHL and in subjects with bilateral CHL, whether these improved perceptual abilities reflect binaural hearing benefits has not yet been clearly established (Agterberg et al., 2012; Colquitt et al., 2011; Priwin et al., 2007; Stenfelt, 2005; Vogt et al., 2019).

Abbreviations: BB, broadband; aBCD, adhesive bone-conduction device; BC, bone-conduction; BCD, bone-conduction device; BP, bilateral plug; CHL, conductive hearing loss; HP, high-pass; ITD, interaural time difference; ILD, interaural level difference; LP, low-pass; MAE, mean absolute error; UP, unilateral plug * Corresponding author. 1120 NW 14th Street, 5th Floor, Miami, FL, 33136, USA. E-mail address: [email protected] (H. Snapp). https://doi.org/10.1016/j.heares.2019.107881 0378-5955/© 2019 Published by Elsevier B.V.

Binaural hearing arises from the interpretation of critical timing and level differences between the two ears (i.e. ITDs and ILDs). Without the detection of these interaural differences, tasks such as separating speech from background noise or localizing sound become more difficult and for some impaired listeners, impossible. For this reason, bilateral stimulation of the auditory system is considered the gold standard in achieving optimal hearing performance. Given the known benefits of binaural hearing, and the ability of BCDs to directly stimulate the cochlea, the reported non-use of BCDs in unilateral CHL (Nelissen et al., 2015) and the low percentage of bilateral application of BCDs in bilateral CHL (Asp and Reinfeldt, 2018; Colquitt et al., 2011; Fan et al., 2014; Marsella et al., 2011; Oliveira et al., 2013) are curious. Particularly in those with pure CHL, where the cochlea remains intact and is optimally primed to best utilize the inputs provided to the auditory system. However, it is possible that the mechanism of stimulation by BC is a contributing factor. Intra-cochlear studies have suggested that stimulation by boneconduction provides comparable stimulation to air-conduction (Bekesy, 1960; Stenfelt and Goode, 2005). This is supported by

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clinical evidence indicating that BCDs are an effective means of providing audibility in those with CHL. How BCD stimulation affects binaural hearing abilities, however, is less clear. BCDs rely on the skull as a medium, which acts as a low pass filter (Stenfelt and Goode, 2005), and allows for multiple pathways of cochlear stimulation (Eeg-Olofsson et al., 2011; Stenfelt and Goode, 2005). Because both cochleae are encased in the bones of the skull, stimulation by BC results in activation of both cochleae. The crosshearing (Eeg-Olofsson et al., 2011) that results from BC stimulation may result in disturbances of timing and level information perceived at the cochlea/e (Stenfelt, 2012; Stenfelt and Zeitooni, 2013). In unilateral CHL, the contralateral normal hearing cochlea is receiving information via the normal auditory pathway and the cross BC stimulation. Increased acuity is observed at the cochlea closest to the stimulation point (Eeg-Olofsson et al., 2011), yet a high degree of intra-subject variability is observed in contralateral threshold detection (Eeg-Olofsson et al., 2011). In bilateral CHL, both cochleae are receiving ipsilateral and contralateral stimulation under bilateral BCD application. How the interaction of these signals affects processing of acoustic information or the resulting impact on binaural hearing abilities is not fully understood (Stenfelt, 2005, 2012; Stenfelt and Zeitooni, 2013). The ability of a unilateral BCD to stimulate both cochleae has been reputed to be advantageous in the bilateral CHL population, as the non-implanted ear receives auditory stimulation (Hol et al., 2005; Snik et al., 2005; Tjellstrom et al., 2001). Localization performance is a well-excepted marker for binaural hearing abilities (Snik et al., 2015). This is primarily due to the fundamental reliance on interaural level and timing cues, and the ability of the normal auditory system to detect the subtle differences in these cues to affect accurate localization of a sound source (Yin et al., 2019). Some studies of effectiveness for percutaneous BCDs in unilateral (de Wolf et al., 2011; Hol et al., 2005) and bilateral (Bosman et al., 2001; Dun et al., 2013) CHL have suggested binaural hearing benefits, although varying in degree and limited in design. Studies of sound localization in acquired (Agterberg et al., 2012) and congenital unilateral CHL (Agterberg et al., 2011a) indicate improved localization abilities with the BCD, although intersubject performance varied considerably with many participants still performing well below normal. Other studies note no clear improvement in localization in patients with congenital unilateral CHL (Kunst et al., 2008). Collectively, these studies suggest that not all listeners gain the same degree of benefit, and it remains to be seen whether the reported improvement is related to binaural processing. All of these studies were limited by heterogeneous patient populations that unavoidably varied in terms of duration of deafness, maturation of the auditory system, degree of loss, hearing asymmetry, duration of BCD use, and technology. In this study, these variables were controlled through simulation of CHL in normal-hearing adult listeners with fully developed auditory systems. The ability to determine the location of a sound source is negatively affected by unilateral and bilateral CHL. Amplification with a BCD should provide improved spatial hearing, and potentially processing of acoustical/binaural cues. The aims of this study were to investigate the unilateral and bilateral aided benefits of BCDs in normal hearing listeners under simulated (plugged) unilateral and bilateral conductive hearing loss conditions using measures of sound localization as a marker for binaural hearing.

recruited from Radboud University, Nijmegen, the Netherlands, participated in this study. All participants had normal hearing bilaterally as determined by air conduction hearing thresholds of <25 dB HL across the standard audiometric test frequencies, 250e8000 Hz.

2.2. Experimental setup and stimuli Localization measurements were performed in a sound-isolated anechoic mobile auditory laboratory (Vogt et al., 2018). The walls were covered with absorbing materials. Twenty-four loudspeakers (Genelec 8010, Genelec Oy, Iisalmi, Finland) were positioned within the horizontal (±70 ) and vertical (þ40 /-30 ) planes. The speakers were covered by a black, sound emitting curtain. Matlab (The MathWorks, Natick, USA) was utilized to control a sound card with 24 analog output channels (MOTU 24Ao, MOTU, Cambridge, USA), and an electronic board (Arduino Uno, Arduino, Somerville, USA), which triggered the fixation LED located at the center of the speaker array. During the task, listeners sat comfortably in a chair located 1.2 m from the speakers. Horizontal and vertical head movements were recorded via infrared cameras (Smarttrack, ART, Munich, Germany). Broadband (BB; 0.5e20 kHz), high-pass (HP; 3e20 kHz), and low-pass (LP; 0.5e1.5 kHz) noise bursts were randomly presented at three different sound levels (45, 55, and 65 dB, A-weighted (dBA)). All stimuli had 150-ms duration and were presented in random order within a block of 80 trials with equal right and left representation across the front hemifield. Participants were instructed to fixate a head-mounted LED towards the perceived sound location via a head movement. Responses were calculated relative to the target location Matlab (The MathWorks, Natick, USA).

2.3. Procedures 2.3.1. Conditions Localization performance was evaluated in the normal hearing condition for all listeners. Listeners were also tested in semirandomized order under simulated unilateral and bilateral CHL conditions, where binaural hearing was disrupted. Participants localization abilities were evaluated in seven listening conditions (Fig. 1): c1) normal hearing, c2) unilateral plug, c3) unilateral plug þ ipsilateral aBCD, c4) unilateral plug þ ipsilateral aBCD þ contralateral pinna mold,1 c5) bilateral plugs, c6) bilateral plugs þ bilateral aBCDs, and c7) bilateral plugs þ unilateral aBCD. Bilaterally aided thresholds, bilaterally plugged thresholds, and normal hearing thresholds were recorded for all participants. Bilateral hearing thresholds were obtained in the unaided condition under earphones in an audiometric sound booth from 250 to 8000 Hz. Thresholds were reassessed in both the bilateral plug (BP) and the BP þ bilateral aBCD conditions in the sound field. Of note, the sound pressure level of thresholds obtained under ear phones are slightly elevated compared to those in the sound field due to the elimination of the effects of acoustic diffraction and by closed ear cavity effects (Tillman et al., 1966). All experimental protocols adhered to the guidelines of the university’s local ethics committees.

2. Methods 2.1. Participants Eleven listeners (6 male, 5 female; age range: 25e39 years),

1 The mold was applied to the pinna of the normal-hearing ear to disrupt spectral pinna cues, leaving the ear canal open. The molding material used was a siliconbased impression material (egger A/soft; Final degree of hardness: 35 shore A; egger Otoplastik þ Labortechnik GmbH, Germany).

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Fig. 1. Schematic overview of the seven listening conditions for which the localization measurements were conducted.

2.3.2. Test device The Adhear, a non-surgical adhesive bone conduction device (aBCD) (MED-EL, Innsbruck, Austria) was used as the bone conduction stimulator. This device consists of a digital audio processor that attaches to a medical grade adhesive adapter that is placed on the mastoid bone just posterior to the auricle, allowing for consist stimulation position of the aBCD across all test conditions. Devices were set to demonstration mode (maximum gain for presumed normal bone conduction), and maintained in the omnidirectional mode for all experimental conditions. EAR Classic™ foam earplugs (3M© New Zealand Pty, Limited), providing a mean attenuation of 39 dB ± 5 dB SD, from 250 Hz to 8000 Hz (measured by audiometric threshold shifts), were used to simulate the unilateral and bilateral CHL listening conditions. To minimize the occlusion effect deep insertion of the plug flush with the opening of the canal was applied at the tolerance of the participant. The intrinsic variation in occlusion between participants was accepted due to the nature of the study. Effective plugging was confirmed with individual thresholds. Six participants were plugged in the right ear and five in the left ear for the unilateral plugged (UP) condition. To avoid shifting of the air-bone gap during localization measurements, experimental listening conditions were semi-randomized so that plugs were maintained in the ears without the need for replacement. For this reason, test order always began or ended with a randomized combination of conditions c1, c5, c6, or c7. 2.4. Data analysis Best linear fit of the stimulus-response relationship for azimuth was determined using equation (1) and for elevation using equation (2):

aRESP ¼ a,aTARG þ b

(1)

εRESP ¼ a,εTARG þ b

(2)

where aRESP and εRESP are the response azimuth and response elevation (in degrees), and aTARG and εTARG are the target azimuth and target elevation (in degrees). a is the response gain (slope, dimensionless) and b is the response bias (offset in degrees). The coefficient of determination (r2) as well as the mean absolute error (MAE, equation (3)) was also computed:

MAE ¼

Pn  i a i¼1

RESP

  a iTARG 

n

(3)

One-way ANOVA was calculated to determine whether there were any statistically significant differences between conditions and stimulus levels (45, 55 and 65 dBA). 3. Results 3.1. Hearing thresholds Fig. 2 shows the normal hearing thresholds of all 11 participants (25 dB HL) from 250 to 8000 Hz. Bilateral plugging resulted in a mean threshold shift of 39 dB HL, ±5 dB SD, consistent with manufacturer specifications (3M©, 2015). Bilateral aided hearing thresholds were significantly lower compared to bilateral plugged thresholds (c6, 18 dB, ± 3 dB SD, p < 0.0001), and remained elevated compared to normal hearing (20 dB, 6 dB SD, p < 0.0001). Target-response relationships for a single representative participant for all seven listening conditions are depicted in Fig. 3, illustrating the main findings of the study. All unilateral plug (UP)

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Fig. 2. Mean audiometric thresholds for unaided right (red O) and left (blue x), BP (grey:), and bilateral Adhear (green þ) listening. Shaded area represents ±1 SD of the mean. (For interpretation of the references to color in this figure legend, the reader is referred to the Web version of this article.)

Fig. 3. Target-response plots of a representative participant (P7) for all listening conditions (c1 e c7). Stimuli presented here are broadband with levels indicated by white data points (45 dBA), grey data points (55dBA), and black data points (65 dBA).

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conditions (top row, c2 e c4) demonstrate a clear bias towards the direction of the open ear, and the aBCD did not affect the localization abilities (gains 0.4 vs 0.5). In the bilateral plugs (BP) conditions (lower row, c5 e c7) sound localization was clearly affected when listening with one aBCD (c6) and when listening with two aBCDs (c7). Presentation levels of the BB stimuli are indicated (white: 45 dBA, grey: 55 dBA, black: 65 dBA). The black regression line represents the best linear fit. 3.2. Localization performance pooled for all participants 3.2.1. Simulated unilateral conductive hearing loss (c2, c3 and c4) Fig. 4A demonstrates that the use of the aBCD in the UP þ aBCD hearing condition (c3) did not affect the localization performance compared to the UP condition (c2), as evidenced by the overall (i.e. pooled for levels) response gains (g ¼ 0.54 ± 0.16 & 0.52 ± 0.18, respectively). The UP þ aBCD þ contralateral mold (c4) further deteriorates the horizontal localization ability, evidenced by the low response gain (g ¼ 0.21). This indicates a use of monaural spectral cues (derived from the normal hearing ear) for localization of sounds in the azimuth plane. Fig. 4B, demonstrates that all stimuli were perceived (>95%). No effect of the aBCD device is observed for response gains for the UP conditions (c2-c4). Localization performance in azimuth is further disrupted by contralateral pinna mold. 3.2.2. Simulated bilateral conductive hearing loss (c5, c6 and c7) Response gains (Fig. 5) demonstrate good sound source localization in the BP (c5) and BP þ Bilateral aBCD condition (c6). Response gains are consistent with normal hearing performance for audible stimuli (65 dBA). The lowest level (45 dBA) was undetected in the majority of listeners (7/11) when bilaterally plugged. As such, criterion for analysis was set to minimum of 50% detection of stimuli. Review of Fig. 3 demonstrates the typical localization behavior in the BP listening condition (c5). Although overall MAE deviates from normal hearing performance, the responses lie about the predicted line (g ¼ 0.7, r2 ¼ 0.84). This data suggests that when audible (i.e the loudest level, 65 dBA), the participants are able to

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take advantage of binaural cues. Application of bilateral aBCDs to the BP condition (c6) resulted in detection of low (45 dBA) and mid-level (55 dBA) BB stimuli (Fig. 5). Review of Fig. 5 shows that the overall response gains are comparable for c1 and c6, indicating good sound source localization. The localization behavior of P7 (Fig. 3) in this condition (c6), shows high gains (g ¼ 0.8) and high coefficients of determination (r2 ¼ 0.76), comparable to that of c5 (i.e. BP without aBCDs). In c7, when listeners were BP but unilaterally aided, a different localization pattern emerged (Fig. 3). Despite increased audibility, marked reduction in source localization accuracy is observed, as evidenced by the poor correlation between stimulus and response azimuth (r2 ¼ 0.33), the low response gains, g (0.37 ± 0.32), and bias, b (17 ± 19 ). BB stimuli are largely lateralized to the aided ear (Fig. 3), and overall MAE significantly increases compared to the BP (p < 0.0001, post hoc Tukey’s HSD), and the BP þ bilateral aBCDs (p < 0.0001, post hoc Tukey’s HSD) listening conditions (MAE ¼ 38 vs 17 & 17, respectively). The response gains (Fig. 5) demonstrate the significant deterioration in localization performance in c7 compared to the other listening conditions. 3.2.3. Frequency bandwidth (Fig. 6) Review of localization of LP and HP stimuli in the BP but unilaterally aided condition (c7), reveals decreased gains for all stimuli compared to the bilateral aBCD condition (c6). The LP signal is lateralized to the aided ear under the BP condition (b ¼ - 42 ), with poor correlation between stimulus and response azimuth (r2 ¼ 0.20), and low response gains (g ¼ 0.25), whereas high-pass stimuli result in higher response gains (g ¼ 0.56) and a decrease in response bias (b ¼ - 27 ) comparatively. HP signals are not as well detected as BB and LP stimuli when bilaterally plugged (c5). Unilateral aBCD allows for consistent perception of all stimuli, although localization of LP and BB signals is significantly disrupted by the unilateral aBCD (Fig. 6). 4. Discussion This study demonstrates localization abilities with non-invasive

Fig. 4. In (A), box plot of the median, interquartile range, and 95% CI for the response gains of the normal hearing (c1) and unilaterally plugged (c2-4) listening conditions. Percent of stimuli perceived is presented. In (B) performance as a function of level is presented, with the shaded region representing the confidence interval about the mean. No effect of the aBCD device is observed for response gains. Localization performance in azimuth is further disrupted by contralateral pinna mold.

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Fig. 5. In (A), box plot of the median, interquartile range, and 95% confidence interval for the response gains of the normal hearing (c1) and bilaterally plugged (c5-c7) listening conditions. Percent of stimuli perceived is presented. In (B) performance as a function of level is presented, with the shaded region representing the confidence interval about the mean. Gain is not calculated for conditions with < a 20% detection rate.

4.1. Lack of effect of the aBCD in simulated unilateral conductive hearing loss (c2 and c3)

Fig. 6. Performance as a function of frequency is presented for each of the BP listening conditions, with the shaded region representing the confidence interval about the mean. Percent perceived is presented by condition and frequency.

aBCDs in normal hearing listeners under simulated (plugged) unilateral and bilateral CHL conditions. Binaural hearing is dependent on processing of ITDs, ILDs, and phase differences (Yin et al., 2019). The known hearing deficits that arise from inability to take advantage of binaural cues are often deleterious. In an effort to assist individuals with hearing loss to gain access to binaural cues, bilateral stimulation has become the gold standard in hearing rehabilitation. Nevertheless, the binaural benefits of this approach with BCDs remain somewhat elusive (Agterberg et al., 2011a; Kunst et al., 2008; Vogt et al., 2019). A variety of factors can influence the processing of these cues, such as symmetry in hearing thresholds (Durlach et al., 1986; Hunig and Burg, 1991) and audibility of the signal (Sabin et al., 2005). In aided listeners, additional factors such as stimulation mode and processing delays may also disrupt these cues.

In the described population, no effect of the aBCD is seen in the unilateral plugged listeners. This can be explained by Fig. 2, where aided thresholds (BP þ bilateral aBCD) demonstrate that a significant asymmetry remains between normal hearing and the aided aBCD thresholds. Others have noted that for binaural hearing benefit, thresholds should not differ by more than 10 dB HL between ears (Bosman et al., 2001; Janssen et al., 2012). The mean interaural threshold difference in the UP þ aBCD (c3) condition exceeded 10 dB HL at all but one frequency (1000 Hz), and increased up to 30 dB HL. ILDs play a significant role in sound localization. The human auditory system is able to detect minimal differences between the ears with studies demonstrating average ILD thresholds of roughly 1e4 dB (Bernstein, 2004; Yost and Dye, 1988). The inability of the aBCD to reach the normal hearing ear thresholds and establish symmetry may account for these findings. When looking at the results in UP þ aBCD condition (c3, Fig. 3), it is clear that the listeners are relying on the normal hearing ear. Localization behavior demonstrates near-normal performance on the open ear side (Fig. 3), with larger errors on the plugged side. Not only is localization not improved by use of the aBCD, but molding of the open ear pinna results in a further deterioration in localization, demonstrating the reliance on the monaural spectral cues of the normal hearing (open) ear, confirming recent observations in children with unilateral CHL listening with a percutaneous BCD (Vogt et al., 2019). The interaural differences in c3 are too great to be perceived as reliable input, and the better ear continues to dominate. This may also be related to the relatively long processing time delays in the studied aBCD, which is 8e10 ms and frequency dependent. The present findings represent transcutaneous aBCD stimulation. Asymmetries are expected to be less significant in BCDs using direct drive stimulation to the bone, and may be resolved with increased gain of power devices. For example, previous research has shown that in acquired unilateral conductive losses (Agterberg et al., 2011a), and in children with congenital

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unilateral conductive hearing loss (Vogt et al., 2019) directional hearing improved with a percutaneous BCD for some participants. BCDs in general have a reduced dynamic range (Snik et al., 2015). As a result, subtle differences in level become obscured and difficult to differentiate. 4.2. Simulated bilateral conductive hearing loss (c5) When looking at group performance, low-level stimuli were largely undetected in the BP condition (c5, Fig. 5). Interestingly, for high-level stimuli that exceeded the plugged hearing thresholds, response gains in c5 were close to that observed in the normal hearing condition. This suggests that when audible, listeners were able to make good use of the available cues. This finding lends itself to the importance of symmetry. Bilateral plugging resulted in a disruption of binaural cues, although relatively small in degree (Figs. 3 and 5). While the plugs introduce both a reduction in level and a timing delay in the signal (Kumpik et al., 2010), this occurs in both ears similarly enough to result in nearly accurate sound source localization. 4.2.1. Bilateral plug þ bilateral aBCD (c6) The BP þ bilateral aBCD condition (c6) allowed for detection of the low-level stimuli (45 dB SPL). Moreover, listeners were able to localize these stimuli with a high degree of accuracy. Response gains reached that of normal hearing performance for all levels (Fig. 5), although the target response plots (Fig. 3) indicate larger scatter, and a worse MAE (p < 0.05) in comparison to the normal hearing condition. As seen with the unaided BP condition (c5), symmetry likely plays an important role in the good source localization observed in this condition. 4.2.2. Bilateral plug þ unilateral aBCD (c7) Unilateral application of the aBCD in the BP listening conditions (c7), however, results in a clear localization bias towards the aBCD side. Here, we observed large deviations in performance for BP individuals using a single aBCD (Figs. 3, 5 and 6). There is clear evidence that bilateral amplification, provides the best possible aided performance, where adding the second aBCD optimally improved the response gains. The data here suggests that when bilaterally plugged but unilaterally aided, performance not only deviates significantly from this, but may disrupt the binaural processing of audible cues (c5). This might be related at least in part to the cross hearing that occurs with bone-conduction stimulation, which manipulates ITD cues (Agterberg et al., 2011b; Stenfelt, 2012; Stenfelt and Zeitooni, 2013). In contrast to the bilateral aBCD condition (c6), LP stimuli were not as well located as HP stimuli (Fig. 6), evidence of the ITD disruption with unilateral aBCD. Unilateral stimulation by bone conduction under bilaterally occluded listening, changes the ITD cue, thereby increasing the bias toward the aided ear. The low frequency ITD cue is dominant in sound source localization (Wightman and Kistler, 1992), and it has been shown that when this is disrupted, listeners rely primarily on intensity differences to make judgments about sound location (Yost and Dye, 1988). Although bilateral stimulation is possible with a unilateral BCD, the abnormal intensity coding that arises disrupts binaural input, even for signals well above the unaided threshold (Fig. 5). In summary, these findings demonstrate that asymmetric hearing creates larger than normal thresholds for detecting ITD and ILDs, leading to reduced localization abilities. Binaural cues are more perturbed by asymmetries in hearing than by elevation of threshold. This is evidenced by the larger localization errors and decreased gain observed in conditions c2 (UP), c3 (UP þ ipsilateral aBCD), and c7 (BP þ unilateral aBCD), than in c5 (BPs alone) and c6

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(BPs þ bilateral aBCDs) where thresholds are elevated but symmetric. All experiments described here utilize the non-invasive Adhear BCD system, which stimulates the hearing organs transcutaneously. Studies indicate that the amplification of this aBCD is similar to BCDs on a softband or headband (Brill et al., 2019; Neumann et al., 2019; Skarzynski et al., 2019). Although, performance patterns of a normal hearing population cannot be directly related to that which is expected in patients with non-normal and/or asymmetric bone conduction thresholds, or in those utilizing direct drive implantable BCDs. Future studies are needed to build upon this data to investigate these findings in patients with conductive hearing loss. Additionally, the participants described here were plugged normal hearing listeners, which does not uniformly represent the unilateral/bilateral CHL patients. 5. Conclusions Sound localization abilities are disrupted by asymmetric hearing. No effect of the aBCD is observed in the UP þ unilateral aBCD condition. This is likely due to the residual asymmetry in bone conduction hearing thresholds observed with the aBCD. Furthermore, results in the UP þ unilateral aBCD condition are expected to be due in part to the transcutaneous pathway, which results in a reduction of gain for signals transmitted by bone conduction. Bilateral aided stimulation provided the best benefit in BP conditions. In this listening condition, aBCDs restored audibility of lowlevel stimuli, and resulted in optimal localization performance for these softer sound levels, demonstrating the importance of bilateral stimulation for bilateral CHL. CRediT authorship contribution statement Hillary Snapp: Conceptualization, Methodology, Formal analysis, Investigation, Writing - original draft. Katharina Vogt: Formal analysis, Writing - review & editing. Martijn J.H. Agterberg: Conceptualization, Methodology, Writing - review & editing, Project administration. Acknowledgements This research was funded by the William Demants og Hustru Ida Emilies Fond (MA), the FP7-PEOPLE-2013-ITN Marie Curie Initial Training Network iCare (KV and MA) and the Radboud University (MA). Appendix A. Supplementary data Supplementary data to this article can be found online at https://doi.org/10.1016/j.heares.2019.107881. References 3M©, 2015. Laboratory attenuation data for 3m hearing protection [Online] Retrieved from. http://multimedia.3m.com/mws/media/1087607O/laboratoryattenuation-data-for-3m-hearing-protection-products.pdf. verified 10/1/2018. Agterberg, M.J., Hol, M.K., Cremers, C.W., Mylanus, E.A., van Opstal, J., Snik, A.F., 2011a. Conductive hearing loss and bone conduction devices: restored binaural hearing? Adv. Oto Rhino Laryngol. 71, 84e91. Agterberg, M.J., Snik, A.F., Hol, M.K., van Esch, T.E., Cremers, C.W., Van Wanrooij, M.M., Van Opstal, A.J., 2011b. Improved horizontal directional hearing in bone conduction device users with acquired unilateral conductive hearing loss. J Assoc Res Otolaryngol 12, 1e11. Agterberg, M.J., Snik, A.F., Hol, M.K., Van Wanrooij, M.M., Van Opstal, A.J., 2012. Contribution of monaural and binaural cues to sound localization in listeners with acquired unilateral conductive hearing loss: improved directional hearing with a bone-conduction device. Hear. Res. 286, 9e18. Asp, F., Reinfeldt, S., 2018. Horizontal sound localisation accuracy in individuals

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