Potential Advantages from Bilateral Cochlear Implants By Ruth Litovsky, Ph.D.

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1 Potential Advantages from Bilateral Cochlear Implants By Ruth Litovsky, Ph.D. ABSTRACT It is well known that, in normal hearing persons, binaural hearing (hearing with two ears) is generally superior to monaural hearing. Today, bilateral cochlear implants (BI-CIs) are offered to a growing number of individuals, including adults and children, in order to provide benefits arising from having two ears. For many deaf persons BI-CIs present an ideal option because BI-CIs provide auditory information that is simply not available when a single ear is stimulated. Potential advantages from BI-CIs vary, depending on the ability of the user to take advantage of various acoustic cues that occur in everyday complex acoustic environments. It is important to keep in mind whether one of the ears should be saved for future treatments or improved technology. At the same time, one must carefully consider whether the central nervous system is most receptive to stimulation during early stages of development, and therefore, whether prolonged auditory deprivation in one of the ears reduces the extent to which the auditory system will later be able to integrate information from the two ears. This paper outlines the potential ways in which someone with BI-CIs might demonstrate benefits in her ability to function. Published work has pointed to improvements in the ability of recipients to understand speech in noise, segregate multiple signals and localize sounds (see references). Other improvements that have not been systematically measured, but have the potential to be, include facilitation of language acquisition, learning, cognition and memory, the fact that the better ear is guaranteed to be implanted and improved quality of life. DEFINITION OF KEY TERMS BI-CI: Bilateral Cochlear Implants: Cochlear implants placed in the two cochleae of an individual patient. This can be achieved either simultaneously (same surgery) or sequentially (separate surgeries). Binaural: Binaural refers to the integration of input along the auditory pathway after both ears are presented with the sound, as happens in the normal auditory system. Bilateral: Bilateral input occurs when both ears are presented with sound. Unlike binaural hearing, coordination of sounds presented to the two ears may not occur. Cochlear implants (CIs) are used increasingly to provide hearing to deaf and hard of hearing individuals who experience little or no benefit from amplification. Adults and children alike can use sound provided by CIs to interpret incoming speech signals. Unilateral CI recipients tend to receive significant benefit, such that most adult users understand the majority of speech and communicate with minimal or no lip reading, especially in quiet listening environments. In addition, many children with a cochlear implant can learn in mainstream environments and communicate with their hearing peers. However, there are variations in the performance of CI users. In part, this is because CI users encounter difficulty when understanding speech in noisy environments, and struggle to find ways to improve communication in their social interactions and the work place. For children, the same issues apply in learning environments, such as classrooms, which are typically filled with noise, reverberation and competing signals. In addition, most CI users report that they cannot locate the position of sound sources, and that all sounds appear to come from inside their ear or behind their ear.

2 Binaural hearing can be especially important in alleviating some of these difficulties, which limit the ability of CI users to orient in the environment and to function easily in complex acoustic spaces. In an effort to improve the audibility and intelligibility of speech signals that occur in noise, and to improve sound localization, bilateral CIs (BI-CI) are being provided to a growing number of patients. To date, several thousand individuals have been implanted bilaterally worldwide, most in procedures that occur months or years apart. Another approach is that of simultaneous implantation in both ears. The growing recommendation and use of BI-CIs in addition to published outcomes data suggest that this approach is no longer considered experimental in appropriately counseled and selected individuals. One might ask why there are increasing recommendations from medical professionals to provide CIs in both ears, rather than adherence to unilateral implantation. The first and most important issue to remind ourselves of is that multi-channel CIs have only been available for a couple of decades, and until they were proven to be highly successful there were good reasons to withhold implantation in both ears. Since CIs are generally accepted as the standard of treatment for severe to profoundly hearing impaired persons who want to hear, the next step is to determine if one or both ears should be implanted and if binaural advantages can be achieved with 2 CIs. Prior to making a decision to implant both cochleae, it is important to consider whether potential drawbacks exist that would have to be accounted for at a later time. For instance, there is an ongoing search for cures for deafness, such as genetic and stem cell therapy, or hair-cell regeneration. It is likely that the physical presence of a CI within the cochlea would conflict with the ability of that organ to respond effectively to regeneration of hair cells, because of the formation of scar tissue and other damage that may be incurred. Stem cells on the other hand, might work in congruence with a CI and provide more effective means of conjointly stimulating the auditory system (e.g., Rejali et al., 2007; Coleman et al., 2007). While these therapies and their potential are extremely exciting, their viability in the mammalian cochlea remains to be fully demonstrated. Therefore, they are not likely to be made medically available within the next decade, possibly longer. With regard to implantable hearing technology, it is likely that implantable devices will undergo further refinement and improvement. This reality raises issues for both adults and children, for whom optimal auditory stimulation is equally important. In addition to bearing in mind issues regarding peripheral stimulation at the level of the cochlea, it is important to take into account the impact of central processing factors and the impact that unilateral vs. bilateral implantation might have on those. These considerations should be incorporated into candidate counseling procedures; to ensure that adult candidates and parents of minors are aware of the potential trade-offs during the decision making process. For children, the issue of auditory plasticity is of the essence. The nervous system is equipped with neural circuits that depend on stimulation. While these circuits are robust, and can respond to stimulation after years of deprivation, success is likely to be maximal if stimulation occurs during early stages in development. If hearing loss is profound in both ears and amplification offers no benefits, then one is left with the following implant choices: (1) Implant both ears early during development, but risk loss of opportunity for at least some of the technology that is likely to be available during a child s life-time. (2) Implant one ear early, and save the second ear for future technology, but risk the potential loss of fidelity with which the auditory system can be bilaterally activated following a prolonged period of deprivation. If one ear has residual hearing and amplification might offer benefits, care should be taken to assess the extent of those benefits prior to embarking on implantation of both ears. The remainder of this paper attempts to outline the potential benefits that can arise when both ears are implanted compared with unilateral implantation. The following section describes these benefits, but it is important to bear in mind the notion that the extent to which they occur will depend on many individual factors, such as the age of the recipient, duration of pre-implantation auditory deprivation, the integrity and survival of neurons being stimulated, and possibly whether the implantation is simultaneous vs. sequential.

3 (1) Bilateral and/or Binaural Hearing: Sounds that occur in the environment are received by the ears after they have bounced off and been transformed by the head/shoulders and by the shape of the ears themselves. Figure 1 shows a simplified diagram (left) of a situation in which the sound source is nearer to left ear. On the right, a graph of relative cues that arise as a result of the interaction between sounds and a person s external anatomy are shown for the two ears. These are discussed in the preceding paper in this series (Litovsky, 2006). Briefly, each location in space around the head will create a different set of interaural cues, consisting of either timing or level differences between the two ears. For instance, a sound that is at 90 degrees to the right will create an interaural timing difference (ITD) of about 0.7 seconds; a sound that is directly in front will have an ITD equal to 0; a sound that is at about 45 degrees will have an ITD of 0.4 seconds. Similarly, interaural level differences are created by the shadowing of the stimulus as it travels around the head. These cues are coded by specialized neural circuits in the brainstem and at higher levels in the auditory system that are dedicated to comparing information received from the right and left ears. The cues that occur for two-eared mammals are known to help an individual with sound localization, suppression of echoes and segregation of speech from competing sounds (other speech or noise) (Middlebrooks and Green, 1991; Litovsky et al., 1999; Bronkhorst, 2000). In the context of this paper, it is important to differentiate between the term, bilateral, which refers to having two functional ears, and binaural, which refers to the underlying perceptual/physiological mechanisms that process sounds at the two ears and throughout the central auditory system. Binaural processing requires bilateral hearing and ensures coordination between the inputs arriving at the two ears. Remarkably, a person with BI-CIs can experience significant benefits when listening with two vs. one CI. In this situation, the fact that each ear receives a signal means that the brain is able to glean two looks at auditory information. For instance, the brain can compare overall disparities between the ears in sound level, resulting in inter-aural level differences (ILDs), which are known to be important for spatial hearing (van Hoesel, 2004). Some gross differences in timing of sounds between the ears might also occur, but are not well documented nor is their benefit understood (van Hoesel, 2004). Most users of BI-CIs are able to take advantage of at least some or all of these auditory cues. Hence, present bilateral hearing can most likely offer the following advantages compared with using a single CI: (1) Ability to localize sounds. For adults, this translates directly to situations in the work place, social situations, recreational sport activities, and everyday activities such as crossing the street in traffic. Numerous studies have documented the added benefit of two CIs for adults in controlled laboratory environments (e.g., van Hoesel and Tyler, 2003; Schoen et al., 2005; Newman et al., 2007). Examples of results collected from 17 Nucleus 24 users are shown in Figures 2 and 3. These studies generally show that under somewhat non-challenging conditions, some BI-CI users are able to localize sounds nearly as well as normal hearing listeners, i.e., their localization error rate can be very low. However, under challenging conditions, such as when the number of loudspeakers in the room is larger and in the presence of noise, BI-CI recipients still perform significantly worse than normal-hearing counterparts (e.g., Grantham et al., 2007). Other than anecdotal reports from bilateral recipients, little is known about documented benefits in realistic situations. For children, the issue of sound localization also translates directly to everyday situations, including the need to monitor multiple ongoing sound sources in classrooms, playground situations and sports activities; safety becomes an issue when the need arises to avoid moving objects, cross a busy street, etc. Recent studies have also shown that sound localization precision in children with bilateral implants is better when listening with two implants compared with one, and better than in children who have a CI in one ear and a hearing aid in the opposite ear (Litovsky et al., 2006a; 2006b)

4 (2) Ability to hear significantly better in noisy environments. This general area can be further subdivided into advantages that might include the ability to segregate speech from background sounds and ability to monitor more than one ongoing important source(s) of information. The former has been studied fairly extensively in both normal hearing persons and in BI-CI users. When both ears are functional, speech intelligibility in noise can improve dramatically compared with unilateral listening. Many complex factors contribute to the ability to separate speech signals from background noise including signal and masker characteristics, and degree of hearing impairment (for a review, see Bronkhorst, 2000). There are, however, three specific components of bilateral hearing that are known to potentially contribute to an advantage (Dillon, 2001). The first component is related to the physical head shadow effect. When speech and competing noise are spatially separated, the signal-to-noise ratio (SNR) at each ear is disparate due to differential filtering of sounds (primarily high frequency) by the physical presence of the head. If both ears are functional the listener can selectively attend to the ear with the more favorable SNR (i.e., the ear opposite to the noise source) to maximize speech recognition performance (as compared with the unfavorable situation where only the ear with the poorer SNR is functional). Another component of bilateral hearing is commonly called the binaural squelch effect. If there is functional input from both ears, the auditory system potentially can combine the information to form a better central representation than that available with only monaural input. This occurs when inter-aural timing and intensity cues arise under conditions of spatial separation of signal and noise. These binaural cues are utilized in centrally-mediated source segregation mechanisms that can significantly improve speech understanding. A third component of bilateral hearing, known as binaural redundancy or summation is thought to occur when speech and noise originate from the same location. Binaural redundancy refers to the auditory system s ability to centrally combine and derive benefit from duplicate representations of the same signal to the two ears. Hearing threshold improves for binaural versus monaural presentation to normal ears, resulting in increased perceptual loudness. These three benefits have been reported in numerous BI-CI users (e.g., van Hoesel and Tyler, 2003; Schleich et al., 2004; Litovsky et al., 2006c; Tyler et al. 2007). Examples of results collected in 17 Nucleus 24 users are shown in Figure 4 (3) Facilitation of language acquisition, learning, cognition and memory. Having two ears provides redundancy in sensory input. By having an incoming signal processed in parallel by both ears, and reach the brain from both sides, there is a higher likelihood that a bilateral CI listener will process the signal more easily. When it comes to parsing out segments of speech, linking the meaning and production patterns to the auditory signal, it is possible that doubling the incoming signal will have facilitatory effects. Furthermore, adults who wear BI-CIs report, anecdotally, that they experience increased ease in their ability to monitor their environment; some say they feel that their cognitive abilities are enhanced, because they can maximize information intake without having to work as hard to extract information from incoming signals. While this aspect of bilateral hearing should be carefully quantified, anecdotal reports from adults point to specific directions where one might look for additional benefits from BI-CIs in children and adults, and should be the topic of future investigations.

5 (4) Implanting the better ear is guaranteed. From a clinical perspective, when a single CI is provided, determining which ear to implant is not always a straightforward choice. Sometimes the ear that has poorer residual hearing is implanted first, in the hope that the second ear would still benefit from a hearing aid or other forms of treatment. In other cases, the ear with better hearing is implanted with the aim of maximizing success from the implant. These choices are often difficult to make and outcomes are not consistently predictable from pre-implantation performance on perceptual measures. The lack of consistency and predictability are borne out when post-implantation performance is evaluated in BI-CI users; the two ears are often asymmetrical such that one ear clearly offers better hearing than the other (Litovsky et al., 2006c). Thus, in addition to the fact that most CI users can take advantage of the combined inputs to the two ears, when BI-CIs are provided, many of these issues are nullified, because either way the better ear is always implanted. Similarly, when listening in noise that is to one side of the head or another, regardless of where the target is located, the listener is always afforded an ear with a better SNR. (5) Quality of life. Subjective reports provided by BI-CI users indicate that most of these recipients enjoy an ease of functioning that comes from hearing with both ears, and have a strong preference for using both CIs together rather than using either ear alone. They report that when they are scanning their auditory scene to determine which sources are present at what location, and when, there are fewer demands on their attention. Although extensive work in this area has not been conducted, quality of life measures that include the Abbreviated Profile of Hearing Aid Benefit (APHAB) as a measure of subjective benefit are beginning to emerge (Litovsky et al., 2006c; Summerfield et al., 2006; Wackym et al., 2006). Another powerful tool that has been used to evaluate subjective quality of life changes when wearing bilateral hearing aids, and that is being adapted to BI-CI users, is the Speech, Spatial and Qualities of Hearing Scale (SSQ) developed by Gatehouse and Noble (2004). Most compelling though, is the fact that the vast majority of BI-CI users report substantial qualitative improvements in their ability to function in everyday life. These are yet to be carefully studied and captured quantitatively. Examples of situations that can lead to improved functioning include: Having a conversation around a dinner table; conducting a meeting at a work-place, i.e. when sitting around a table surrounded by multiple conversations; while driving in the car and monitoring road traffic or listening for an ambulance; maneuvering in the dark; participating in sports; and many more. Overall, under these situations, there are psychological factors that seem to be affected when BI-CI users function with one vs. two devices. In our lab we have conducted anecdotal interviews with several dozen recipients, and we have the overwhelming impression that these individuals self-perception of their own functioning is that stress levels are reduced and confidence is enhanced when using both implants compared with one. The vast majority of recipients prefer to use both implants on a daily basis and report discomfort, stress and lack of confidence in their auditory skills when one of the devices is not activated. While these changes in quality of life have not been carefully studied, they merit serious consideration for future work. A recent study by Litovsky et al. (2006c) used the Ease of Communication, Background Noise, and Reverberation subscales of the APHAB questionnaire to quantify some of these subjective impressions. Results from that study are shown in Figure 5. In summary, in order to improve the ability of adults and children to hear in noise and to localize sounds, CI recipients have received implants in both ears, otherwise known as BI-CIs. Outcome measures suggest that these benefits (sound localization, hearing better in noisy environments, implanting the better ear, quality of life) are present in the majority of recipients, although their performance is still not at the level of normal-hearing listeners with true binaural capabilities. Other improvements that have not been systematically measured, but have the potential to be measured include facilitation of language acquisition, learning, cognition and memory, the fact that the better ear is guaranteed to be implanted and better quality of life.

6 REFERENCES Bronkhorst, A. (2000). The cocktail party phenomenon: a review of research on speech intelligibility in multiple-talker conditions. Acustica, 86, Coleman B, de Silva MG, Shepherd RK. (2007). The Potential of Stem Cells for Auditory Neuron Generation and Replacement. Stem Cells. Jul 26; [Epub ahead of print] Dillon, H. (2001). Binaural and bilateral considerations in hearing aid fitting. In: Hearing Aids (pp ). Turramurra, Australia: Boomerang Press. Gatehouse S, Noble W. (2004). The Speech, Spatial and Qualities of Hearing Scale (SSQ). Int J Audiol. 43(2): Grantham DW, Ashmead DH, Ricketts TA, Labadie RF, Haynes DS. (2007). Horizontal-plane localization of noise and speech signals by postlingually deafened adults fitted with bilateral cochlear implants. Ear Hear. 28(4): Litovsky RY, Colburn HS, Yost WA, Guzman SJ. (1999). The precedence effect. J Acoust Soc Am. 106(4 Pt 1): Litovsky, R. Y., Johnstone, P. M., Godar, S., Agrawal, S., Parkinson, A., Peters, R., Lake, J. (2006a). Bilateral cochlear implants in children: localization acuity measured with minimum audible angle. Ear and Hearing, 27, Litovsky, R. Y., Johnstone, P. M., Godar, S. P. (2006b). Benefits of bilateral cochlear implants and/or hearing aids in children. Int J Audiol, 45 (Suppl), Litovsky R, Parkinson A, Arcaroli J, Sammeth C. (2006c). Simultaneous bilateral cochlear implantation in adults: a multicenter clinical study. Ear Hear. 27(6): Litovsky, R.Y. (2006). Binaural Hearing. White papers series, published by Cochlear Americas, February. Middlebrooks JC, Green DM. (1991). Sound localization by human listeners. Annu Rev Psychol. 42: Review. Neuman AC, Haravon A, Sislian N, Waltzman SB. (2007). Sound-direction identification with bilateral cochlear implants. Ear Hear. 28(1): Rejali D, Lee VA, Abrashkin KA, Humayun N, Swiderski DL, Raphael Y.(2007). Cochlear implants and ex vivo BDNF gene therapy protect spiral ganglion neurons. Hear Res. Jun;228(1-2): Epub 2007 Mar 7. Schleich, P., Nopp, P, D Haese, P. (2004). Head shadow, squelch, and summation effects in bilateral users of the MED-EL COMBI 40/40_ cochlear implant. Ear and Hearing, 25, Schoen F, Mueller J, Helms J, Nopp P. (2005). Sound localization and sensitivity to interaural cues in bilateral users of the Med-El Combi 40/40+cochlear implant system. Otol Neurotol. 26(3): Summerfield, QA, Barton GR, Toner J, et al., (2006). Self-reported benefits from successive bilateral cochlear implantation in post-lingually deafened adults: randomised controlled trial. Int J Audiol. 45 Suppl 1:S Tyler RS, Dunn CC, Witt SA, Noble WG. (2007). Speech perception and localization with adults with bilateral sequential cochlear implants. Ear Hear. 28(2 Suppl):86S-90S. van Hoesel, R. J. M. (2004). Exploring the benefits of bilateral cochlear implants. Audiology and Neuro-Otology, 9, van Hoesel, R. J. M., Tyler, R. S. (2003). Speech perception, localization, and lateralization with bilateral cochlear implants. Journal of the Acoustical Society of America, 113, Wackym PA, Runge-Samuelson CL, Firszt JB, Alkaf FM, Burg LS. (2007). More challenging speech-perception tasks demonstrate binaural benefit in bilateral cochlear implant users. Ear Hear. 28(2 Suppl):80S-85S.

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