Development of Sound Localization Strategies in Children with Bilateral Cochlear Implants

RESEARCH ARTICLE Development of Sound Localization Strategies in Children with Bilateral Cochlear Implants Yi Zheng¤, Shelly P. Godar, Ruth Y. Litovsky* Waisman Center, University of Wisconsin Madison, Madison, Wisconsin, United States of America ¤ Current address: Institut d’Etudes de la Cognition, Ecole Normale Supérieure, Paris, France * Abstract OPEN ACCESS Citation: Zheng Y, Godar SP, Litovsky RY (2015) Development of Sound Localization Strategies in Children with Bilateral Cochlear Implants. PLoS ONE 10(8): e0135790. doi:10.1371/journal.pone.0135790 Editor: Frederic Dick, Birkbeck College, UNITED KINGDOM Received: September 9, 2014 Accepted: July 27, 2015 Published: August 19, 2015 Copyright: © 2015 Zheng et al. This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. Data Availability Statement: Files necessary to replicate the study, including stimuli and matlab code for data analysis, are held in Dryad at doi: 10.5061/ dryad.0m09h. The authors can also be contacted for assistance or further details at www.waisman.wisc. edu/bhl or . Funding: This work was supported by National Institutes of Health, Grant 5R01-DC008365, 2P30HD003352 http://www.nih.gov. Competing Interests: The authors have declared that no competing interests exist. Localizing sounds in our environment is one of the fundamental perceptual abilities that enable humans to communicate, and to remain safe. Because the acoustic cues necessary for computing source locations consist of differences between the two ears in signal intensity and arrival time, sound localization is fairly poor when a single ear is available. In adults who become deaf and are fitted with cochlear implants (CIs) sound localization is known to improve when bilateral CIs (BiCIs) are used compared to when a single CI is used. The aim of the present study was to investigate the emergence of spatial hearing sensitivity in children who use BiCIs, with a particular focus on the development of behavioral localization patterns when stimuli are presented in free-field horizontal acoustic space. A new analysis was implemented to quantify patterns observed in children for mapping acoustic space to a spatially relevant perceptual representation. Children with normal hearing were found to distribute their responses in a manner that demonstrated high spatial sensitivity. In contrast, children with BiCIs tended to classify sound source locations to the left and right; with increased bilateral hearing experience, they developed a perceptual map of space that was better aligned with the acoustic space. The results indicate experience-dependent refinement of spatial hearing skills in children with CIs. Localization strategies appear to undergo transitions from sound source categorization strategies to more fine-grained location identification strategies. This may provide evidence for neural plasticity, with implications for training of spatial hearing ability in CI users. Introduction The number of children receiving cochlear implants (CIs) in both ears (bilateral CIs; BiCIs) has grown in recent years. This clinical trend is, in part, motivated by the fact that post-lingually deafened adults demonstrate significant benefits on measures of sound localization, and speech understanding in the presence of interfering stimuli, when using BiCIs compared with a single-CI listening mode [1–3]. Studies on spatial hearing in children who are fitted with BiCIs PLOS ONE | DOI:10.1371/journal.pone.0135790 August 19, 2015 1 / 24 Emerging Localization Strategies in Pediatric Cochlear Implant Users offer opportunities to understand both basic neuroscience issues, and clinically relevant issues. Early research in this population showed that, during the first year after bilateral activation, performance on spatial hearing tasks is better with BiCIs than with a single CI [4]. At a clinical level, parents on behalf of their children are making decisions as to whether the children should receive one or two CIs. What remains to be better understood is the extent to which children with BiCIs will be able to function similarly to children with normal hearing (NH). The bilaterally implanted pediatric population offers a compelling opportunity to investigate whether spatial hearing skills can emerge in a human whose auditory system was deprived of hearing at birth. More so, many of the children received sequential implantation, thus, they experienced a period of monaural deprivation during the time that the first CI was activated; subsequently they transitioned to hearing bilaterally. The unique experiences of these children who are fitted with BiCIs may influence the development of spatial hearing skills and binaural encoding capacity. There is evidence that humans [5] and animals [6, 7]learn to localize sound early during development, and that experience-induced plasticity is greatest during this time period. These studies indicate that neural circuitry underlying sound localization is calibrated through ongoing experience with available spatial cues. In humans, behavioral studies of sound localization typically use two different psychophysical methods. One type of task measures the smallest sound source separation in space that subjects can reliably discriminate. This type of a “relative” task is exemplified by the measure of minimum audible angle (MAA) [8]. Indeed, it has been found that children who received BiCIs after age 4 exhibited MAA thresholds near 20° [9]; in contrast, best-performing NH children have MAA thresholds as low as 3° by 2 years of age [9] and 1-2° by 5 years of age[10]. The average thresholds are approximately 6° for stimuli presented at static levels [9]. In 2-year old BiCIs users whose CIs were activated by age 12 months, MAAs can be within normal limits, but this is not the case for all children [4]. Although the MAA task can be used to evaluate subjects’ spatial acuity, it provides little information regarding subjects’ ability to map spatial locations, nor regarding localization accuracy. Absolute sound localization is a measure of listeners’ ability to specify the absolute location of a sound source. Several studies with children who use CIs have implemented this approach to investigate spatial hearing skills in the horizontal plane. A standard metric for quantifying listeners’ performance is the root mean square (RMS) error over the entire source array, with lower RMS values representing better performance. Litovsky et al. [2] were the first to implement this approach in pediatric BiCIs users, testing the first 3 children in this unique population using an array of 15-loudspeakers, spanning from -70° to 70°. These children were 8–12 years old at the time that they received the second CI, and only had 3 months of experience with the second CI. Results (...truncated)