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      Development of Sound Localization Strategies in Children with Bilateral Cochlear Implants

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          Abstract

          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.

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          Most cited references41

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          A place theory of sound localization.

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            A neural code for low-frequency sound localization in mammals.

            We report a systematic relationship between sound-frequency tuning and sensitivity to interaural time delays for neurons in the midbrain nucleus of the inferior colliculus; neurons with relatively low best frequencies (BFs) showed response peaks at long delays, whereas neurons with relatively high BFs showed response peaks at short delays. The consequence of this relationship is that the steepest region of the function relating discharge rate to interaural time delay (ITD) fell close to midline for all neurons irrespective of BF. These data provide support for a processing of the output of coincidence detectors subserving low-frequency sound localization in which the location of a sound source is determined by the activity in two broad, hemispheric spatial channels, rather than numerous channels tuned to discrete spatial positions.
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              Speech perception, localization, and lateralization with bilateral cochlear implants.

              Five bilateral cochlear implant users were tested for their localization abilities and speech understanding in noise, for both monaural and binaural listening conditions. They also participated in lateralization tasks to assess the impact of variations in interaural time delays (ITDs) and interaural level differences (ILDs) for electrical pulse trains under direct computer control. The localization task used pink noise bursts presented from an eight-loudspeaker array spanning an arc of approximately 108 degrees in front of the listeners at ear level (0-degree elevation). Subjects showed large benefits from bilateral device use compared to either side alone. Typical root-mean-square (rms) averaged errors across all eight loudspeakers in the array were about 10 degrees for bilateral device use and ranged from 20 degrees to 60 degrees using either ear alone. Speech reception thresholds (SRTs) were measured for sentences presented from directly in front of the listeners (0 degrees) in spectrally matching speech-weighted noise at either 0 degrees, +90 degrees or -90 degrees for four subjects out of five tested who could perform the task. For noise to either side, bilateral device use showed a substantial benefit over unilateral device use when noise was ipsilateral to the unilateral device. This was primarily because of monaural head-shadow effects, which resulted in robust SRT improvements (P<0.001) of about 4 to 5 dB when ipsilateral and contralateral noise positions were compared. The additional benefit of using both ears compared to the shadowed ear (i.e., binaural unmasking) was only 1 or 2 dB and less robust (P = 0.04). Results from the lateralization studies showed consistently good sensitivity to ILDs; better than the smallest level adjustment available in the implants (0.17 dB) for some subjects. Sensitivity to ITDs was moderate on the other hand, typically of the order of 100 micros. ITD sensitivity deteriorated rapidly when stimulation rates for unmodulated pulse-trains increased above a few hundred Hz but at 800 pps showed sensitivity comparable to 50-pps pulse-trains when a 50-Hz modulation was applied. In our opinion, these results clearly demonstrate important benefits are available from bilateral implantation, both for localizing sounds (in quiet) and for listening in noise when signal and noise sources are spatially separated. The data do indicate, however, that effects of interaural timing cues are weaker than those from interaural level cues and according to our psychophysical findings rely on the availability of low-rate information below a few hundred Hz.
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                Author and article information

                Contributors
                Role: Editor
                Journal
                PLoS One
                PLoS ONE
                plos
                plosone
                PLoS ONE
                Public Library of Science (San Francisco, CA USA )
                1932-6203
                19 August 2015
                2015
                : 10
                : 8
                : e0135790
                Affiliations
                [001]Waisman Center, University of Wisconsin Madison, Madison, Wisconsin, United States of America
                Birkbeck College, UNITED KINGDOM
                Author notes

                Competing Interests: The authors have declared that no competing interests exist.

                Conceived and designed the experiments: YZ RL. Performed the experiments: YZ SG RL. Analyzed the data: YZ SG RL. Contributed reagents/materials/analysis tools: YZ RL. Wrote the paper: YZ SG RL. Designed the software used in analysis: RL YZ.

                [¤]

                Current address: Institut d’Etudes de la Cognition, Ecole Normale Supérieure, Paris, France

                Article
                PONE-D-14-40054
                10.1371/journal.pone.0135790
                4545829
                26288142
                b5284cb1-b64b-4547-a2af-268e72839f39
                Copyright @ 2015

                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

                History
                : 9 September 2014
                : 27 July 2015
                Page count
                Figures: 8, Tables: 3, Pages: 24
                Funding
                This work was supported by National Institutes of Health, Grant 5R01-DC008365, 2P30-HD003352 http://www.nih.gov.
                Categories
                Research Article
                Custom metadata
                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 litovsky@ 123456waisman.wisc.edu .

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