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      Context-Specific Reweighting of Auditory Spatial Cues following Altered Experience during Development

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      1 , , 1 , 1 , ∗∗
      Current Biology
      Cell Press

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          Summary

          Background

          Neural systems must weight and integrate different sensory cues in order to make decisions. However, environmental conditions often change over time, altering the reliability of different cues and therefore the optimal way for combining them. To explore how cue integration develops in dynamic environments, we examined the effects on auditory spatial processing of rearing ferrets with localization cues that were modified via a unilateral earplug, interspersed with brief periods of normal hearing.

          Results

          In contrast with control animals, which rely primarily on timing and intensity differences between their two ears to localize sound sources, the juvenile-plugged ferrets developed the ability to localize sounds accurately by relying more on the unchanged spectral localization cues provided by the single normal ear. This adaptive process was paralleled by changes in neuronal responses in the primary auditory cortex, which became relatively more sensitive to these monaural spatial cues. Our behavioral and physiological data demonstrated, however, that the reweighting of different spatial cues disappeared as soon as normal hearing was experienced, showing for the first time that this type of plasticity can be context specific.

          Conclusions

          These results show that developmental changes can be selectively expressed in response to specific acoustic conditions. In this way, the auditory system can develop and simultaneously maintain two distinct models of auditory space and switch between these models depending on the prevailing sensory context. This ability is likely to be critical for maintaining accurate perception in dynamic environments and may point toward novel therapeutic strategies for individuals who experience sensory deficits during development.

          Graphical Abstract

          Highlights

          • Ferrets reared with a unilateral hearing loss are able to localize sounds accurately

          • Adaptation relies on cue reweighting that reverses when normal hearing is available

          • Auditory cortical neurons show corresponding context-specific plasticity

          • Contextual cue reweighting maintains perceptual stability in dynamic environments

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          Most cited references41

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          Rapid task-related plasticity of spectrotemporal receptive fields in primary auditory cortex.

          We investigated the hypothesis that task performance can rapidly and adaptively reshape cortical receptive field properties in accord with specific task demands and salient sensory cues. We recorded neuronal responses in the primary auditory cortex of behaving ferrets that were trained to detect a target tone of any frequency. Cortical plasticity was quantified by measuring focal changes in each cell's spectrotemporal response field (STRF) in a series of passive and active behavioral conditions. STRF measurements were made simultaneously with task performance, providing multiple snapshots of the dynamic STRF during ongoing behavior. Attending to a specific target frequency during the detection task consistently induced localized facilitative changes in STRF shape, which were swift in onset. Such modulatory changes may enhance overall cortical responsiveness to the target tone and increase the likelihood of 'capturing' the attended target during the detection task. Some receptive field changes persisted for hours after the task was over and hence may contribute to long-term sensory memory.
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            The dominant role of low-frequency interaural time differences in sound localization.

            Two experiments are described in which listeners judge the apparent directions of virtual sound sources-headphone-presented sounds that are processed in order to simulate free-field sounds. Previous results suggest that when the cues to sound direction are preserved by the simulation, the apparent directions of virtual sources are nearly the same as the apparent directions of real free-field sources. In the experiments reported here, the interaural phase relations in the processing algorithms are manipulated in order to produce stimuli in which the interaural time difference cues signal one direction and interaural intensity and pinna cues signal another direction. The apparent directions of these conflicting cue stimuli almost always follow the interaural time cue, as long as the wideband stimuli include low frequencies. With low frequencies removed from the stimuli, the dominance of interaural time difference disappears, and apparent direction is determined primarily by interaural intensity difference and pinna cues.
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              Relearning sound localization with new ears.

              Because the inner ear is not organized spatially, sound localization relies on the neural processing of implicit acoustic cues. To determine a sound's position, the brain must learn and calibrate these cues, using accurate spatial feedback from other sensorimotor systems. Experimental evidence for such a system has been demonstrated in barn owls, but not in humans. Here, we demonstrate the existence of ongoing spatial calibration in the adult human auditory system. The spectral elevation cues of human subjects were disrupted by modifying their outer ears (pinnae) with molds. Although localization of sound elevation was dramatically degraded immediately after the modification, accurate performance was steadily reacquired. Interestingly, learning the new spectral cues did not interfere with the neural representation of the original cues, as subjects could localize sounds with both normal and modified pinnae.
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                Author and article information

                Contributors
                Journal
                Curr Biol
                Curr. Biol
                Current Biology
                Cell Press
                0960-9822
                1879-0445
                22 July 2013
                22 July 2013
                : 23
                : 14
                : 1291-1299
                Affiliations
                [1 ]Department of Physiology, Anatomy and Genetics, University of Oxford, Parks Road, Oxford OX1 3PT, UK
                Author notes
                []Corresponding author peter.keating@ 123456dpag.ox.ac.uk
                [∗∗ ]Corresponding author andrew.king@ 123456dpag.ox.ac.uk
                Article
                CURBIO10382
                10.1016/j.cub.2013.05.045
                3722484
                23810532
                f907bfc9-8ce1-470b-841c-1a31c926ecab
                © 2013 The Authors

                This document may be redistributed and reused, subject to certain conditions.

                History
                : 15 March 2013
                : 13 May 2013
                : 24 May 2013
                Categories
                Article

                Life sciences
                Life sciences

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