Plasticity in the neural coding of auditory space in the mammalian brain

Abstract

Sound localization relies on the neural processing of monaural and binaural spatial cues that arise from the way sounds interact with the head and external ears. Neurophysiological studies of animals raised with abnormal sensory inputs show that the map of auditory space in the superior colliculus is shaped during development by both auditory and visual experience. An example of this plasticity is provided by monaural occlusion during infancy, which leads to compensatory changes in auditory spatial tuning that tend to preserve the alignment between the neural representations of visual and auditory space. Adaptive changes also take place in sound localization behavior, as demonstrated by the fact that ferrets raised and tested with one ear plugged learn to localize as accurately as control animals. In both cases, these adjustments may involve greater use of monaural spectral cues provided by the other ear. Although plasticity in the auditory space map seems to be restricted to development, adult ferrets show some recovery of sound localization behavior after long-term monaural occlusion. The capacity for behavioral adaptation is, however, task dependent, because auditory spatial acuity and binaural unmasking (a measure of the spatial contribution to the "cocktail party effect") are permanently impaired by chronically plugging one ear, both in infancy but especially in adulthood. Experience-induced plasticity allows the neural circuitry underlying sound localization to be customized to individual characteristics, such as the size and shape of the head and ears, and to compensate for natural conductive hearing losses, including those associated with middle ear disease in infancy. C onsiderable plasticity exists in the neural circuits that process sensory information. Although plasticity is greatest during development, certain aspects of the mature brain maintain the capacity to reorganize in response to changes in the activity patterns of sensory inputs. Experience-mediated plasticity is most commonly associated with higher-level response properties that are generated within the brain by serial stages of computation. One of the best examples is provided by the neural mechanisms underlying sound localization, which are adapted by experience to the features of the individual.Identifying the location of sounds produced by potential mates, prey, or predators is one of the most important functions of the auditory system. This ability relies on the extraction of direction-dependent cues generated by the head, torso, and external ears. For localization in the horizontal plane, the separation of the two ears allows mammals to use interaural time differences (ITDs) at low frequencies and interaural level differences (ILDs) at high frequencies (1, 2). These binaural cues also contribute to the ability of listeners to detect and discriminate signals of interest against a background of masking noise (3).ITDs and ILDs do not, by themselves, provide a sufficient basis for localizing a sound source. For individual frequencies, bo...

Contribution of Head Shadow and Pinna Cues to Chronic Monaural Sound Localization

“…After application of a unilateral or binaural mold, their azimuth localization responses are not affected (data not shown in this study, but see Oldfield and Parker, 1984;Hofman and Van Opstal, 2003), whereas manipulation of spectral cues in a virtual set-up has little influence on lateral angle judgments (Macpherson and Middlebrooks, 2002). Applying a monaural plug to normalhearing listeners leads to an immediate and long-lasting shift of the azimuth percept toward the side of the free ear both in humans (Oldfield and Parker, 1986;Butler et al, 1990;Slattery and Middlebrooks, 1994) and in experimental animals (Knudsen et al, 1982;King et al, 2000).…”

“…After plugging one ear, young ferrets relearn to localize sounds, presumably by using spectral cues of the intact ear (King et al, 2000). It has been argued, however, that because plugging perturbs binaural cues in a frequency-dependent way, listeners could in principle maintain a binaural strategy by relying on lowfrequency information (Wightman and Kistler, 1997).…”

Tradeoffs and Constraints on Neural Representation in Networks of Cortical Neurons

“…It would also be possible to study the effect of stimulation history more systematically and further into the past. Finally, perhaps the most intriguing aspects of the representation question is its plasticity (Recanzone et al, 1993;King et al, 2000), and the way it is modulated by neural signals external to the assembly. In vitro studies may include modulation and plasticity (Chiappalone et al, 2008) of representation by various methods, such as closed loop electrical stimulation and selective application of neuromodulators.…”

Lateralization of Interimplant Timing and Level Differences in Children Who Use Bilateral Cochlear Implants

“…The area of the auditory brainstem most relevant to the present paper is the superior olivary complex, as interaural level and timing differences are initially processed here (King et al 2000) (Fig. 1.3).…”

“…Further areas of consideration include higher centres implicated in the coding of auditory space, such as the superior colliculus (King et al 1998;King et al 2000;Middlebrooks and Knudsen 1984) and the primary auditory cortex (King et al 2000). In order to promote binaural processing in children with bilateral cochlear implants, an understanding of the effect of deafness on the development of these important auditory centres is necessary.…”