The Maturation of the Superior Collicular Map of Auditory Space in the Guinea Pig is Disrupted by Developmental Visual Deprivation (original) (raw)
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Analysis of the superior colliculus auditory space map function in guinea pig behavior
Neuroscience Research Communications, 1998
In the deep layers of the superior colliculus (SC) a map-like representation of auditory space and multimodal integration has been described, but the contribution of the map to guinea pig behavior is unknown. The present work was targeted at exploring its possible role in both spatial auditory discrimination learning and in a positive patterning paradigm, where combined visual/auditory stimuli were rewarded. Emergence of the auditory map was prevented by a darkrearing regime known to cause a selective disturbance of this map. Surprisingly, dark-reared guinea pigs were able to learn both the spatial auditory task and the positive pattern paradigm showing no deficit compared to age-matched controls. Subsequent electrophysiological mapping confirmed the lack of the auditory space map in deprived animals but not in controls. Accordingly, our data suggest that the SC map of auditory space is not essential for learning the behavioral paradigms used. The possible contribution of other auditory/multimodal brain areas is discussed.
2020
The development of spatially registered auditory maps in the external nucleus of the inferior colliculus (ICx) in young owls and their maintenance in adult animals is visually guided and evolves dynamically. To investigate the underlying neural mechanisms of this process, we developed a model of stabilized neoHebbian correlative learning which is augmented by an eligibility signal and a temporal trace of activations. This 3-component learning algorithm facilitates stable, yet flexible, formation of spatially registered auditory space maps composed of conductance-based topographically organized neural units. Spatially aligned maps are learned for visual and auditory input stimuli that arrive in temporal and spatial registration. The reliability of visual sensory inputs can be used to regulate the learning rate in the form of an eligibility trace. We show that by shifting visual sensory inputs at the onset of learning the topography of auditory space maps is shifted accordingly. Simulation results explain why a shift of auditory maps in mature animals is possible only if corrections are induced in small steps. We conclude that learning spatially aligned auditory maps is flexibly controlled by reliable visual sensory neurons and can be formalized by a biological plausible unsupervised learning mechanism.
Journal of Neuroscience, 2008
Auditory neurons in the superior colliculus (SC) respond preferentially to sounds from restricted directions to form a map of auditory space. The development of this representation is shaped by sensory experience, but little is known about the relative contribution of peripheral and central factors to the emergence of adult responses. By recording from the SC of anesthetized ferrets at different age points, we show that the map matures gradually after birth; the spatial receptive fields (SRFs) become more sharply tuned and topographic order emerges by the end of the second postnatal month. Principal components analysis of the head-related transfer function revealed that the time course of map development is mirrored by the maturation of the spatial cues generated by the growing head and external ears. However, using virtual acoustic space stimuli, we show that these acoustical changes are not by themselves responsible for the emergence of SC map topography. Presenting stimuli to infant ferrets through virtual adult ears did not improve the order in the representation of sound azimuth in the SC. But by using linear discriminant analysis to compare different response properties across age, we found that the SRFs of infant neurons nevertheless became more adult-like when stimuli were delivered through virtual adult ears. Hence, although the emergence of auditory topography is likely to depend on refinements in neural circuitry, maturation of the structure of the SRFs (particularly their spatial extent) can be largely accounted for by changes in the acoustics associated with growth of the head and ears.
Experimental Brain Research, 1993
There have been conflicting reports concerning the importance of visual experience in the development of auditory localization mechanisms. We have examined the representation of auditory space in the superior colliculus of adult ferrets that were visually deprived by binocular eyelid suture from postnatal days 25-28, prior to natural eye opening, until the time of recording. This procedure attenuated the transmission of light by a factor of at least 20-25 and blurred the image so that, as long as the eyelids were still fused, the responses of visual units in the superficial layers of the superior colliculus were labile and very poorly tuned. After the eyelids were opened, the representation of the visual field in these layers appeared to be normal. Acoustically responsive units were, as usual, almost exclusively restricted to the deeper layers of the superior colliculus. However, unlike normal animals, where responses occurring only at stimulus onset predominate, most of these units exhibited sustained or multi-peaked discharge patterns. The degree of spatial tuning of individual units recorded from the normal and deprived groups of animals was not significantly different in either azimuth or elevation. Normally orientated maps of both sound azimuth and elevation were also found in the visually deprived ferrets. However, abnormalities were present in the topography and precision of these representations and consequently in their alignment with the overlying visual map. In particular, an increase was observed in the proportion of auditory units with spatially ambiguous receptive fields, in which the maximum response occurred at two distinct locations. These results indicate that patterned visual experience is not required for establishing at least a crude map of auditory space in the superior colliculus, but suggest that it may play a role in refining this representation during development.
The Journal of Neuroscience, 1998
We have examined whether the superficial layers of the superior colliculus (SC) provide the source of visual signals that guide the development of the auditory space map in the deeper layers. Anatomical tracing experiments with fluorescent microspheres revealed that a retinotopic map is present in the newborn ferret SC. Aspiration of the caudal region of the superficial layers of the right SC on postnatal day 0 did not cause a reorganization of this projection. Consequently, recordings made when the animals were mature showed that visual units in the remaining superficial layers in rostral SC had receptive fields that spanned a restricted region of anterior space. Auditory units recorded beneath the remaining superficial layers were tuned to corresponding anterior locations. Both the superficial layer visual map and the deeper layer auditory map were normal in the left, unoperated SC. The majority of auditory units recorded throughout the deeper layers ventral to the superficial lay...
King. Interaural timing cues do not contribute to the map of space in the ferret superior colliculus: a virtual acoustic space study. . In this study, we used individualized virtual acoustic space (VAS) stimuli to investigate the representation of auditory space in the superior colliculus (SC) of anesthetized ferrets. The VAS stimuli were generated by convolving broadband noise bursts with each animal's own headrelated transfer function and presented over earphones. Comparison of the amplitude spectra of the free-field and VAS signals and of the spatial receptive fields of neurons recorded in the inferior colliculus with each form of stimulation confirmed that the VAS provided an accurate simulation of sounds presented in the free field. Units recorded in the deeper layers of the SC responded predominantly to virtual sound directions within the contralateral hemifield. In most cases, increasing the sound level resulted in stronger spike discharges and broader spatial receptive fields. However, the preferred sound directions, as defined by the direction of the centroid vector, remained largely unchanged across different levels and, as observed in previous free-field studies, varied topographically in azimuth along the rostrocaudal axis of the SC. We also examined the contribution of interaural time differences (ITDs) to map topography by digitally manipulating the VAS stimuli so that ITDs were held constant while allowing other spatial cues to vary naturally. The response properties of the majority of units, including centroid direction, remained unchanged with fixed ITDs, indicating that sensitivity to this cue is not responsible for tuning to different sound directions. These results are consistent with previous data suggesting that sensitivity to interaural level differences and spectral cues provides the basis for the map of auditory space in the mammalian SC.
Time attracts auditory space representation during development
Behavioural Brain Research, 2019
Vision is the most accurate sense for spatial representation, whereas audition is for temporal representation. However, how different sensory modalities shape the development of spatial and temporal representations is still unclear. Here, 45 children aged 11-13 years were tested to investigate the abilities to evaluate spatial features of auditory stimuli during bisection tasks, while conflicting or non-conflicting spatial and temporal information was delivered. Since audition is fundamental for temporal representation, the hypothesis was that temporal information could influence auditory spatial representation development. Results show a strong interaction between the temporal and the spatial domain. Younger children are not able to build complex spatial representations when the temporal domain is uninformative about space. However, when the spatial information is coherent with the temporal information children of all age are able to decode complex spatial relationships. When spatial and temporal cues are conflicting, younger children are strongly attracted by the temporal instead of spatial information, while older participants result unaffected by the cross-domain conflict. These findings suggest that during development temporal representation of events is used to infer spatial coordinates of the environment, offering important opportunities for new teaching and rehabilitation strategies.
Plasticity in the neural coding of auditory space in the mammalian brain
Proceedings of the National Academy of Sciences, 2000
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.