Changes induced in the representation of auditory space in the superior colliculus by rearing ferrets with binocular eyelid suture

Abstract

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 a 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.

Early life exposure to noise alters the representation of auditory localization cues in the auditory space map of the barn owl

“…Dark-rearing experiments in rats demonstrated that visual experience is important for maintenance but not for the development of the visual map in the SC (Carrasco et al 2005). Similarly, in barn owls and ferrets, visual manipulations such as blind (sutured eyelids) or prisms-rearing had very little effect on the visual space map (Knudsen et al 1991;Feldman and Knudsen 1997;King and Carlile 1993).…”

“…More direct evidence for the involvement of sensory experience has been achieved through long-term manipulation experiments, such as earplug, blind, and dark rearing. Visual deprivation studies have demonstrated an abnormal alignment of the auditory map with the visual map in ferrets (King and Carlile 1993) and barn owls (Knudsen et al 1991) but mostly normal auditory receptive fields. The effects of earplugs on barn owls have been a frequency-dependent compensating shift in the tuning of neurons (Mogdans and Knudsen 1992;Gold and Knudsen 1999).…”

Functional Topography of Converging Visual and Auditory Inputs to Neurons in the Rat Superior Colliculus

“…Degradation of visual inputs by binocular eyelid suture in young ferrets (King and Carlile 1993) and owls caused abnormalities in the organization of the auditory space map in the SC. In guinea pigs, dark rearing, which completely eliminates all visual information, was found to result in dSC cells with broad auditory spatial receptive fields and an auditory representation that showed little or no topographic order (Withington et al 1994).…”

Relearning Auditory Spectral Cues for Locations Inside and Outside the Visual Field

“…Much of this previous work has focussed on developmental adaptive changes and on the alignment of auditory and visual representations at the neuronal level (e.g. ferret: King et al 1988;King and Carlile 1993;barn owl: Knudsen and Brainard 1991). In general, there is a significant amount of evidence for interactions between the visual and auditory modalities that could point to visual inputs as a functional basis for auditory recalibration (see King 2009 for review).…”