Stretched and upside-down maps of auditory space in the optic tectum of blind-reared owls; acoustic basis and behavioral correlates

Abstract

Vision during early life plays an important role in calibrating sound localization behavior. This study investigates the effects of visual deprivation on sound localization and on the neural representation of auditory space. Nine barn owls were raised with eyelids sutured closed; one owl was congenitally anophthalmic. Data from these birds were compared with data from owls raised with normal visual experience. Sound localization behavior was significantly less precise in blind- reared owls than in normal owls. The scatter of localization errors was particularly large in elevation, though it was abnormally large in both dimensions. However, there was no systematic bias to the localization errors measured over a range of source locations. This indicates that the representation of auditory space is degraded in some way for blind- reared owls, but on average is properly calibrated. The spatial tuning of auditory neurons in the optic tectum was studied in seven of the blind-reared owls to assess the effects of early visual deprivation on the neural representation of auditory space. In normal owls, units in the optic tectum are sharply tuned for sound source location and are organized systematically according to the locations of their receptive fields to form a map of auditory space. In blind-reared owls, the following auditory properties were abnormal: (1) auditory tuning for source elevation was abnormally broad, (2) the progression of the azimuths and elevations of auditory receptive fields across the tectum was erratic, and (3) in five of the seven owls, the auditory representation of elevation was systematically stretched, and in the two others large portions of the representation of elevation were flipped upside down. The following unit properties were apparently unaffected by blind rearing: (1) the sharpness of tuning for sound source azimuth, (2) the orientation of the auditory representation of azimuth, and (3) the mutual alignment of the auditory and visual receptive fields in the region of the tectum representing the area of space directly in front of the animal. The data demonstrate that the brain is capable of generating an auditory map of space without vision, but that the normal precision and topography of the map depend on visual experience. The space map results from the tuning of tectal units for interaural intensity differences (IIDs) and interaural time differences (ITDs; Olsen et al., 1989).

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).…”

Audiovisual links in exogenous covert spatial orienting

“…These show in several species that the representation of auditory space in the deeper layers of the SC depends on experience, and can be manipulated by varying the visual environment (King & Carlile, 1993;King, Hutchings, Moore, & Blakemore, 1988;Knudsen & Brainard, 1991;Knudsen, Esterly, & du Lac, 1991;Withington, 1992). By contrast, the spatial organization ofthe superficial, purely visual layers ofthe SC is apparent at the earliest physiological recordings (King & Carlile, 1993), and several manipulations of auditory experience are thought to have no influence on these visual maps (King, personal communication, April 29, 1994, reviewing a number of studies: Knudsen, Esterly, & Knudsen, 1984;Withington-Wray, Binns, Dhanjal, Brickley, & Keating, 1990).…”

Development of output connections from the inferior colliculus to the optic tectum in barn owls

“…The visual information needed for the elimination of the visual-auditory mismatch in the bimodal map is provided from OT neurons (Hyde and Knudsen, 2002;Gutfreund et al, 2002), the identity of which is not clear because both neurons of the SGC (Luksch et al, 2000) and neurons of the intermediate layers (Hyde and Knudsen, 2000) have been shown to project to the ICX. Largely normal ITD tuning develops in the absence of visual experience (Knudsen et al, 1991) or is reestablished after prisms are removed (Brainard and Knudsen, 1995). Since the spatial patterns of ITDs are relatively constant across frequencies and across individuals (Keller et al, 1998), the information necessary to establish approximately correct associations for azimuthal localization could be encoded genetically (Knudsen, 1999).…”