Vision calibrates sound localization in developing barn owls

Abstract

This study demonstrates that continuous exposure of baby barn owls to a displaced visual field causes a shift in sound localization in the direction of the visual displacement. This implies an innate dominance of vision over audition in the development and maintenance of sound localization. Twelve owls were raised from the first day of eye opening wearing binocular prisms that displaced the visual field to the right by 11 degrees, 23 degrees, or 34 degrees. The prisms were worn for periods of up to 7 months. Consistent with previous results (Knudsen and Knudsen, 1989a), owls reared with displacing prisms did not adjust head orientation to visual stimuli. While wearing prisms, owls consistently oriented the head to the right of visual targets, and, as soon as the prisms were removed, they oriented the head directly at visual targets, as do normal owls. In contrast, prism-reared owls did change head orientation to sound sources even though auditory cues were not altered significantly. Birds reared wearing 11 degrees or 23 degrees prisms oriented the head to the right of acoustic targets by an amount approximately equal to the optical displacement induced by the prisms. Birds raised wearing 34 degrees prisms adjusted sound localization by only about 50% of the optical displacement. Thus, visually guided adjustment of sound localization appears to be limited to about 20 degrees in azimuth. The data indicate that when confronted with consistently discordant localization information from the auditory and visual systems, developing owls use vision to calibrate associations of auditory localization cues with locations in space in an attempt to bring into alignment the perceived locations of auditory and visual stimuli emanating from a common source. Vision exerts this instructive influence on sound localization whether or not visual information is accurate.

Active sensing via movement shapes spatiotemporal patterns of sensory feedback

“…This is consistent with their life history, as they hide in root systems, grasses and debris during daylight hours when visual cues are present Stamper et al, 2010). Similarly, other nocturnal or crepuscular animals that can rely on non-visual sensory information for the control of behavior also preferentially rely on visual cues when they are present (Knudsen and Knudsen, 1989;Penteriani et al, 2007;Cummings et al, 2008).…”

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

“…King et al 1988;Knudsen and Knudsen 1989;Knudsen and Knudsen 1990;Brainard and Knudsen 1998;Knudsen 2002). Largely because of the convenience of a topographical representation of auditory space, much of this work has exploited the superior colliculus of the mammal or the barn owl.…”

Hunting Increases Adaptive Auditory Map Plasticity in Adult Barn Owls

“…Moreover, juvenile owls frequently exhibited full map shifts without hunting and while housed in small individual cages (Knudsen and Knudsen, 1989b). Thus the high degree of plasticity expressed in hunting adult owls is still less than the plasticity expressed by juvenile owls during the sensitive period.…”

“…Recent studies have shown that environmental factors such as social interactions and environmental richness also modulate plasticity (Newport et al, 2001;Goldstein et al, 2003;Cancedda et al, 2004). Barn owls pass through a similar sensitive period during which experience exerts an exceptionally strong shaping influence on sound localization behavior (Knudsen and Knudsen, 1989b). The effects of experience on sound localization have been traced to specific sites within the owl's midbrain, making it possible to correlate behavioral learning with changes in underlying neural circuits (Feldman and Knudsen, 1998;DeBello et al, 2001).…”