Sound localization was disrupted in young barn owls by chronically plugging one ear. Owls that were younger than 8 weeks of age at the time of ear plugging recovered normal localization accuracy while plugged, whereas those that were older than 8 weeks at the time of ear plugging did not. The end of the sensitive period for the adjustment of sound localization accuracy coincides with the maturation of the head and ears, suggesting that the exposure of the auditory system to stable, adult-like acoustic cues could play a role in bringing the sensitive period to a close. The results demonstrate that, early in development, associations between auditory cues and locations in space can be altered by experience.Animals localize sounds by associating sets of monaural and binaural cues with locations in space. The most reliable cues are binaural, i.e., differences in the timing and intensity of sounds at the two ears. The reliability of these cues results from the fact that they depend only upon the size and shape of the head and ears and do not require assumptions about the properties of the original sound stimulus or the acoustic environment (Searle et al., 1976). Therefore, once the auditory system is calibrated to the passive acoustic properties of the head and ears and correlates frequency-specific binaural differences with locations in space, these binaural cues become unconditional indicators of the location of a sound source.In the course of normal development, growth of the head and ears increases the range of binaural disparities experienced by the auditory system and alters the correlations of binaural cues with locations in space. Among adults, the size of the head and ears varies; therefore the associations between binaural cues and locations in space differ slightly for each individual. In light of this variability, how does the auditory system establish correct associations between binaural cues and locations in space? One solution might be that calibration of the sound localization circuitry is based upon sensory experience. To explore this possibility we have investigated

We studied the ability of barn owls to recover accurate sound localization after being raised with one ear occluded. Most of the owls had ear plugs inserted before they reached adult size, and therefore they never experienced normal adult localization cues until their ear plugs were removed. Upon removal of their ear plugs, these owls exhibited large systematic sound localization errors. The rate at which they recovered accurate localization decreased with the age of the bird at the time of plug removal, and recovery essentially ceased when owls reached 38 to 42 weeks of age. We interpret this age as the end of a critical period for the consolidation of associations between auditory cues and locations in space. Owls that had experienced adult localization cues for a short period of time before ear plugging recovered normal accuracy rapidly, even if they remained plugged well past the end of the critical period. This suggests that a brief exposure to normal adult cues early in the critical period is sufficient to enable the recovery of localization accuracy much later in life.

This study describes developmental changes in the capacity of owls to adjust sound localization in response to chronic prismatic displacement of the visual field and to recover accurate sound localization following the restoration of normal vision. Matched, binocular displacing prisms were mounted over the eyes of 19 barn owls (Tyto alba) beginning at ages ranging from 10 to 272 d. In nearly all cases, the visual field was shifted 23 degrees to the right. Sound localization was assessed on the basis of head orientations to sound sources, measured in a darkened sound chamber with a search coil system. Chronic exposure to a displaced visual field caused the owls to alter sound localization in the direction of the visual field displacement, thereby inducing a sound-localization error. The size of the sound-localization error that resulted depended on the age of the animal when prism experience began. Maximal errors of about 20 degrees were induced only when prism experience began by 21 d of age. As prism experience began at later ages, the magnitude of induced errors decreased. A bird that wore prisms beginning at 102 d of age, altered sound localization by only 6 degrees. An adult owl, when exposed chronically to a displaced visual field, altered sound localization by about 3 degrees. We refer to the early period in life when displaced vision induces exceptionally large sound-localization errors (relative to those induced in the adult) as a sensitive period. The capacity to recover accurate sound localization following restoration of normal vision was tested in 7 owls that had been raised wearing prisms. Four owls that had prisms removed by 182 d of age recovered accurate localization rapidly (over a period of weeks), whereas 3 owls that were older when the prisms were removed did not recover accurate localization when tested for up to 7 months after prism removal. Adjustment of sound localization slowed greatly or ceased at about 200 days of age, referred to here as the critical period for visual calibration of sound localization. Three owls were subjected repetitively to displacement of the visual field. An owl that adjusted sound localization to the left of normal during the sensitive period retained the capacity to adjust again to the left, but not to the right of normal, later in the critical period. The converse was true for an owl that adjusted sound localization to the right of normal during the sensitive period.(ABSTRACT TRUNCATED AT 400 WORDS)

The capacity of barn owls to adapt visuomotor behavior in response to prism-induced displacement of the visual field was tested in babies and adults. Matched, binocular Fresnel prisms, which displaced the visual field 11 degrees, 23 degrees, or 34 degrees to the right, were placed on owls for periods of up to 99 d. Seven baby owls wore the prisms from the day the eyelids first opened; 2 owls wore them as adults. Prism adaptation was measured by the accuracy with which a target was approached and struck with the talons, a behavior similar to pointing behavior used commonly to assess prism adaptation in primates. Baby and adult owls exhibited a limited capacity to adapt this visuomotor behavior. Acquisition of adapted behavior was slow, taking place over a period of weeks, and was never complete even for owls that were raised viewing the world through relatively weak (11 degrees) displacing prisms. When the prisms were removed from adapted owls, they struck to the opposite side of the target. The recovery of strike accuracy following prism removal was rapid; 7 of 9 owls recovered normal accuracy within 30 min of prism removal, despite having worn the prisms for months. This limited capacity for adaptation contrasts dramatically with the extensive and rapid adaptation exhibited by adult primates exposed to comparable prismatic displacements. The mechanism of adaptation used by the owls was to alter the movements employed for approaching targets. Instead of moving straight ahead, the head and body moved diagonally relative to the orientation of the head. Thus, in contrast to prism adaptation by humans that can involve reinterpretation of eye, head, and limb position, prism adaptation by owls is based on changes in the motor commands that underlie approach behavior.

Early in life, the barn owl passes through a sensitive period during which it can interpret and make use of abnormal auditory cues for accurate sound localization. This capacity is lost at about 8 weeks of age, just after the head and ears reach adult size (knudsen et al. 1984a). The end of the sensitive period could be triggered either by an age-dependent process or by the exposure of the auditory system to stable or adult-like cues. To distinguish between these alternatives, we subjected baby owls to constant abnormal cues (chronic monaural occlusion) or to frequently changing abnormal cues (alternating monaural occlusion) throughout the sensitive period. In the first group of animals (n = 2), one ear was plugged continuously until 73 or 79 d of age, respectively, and then the earplug was switched to the opposite ear. Although these animals adjusted sound localization accuracy during the initial chronic monaural occlusion, they could not localize sounds at all after the earplug was switched to the opposite ear, and they remained unable to localize sounds as long as the opposite ear remained occluded (7 and 27 weeks, respectively). When the second monaural occlusion was finally removed, both birds localized sounds with errors that were similar to the errors they exhibited immediately after removal of the first monaural occlusion. One bird that was 127-d-old at the time the second earplug was removed corrected its localization error; the other bird, 250-d-old when the second earplug was removed, did not.(ABSTRACT TRUNCATED AT 250 WORDS)