The sensitive period for auditory localization in barn owls is limited by age, not by experience

Abstract

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. 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 cures. To distinguish between these alternatives, the authors 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. These results demonstrate that abnormal associations between auditory cues and sound-source locations can remain stable for long periods of time without functional validation, and that the critical period for adjusting auditory localization accuracy can end by a certain age even though an animal cannot localize sounds. However, because these animals could not localize sounds once the earplug was switched to the opposite ear, these data did not answer the question of whether or not the sensitive period had been extended. Therefore, in a second group of baby owls (n = 4), the authors switched the earplug from one to the other every second day. This high rate of alternating monaural occlusion ensured that the animals never adjusted completely to the abnormal cues. Alternating occlusion continued until the birds were older than 60 d of age and was followed by chronic monaural occlusion to test the ability of the animals to adjust auditory localization. None of these birds adjusted auditory localization when exposed to chronic monaural occlusion. Thus, despite exposure to abnormal and changing auditory cues, the sensitive period still ended at about 8 weeks of age. On the basis of these data, the authors conclude that the end of the sensitive period is triggered by a process that is essentially, if not exclusively, age-dependent.