Adaptive adjustment of unit tuning to sound localization cues in response to monaural occlusion in developing owl optic tectum

Abstract

Bimodal units in the barn owl's optic tectum are tuned to the location of auditory and visual stimuli, and are systematically organized according to their spatial tuning to form mutually aligned maps of auditory and visual space. Map alignment results from the fact that, normally, units are tuned to the values of interaural level difference (ILD) and interaural time difference (ITD) produced by a sound source at the location of their visual receptive fields (VRFs). Monaural occlusion alters the correspondence of ILD and ITD values with locations in space. We investigated the effect that raising owls with a chronic monaural occlusion has on the tuning of tectal units to ILD and ITD. Owls were monaurally occluded beginning at 1 month of age. The effects of monaural occlusion were assessed 2-4 months later by comparing the ILD and ITD tuning of units in monaurally occluded owls with the ILD and ITD tuning of units with equivalent VRFs in normal owls. ILD and ITD tuning was shifted substantially and in the direction of the unoccluded ear (the adaptive direction) in owls raised with a monaural occlusion. In most tecta, the mapped representations of ILD and ITD were shifted systematically. In addition, in some tecta, monaural occlusion induced a change in the topography of the ILD map such that ILD tuning remained essentially constant at values near 0 dB over abnormally large portions of the tectum. Across all recording sites, the average shift in ILD tuning was 9 dB (n = 396) and the average shift in ITD tuning was 40 microseconds (n = 414). In four of five animals, the magnitude of the effect was not equivalent on the two sides of the brain, the adjustments being significantly larger and more systematic on the side ipsilateral to the occlusion. Such differences in the altered ILD and ITD maps on the two sides of the brain in individual animals indicate that, although a component of the adaptive adjustment might be due to regulation of the gain and phase response of the monaural signals early in the auditory pathway, a major component of the adjustment must occur at or beyond the level where the encoding of ILDs and ITDs for left and right space separates.