Experience-dependent plasticity in the inferior colliculus: a site for visual calibration of the neural representation of auditory space in the barn owl

Abstract

The optic tectum (homolog of the superior colliculus) contains mutually aligned neural maps of auditory and visual space. During development, the organization of the auditory map is guided by spatial information provided by vision: barn owls raised wearing prismatic spectacles, which optically shift the visual field and the visual map in the optic tectum, develop an auditory map that is shifted by an approximately equivalent amount, such that alignment between the two maps is preserved (Knudsen and Brainard, 1991). In this study we investigated whether this shift in the auditory map is intrinsic to the optic tectum or whether it reflects plasticity at an earlier stage in the auditory pathway. Owls were raised wearing prismatic spectacles that displaced the visual field by 23 degrees to the left or right. This manipulation alters the normal correspondence between locations in the visual field and interaural time difference (ITD), the primary cue for the azimuth of a sound source. In normal owls and in owls with at least 150 d of prism experience, extracellular unit recordings were used to assess the representations of ITD at anatomically and physiologically defined sites in the optic tectum and in the two prior stages of the auditory pathway, the external and central nuclei of the inferior colliculus (ICx and ICc). In the optic tectum of normal owls, the values of ITD to which units responded most strongly (best ITDs) varied systematically with the azimuths of unit visual receptive fields (VRFs). In the prism-reared owls, best ITDs were shifted from normal toward the values of ITD produced by sounds at the locations of the units' optically displaced VRFs. In the ICx of prism-reared owls, the representation of ITD also was shifted from normal, by an amount and in a direction that could completely account for the shift in ITD measured in the optic tectum. At some sites in the ICx, the shift in ITD tuning was apparent within the first 7-8 msec of the response; shifted tuning at such short latencies argues that the altered representation of ITD in the ICx reflects plasticity in the ascending auditory pathway, and is not the result of descending activity from higher auditory centers. In the ICc, which immediately precedes the ICx in the ascending pathway, the representation of ITD was normal. The results indicate that the visual instruction of auditory spatial tuning of neurons in the optic tectum reflects plasticity at the level of the ICx, the site where the auditory map of space is first synthesized.