Anatomical and pharmacological correlates of learning in the neural representation of auditory space in the barn owl

Sensory experience early in life powerfully shapes the form and function of developing neural circuits. In the barn owl (Tyto alba), visual experience calibrates auditory spatial tuning in the external nucleus of the inferior colliculus (ICX). When owls are reared wearing prismatic spectacles that displace the visual field in azimuth, the tuning of ICX neurons for interaural time difference (ITD), the owl's primary cue for sound source azimuth, becomes altered systematically. The result of this experience-dependent plasticity is to maintain alignment of auditory and visual space maps in the optic tectum, the principal target of the ICX. In this dissertation, the cellular basis for this plasticity is explored.; In the first experiments, an anatomical basis for this plasticity was identified. The ICX receives its principal auditory input from the lateral shell of the central nucleus of the inferior colliculus (ICCls), where ITD tuning is not modified by prism-rearing. In juvenile owls before prism attachment, as well as in normal adults, retrograde tracing with biotinylated dextran amine demonstrated that the ICCls-ICX projection was topographic, linking sites of like ITD tuning in the two nuclei. In prism-reared owls, topography was altered such that ICX sites received abnormal input from ICCls regions encoding the ITD values to which the ICX neurons had become responsive during prism-rearing.; The contribution of the N-methyl-d-aspartate (NMDA) subtype of excitatory amino acid receptor to this plasticity was investigated using in vivo iontophoretic techniques. In normal owls, both NMDA and non-NMDA glutamate receptors participate in auditory transmission in the ICX. In prism-reared owls, the abnormal responses that are acquired by ICX neurons during prism-rearing were found to be mediated preferentially by NMDA receptors, relative to normal responses expressed by the same ICX neurons. This pharmacological specialization of learned responses was retained for several months, after which these responses reverted to normal pharmacology. These anatomical and pharmacological results support a speculative model for plasticity in which acquisition of learned responses by ICX neurons is mediated by formation of ICCls-ICX synapses with enhanced NMDA receptor currents.