Learning and remembering spatial relations is an important human capacity. Many lines of evidence suggest that the hippocampus is essential for this form of learning, both in humans and in animals. However, much less is known of how spatial relations are encoded in the hippocampus or of how the hippocampus changes as learning of spatial relations occurs. This application will study the substrate for spatial learning using a novel animal model: seed storage in birds. Several species of birds hide large numbers of seeds and are able to retrieve them reliably weeks or months later. Several studies suggest that the hippocampus is necessary for the learning--it is larger in species that store than in related ones that do not, and birds that store are unable to retrieve if the hippocampus is lessoned. The P.I. and colleagues showed that the volume of the avian hippocampus increases in juveniles with the onset of storage and retrieval, and fluctuates seasonally in adults with use of seed storage and retrieval. This demonstrates that the structure of this complex neural network is modified in adulthood to allow for (or to encode) spatial learning. Furthermore, inactivating the hippocampus disrupts retrieval based on spatial cues. Experiments in the present proposal build on these findings. One series of experiments will measure changes in the structure and projections of hippocampal neurons from spring to fall, as the birds increase their storage and retrieval. Plastic changes in anatomy will be compared to observations in a species that does not store food. We will try to determine the cause for the fall changes in behavior and neuroanatomy. A second series of experiments will examine hippocampal functioning. Two experiments will impair neuronal activity and look for changes in spatial learning or recall. A third will use immediate early gene expression as a marker of the neuronal activity associated with recall of spatial memories. It is intended to determine whether retrieving recent and remote spatial memories activates the same neural substrate. This proposal assesses several major aspects of the neurobiology of avian spatial learning. It searches for structural features related to the behavioral capacity, for long term structural change in the system related to seasonal changes in the frequency of the behavior, and for short term changes related to use. Each of these issues is closely related to human spatial learning, its neural substrate and its capacity for change.
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