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 lesioned. The P.I. and colleagues recently 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 can be modified in adulthood to allow for (or to encode) spatial learning. Experiments in the present proposal build on this finding. One series of experiments will compare neuronal morphology and connectivity is species that store and species that do not, to determine whether the augmented volume in storing species is due to increases in a particular constituent of the hippocampus, and whether it is focused on particular regions of the hippocampus. These studies provide detailed neuroanatomy not yet available for this system and may suggest sites or features likely to be especially important for the learned behavior. A second series will determine whether subdivisions of the hippocampus are especially important for storage or for retrieval by either temporarily inactivating portions of the hippocampus or by looking for sites of expression of the immediate early gene c-fos with storage or retrieval. These experiments are designed to separate effects of memory consolidation from memory retrieval. A final series will measure long-term morphological consequences of manipulating experience with spatial learning in adult birds. This will help determine whether the increase in hippocampal volume previously observed permits spatial learning or is caused by it. This proposal assesses several major issues about the neurobiology of avian spatial learning. It searches for network 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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