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The Journal of Neuroscience, September 1, 2004, 24(35):7681-7689; doi:10.1523/JNEUROSCI.1958-04.2004
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Behavioral/Systems/Cognitive
Hippocampal Plasticity across Multiple Days of Exposure to Novel Environments
Loren M. Frank,1,2,3,4 Garrett B. Stanley,2,3 andEmery N. Brown1,3 1Neuroscience Statistics Research Laboratory, Department of Anesthesia and Critical Care, Massachusetts General Hospital, Boston, Massachusetts 02114, 2Division of Engineering and Applied Sciences, Harvard University, Cambridge, Massachusetts 02138, 3Harvard/Massachusetts Institute of Technology, Division of Health Sciences and Technology, Cambridge, Massachusetts 02139, and 4Keck Center for Integrative Neuroscience, Department of Physiology, University of California San Francisco, San Francisco, California 94143
The hippocampus is essential for learning complex spatial relationships, but little is known about how hippocampal neural activity changes as animals learn about a novel environment. We studied the formation of new place representations in rats by examining the changes in place-specific firing of neurons in the CA1 region of the hippocampus and the relationship between these changes and behavioral change across multiple days of exposure to novel places. We found that many neurons showed very rapid changes on the first day of exposure to the novel place, including many cases in which a previously silent neuron developed a place field over the course of a single pass through the environment. Across the population, the largest changes in neural activity occurred on day 2 of exposure to a novel place, but only if the animal had little experience (<4 min) in that location on day 1. Longer exposures on day 1 were associated with smaller changes on day 2, suggesting that hippocampal neurons required 5-6 min of experience to form a stable spatial representation. Even after the representation stabilized, the animals' behavior remained different in the novel places, suggesting that other brain regions continued to distinguish novel from familiar locations. These results show that the hippocampus can form new spatial representations quickly but that stable hippocampal representations are not sufficient for a place to be treated as familiar.
Key words: hippocampus; learning; memory; spatial; adaptive estimation; place cells
Received May 20, 2004; revised July 15, 2004; accepted July 23, 2004.
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