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The Journal of Neuroscience, March 21, 2007, 27(12):3252-3259; doi:10.1523/JNEUROSCI.4941-06.2007

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Behavioral/Systems/Cognitive
Experience-Specific Functional Modification of the Dentate Gyrus through Adult Neurogenesis: A Critical Period during an Immature Stage

Ayumu Tashiro, Hiroshi Makino, and Fred H. Gage

Laboratory of Genetics, The Salk Institute for Biological Studies, La Jolla, California 92037

Correspondence should be addressed to Fred H. Gage, 10010 North Torrey Pines Road, La Jolla, CA 92037. Email: gage{at}salk.edu

Neural circuits in the dentate gyrus are continuously modified by adult neurogenesis, whose level is affected by the animal's experience. However, it is not known whether this experience-dependent anatomical modification alters the functional properties of the dentate gyrus. Here, using the expression of immediate early gene products, c-fos and Zif268, as indicators of recently activated neurons, we show that previous exposure to an enriched environment increases the total number of new neurons and the number of new neurons responding to reexposure to the same environment. The increase in the density of activated new neurons occurred specifically in response to exposure to the same environment but not to a different experience. Furthermore, we found that these experience-specific modifications are affected exclusively by previous exposure around the second week after neuronal birth but not later than 3 weeks. Thus, the animal's experience within a critical period during an immature stage of new neurons determines the survival and population response of the new neurons and may affect later neural representation of the experience in the dentate gyrus. This experience-specific functional modification through adult neurogenesis could be a mechanism by which new neurons exert a long-term influence on the function of the dentate gyrus related to learning and memory.

Key words: enriched environment; c-fos; zif268; immediate early gene; dentate gyrus; hippocampus; memory; neurogenesis

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Received Nov. 14, 2006; revised Jan. 30, 2007; accepted Feb. 15, 2007.

Correspondence should be addressed to Fred H. Gage, 10010 North Torrey Pines Road, La Jolla, CA 92037. Email: gage{at}salk.edu

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