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The Journal of Neuroscience, July 25, 2007, 27(30):8031-8039; doi:10.1523/JNEUROSCI.2003-07.2007

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Behavioral/Systems/Cognitive
Evidence That Long-Term Potentiation Occurs within Individual Hippocampal Synapses during Learning

Vadim Fedulov,¹ Christopher S. Rex,² Danielle A. Simmons,³ Linda Palmer,⁴ Christine M. Gall,^1,2 and Gary Lynch³

Departments of ¹Anatomy and Neurobiology, ²Neurobiology and Behavior, and ³Psychiatry and Human Behavior, University of California, Irvine, California 92617-4291, and ⁴Department of Philosophy, Carnegie Mellon University, Pittsburgh, Pennsylvania 15213

Correspondence should be addressed to Gary Lynch, 101 Theory Drive, #250, University of California, Irvine, CA 92612-1695. Email: glynch{at}uci.edu

Stabilization of long-term potentiation (LTP) depends on multiple signaling cascades linked to actin polymerization. We used one of these, involving phosphorylation of the regulatory protein cofilin, as a marker to test whether LTP-related changes occur in hippocampal synapses during unsupervised learning. Well handled rats were allowed to explore a compartmentalized environment for 30 min after an injection of vehicle or the NMDA receptor antagonist (±)-3-(2-carboxypiperazin-4-yl)propyl-1-phosphonic acid (CPP). Another group of rats consisted of vehicle-injected, home-cage controls. Vehicle-treated rats that explored the environment had 30% more spines with dense phosphorylated (p) cofilin immunoreactivity in hippocampal field CA1 than did rats in the home-cage group. The increase in pCofilin-positive spines and behavioral evidence for memory of the explored environment were both eliminated by CPP. Coimmunostaining for pCofilin and the postsynaptic density protein 95 (PSD-95) showed that synapses on pCofilin-positive spines were substantially larger than those on neighboring (pCofilin-negative) spines. These results establish that uncommon cellular events associated with LTP, including changes in synapse size, occur in individual spines during learning, and provide a technique for mapping potential engrams.

Key words: cofilin; actin; PSD-95; phosphorylation; unsupervised learning; immunoreactivity

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Received May 2, 2007; revised June 14, 2007; accepted June 14, 2007.

Correspondence should be addressed to Gary Lynch, 101 Theory Drive, #250, University of California, Irvine, CA 92612-1695. Email: glynch{at}uci.edu

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