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The Journal of Neuroscience, May 16, 2007, 27(20):5363-5372; doi:10.1523/JNEUROSCI.0164-07.2007

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Behavioral/Systems/Cognitive
Changes in Synaptic Morphology Accompany Actin Signaling during LTP

Lulu Y. Chen,^1 * Christopher S. Rex,^3 * Malcolm S. Casale,² Christine M. Gall,^1,3 and Gary Lynch²

¹Departments of Anatomy and Neurobiology and ²Psychiatry and Human Behavior, University of California, Irvine, California 92697-4292, and ³Department of Neurobiology and Behavior, University of California, Irvine, California 92697-4550

Correspondence should be addressed to Christine M. Gall, Gillespie Neuroscience Research Facility, University of California, Irvine, CA 92697-4292. Email: cmgall{at}uci.edu

Stabilization of long-term potentiation (LTP) is commonly proposed to involve changes in synaptic morphology and reorganization of the spine cytoskeleton. Here we tested whether, as predicted from this hypothesis, induction of LTP by theta-burst stimulation activates an actin regulatory pathway and alters synapse morphology within the same dendritic spines. TBS increased severalfold the numbers of spines containing phosphorylated (p) p21-activated kinase (PAK) or its downstream target cofilin; the latter regulates actin filament assembly. The PAK/cofilin phosphoproteins were increased at 2 min but not 30 s post-TBS, peaked at 7 min, and then declined. Double immunostaining for the postsynaptic density protein PSD95 revealed that spines with high pPAK or pCofilin levels had larger synapses (+60–70%) with a more normal size frequency distribution than did neighboring spines. Based on these results and simulations of shape changes to synapse-like objects, we propose that theta stimulation markedly increases the probability that a spine will enter a state characterized by a large, ovoid synapse and that this morphology is important for expression and later stabilization of LTP.

Key words: synaptic plasticity; p21-activated kinase; cofilin; dendritic spines; postsynaptic density; phosphorylation

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Received Jan. 15, 2007; revised April 11, 2007; accepted April 12, 2007.

Correspondence should be addressed to Christine M. Gall, Gillespie Neuroscience Research Facility, University of California, Irvine, CA 92697-4292. Email: cmgall{at}uci.edu

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