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The Journal of Neuroscience, August 2, 2006, 26(31):8137-8147; doi:10.1523/JNEUROSCI.1183-06.2006

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Cellular/Molecular
Actin-Dependent Activation of Presynaptic Silent Synapses Contributes to Long-Term Synaptic Plasticity in Developing Hippocampal Neurons

Jun Yao, Jinshun Qi, and Gong Chen

Department of Biology, The Pennsylvania State University, University Park, Pennsylvania 16802

Correspondence should be addressed to Dr. Gong Chen, Assistant Professor, Department of Biology, Huck Institutes of Life Sciences, 201 Life Sciences Building, The Pennsylvania State University, University Park, PA 16802. Email: gongchen{at}psu.edu

Developing neurons have greater capacity in experience-dependent plasticity than adult neurons but the molecular mechanism is not well understood. Here we report a developmentally regulated long-term synaptic plasticity through actin-dependent activation of presynaptic silent synapses in cultured hippocampal neurons. Live FM 1-43 imaging and retrospective immunocytochemistry revealed that many presynaptic boutons in immature neurons are functionally silent at resting conditions, but can be converted into active ones after repetitive neuronal stimulation. The activation of presynaptic silent synapses is dependent on L-type calcium channels and protein kinase A (PKA)/PKC signaling pathways. Moreover, blocking actin polymerization with latrunculin A and cytochalasin B abolishes long-term increase of presynaptic functional boutons induced by repetitive stimulation, whereas actin polymerizer jasplakinolide increases the number of active boutons in immature neurons. In mature neurons, however, presynaptic boutons are mostly functional and repetitive stimulation did not induce additional enhancement. Quantitative immunostaining with phalloidin revealed a significant increase in axonal F-actin level after repetitive stimulation in immature but not mature neurons. These results suggest that actin-dependent activation of presynaptic silent synapses contributes significantly to the long-term synaptic plasticity during neuronal development.

Key words: actin; activity; synaptic plasticity; presynaptic; silent synapse; hippocampus

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Received Dec. 8, 2005; revised June 4, 2006; accepted July 3, 2006.

Correspondence should be addressed to Dr. Gong Chen, Assistant Professor, Department of Biology, Huck Institutes of Life Sciences, 201 Life Sciences Building, The Pennsylvania State University, University Park, PA 16802. Email: gongchen{at}psu.edu

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