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The Journal of Neuroscience, October 24, 2007, 27(43):11510-11521; doi:10.1523/JNEUROSCI.3077-07.2007

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Development/Plasticity/Repair
Slow Presynaptic and Fast Postsynaptic Components of Compound Long-Term Potentiation

Ildar T. Bayazitov, Robert J. Richardson, Robert G. Fricke, and Stanislav S. Zakharenko

Department of Developmental Neurobiology, St. Jude Children's Research Hospital, Memphis, Tennessee 38105

Correspondence should be addressed to Stanislav S. Zakharenko, St. Jude Children's Research Hospital, 332 North Lauderdale Street, Mail Stop 323, Memphis, TN 38105. Email: stanislav.zakharenko{at}stjude.org

Long-term potentiation (LTP) mediates learning and memory in the mammalian hippocampus. Whether a presynaptic or postsynaptic neuron principally enhances synaptic transmission during LTP remains controversial. Acute hippocampal slices were made from transgenic mouse strains that express synaptopHluorin in neurons. SynaptopHluorin is an indicator of synaptic vesicle recycling; thus, we monitored functional changes in presynaptic boutons of CA3 pyramidal cells by measuring changes in synaptopHluorin fluorescence. Simultaneously, we recorded field excitatory postsynaptic potentials to monitor changes in the strength of excitatory synapses between CA3 and CA1 pyramidal neurons. We found that LTP consists of two components, a slow presynaptic component and a fast postsynaptic component. The presynaptic mechanisms contribute mostly to the late phase of compound LTP, whereas the postsynaptic mechanisms are crucial during the early phase of LTP. We also found that protein kinase A (PKA) and L-type voltage-gated calcium channels are crucial for the expression of the presynaptic component of compound LTP, and NMDA channels are essential for that of the postsynaptic component of LTP. These data are the first direct evidence that presynaptic and postsynaptic components of LTP are temporally and mechanistically distinct.

Key words: LTP; hippocampus; presynaptic; synaptic vesicle release; synaptopHluorin; two-photon laser-scanning microscopy; postsynaptic

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Received Jan. 4, 2007; revised Aug. 22, 2007; accepted Sept. 7, 2007.

Correspondence should be addressed to Stanislav S. Zakharenko, St. Jude Children's Research Hospital, 332 North Lauderdale Street, Mail Stop 323, Memphis, TN 38105. Email: stanislav.zakharenko{at}stjude.org

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