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The Journal of Neuroscience, March 3, 2004, 24(9):2112-2121; doi:10.1523/JNEUROSCI.4645-03.2004

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Cellular/Molecular
Two Loci of Expression for Long-Term Depression at Hippocampal Mossy Fiber-Interneuron Synapses

Saobo Lei and Chris J. McBain

Laboratory of Cellular and Synaptic Neurophysiology, National Institute of Child Health and Human Development, National Institutes of Health, Bethesda, Maryland 20892-4495

Two distinct forms of long-term depression (LTD) exist at mossy fiber synapses between dentate gyrus granule cells and hippocampal CA3 stratum lucidum interneurons. Although induction of each form of LTD requires an elevation of postsynaptic intracellular Ca²⁺, at Ca²⁺-impermeable AMPA receptor (CI-AMPAR) synapses, induction is NMDA receptor (NMDAR) dependent, whereas LTD at Ca²⁺-permeable AMPA receptor (CP-AMPAR) synapses is NMDAR independent. However, the expression locus of either form of LTD is not known. Using a number of criteria, including the coefficient of variation, paired-pulse ratio, AMPA-NMDA receptor activity, and the low-affinity AMPAR antagonist -D-glutamyl-glycine, we demonstrate that LTD expression at CP-AMPAR synapses is presynaptic and results from reduced transmitter release, whereas LTD expression at CI-AMPAR synapses is postsynaptic. The N-ethylmaleimide-sensitive fusion protein-AP2-clathrin adaptor protein 2 inhibitory peptide pep2m occluded LTD expression at CI-AMPAR synapses but not at CP-AMPAR synapses, confirming that CI-AMPAR LTD involves postsynaptic AMPAR trafficking. Thus, mossy fiber innervation of CA3 stratum lucidum interneurons occurs via two parallel systems targeted to either Ca²⁺-permeable or Ca²⁺-impermeable AMPA receptors, each with a distinct expression locus for long-term synaptic plasticity.

Key words: AMPA; depression; hippocampus; interneuron; synapse; glutamate

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Received Oct 14, 2003; revised December 17, 2003; accepted January 6, 2004.

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