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The Journal of Neuroscience, October 29, 2003, 23(30):9786-9795

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Cellular/Molecular
Depolarization-Induced Long-Term Depression at Hippocampal Mossy Fiber-CA3 Pyramidal Neuron Synapses

Saobo Lei,¹ Kenneth A. Pelkey,¹ Lisa Topolnik,² Patrice Congar,² Jean-Claude Lacaille,² and Chris J. McBain¹

¹Laboratory of Cellular and Synaptic Neurophysiology, National Institute of Child Health and Human Development, National Institutes of Health, Bethesda, Maryland 20892, and ²Département de Physiologie, Centre de Recherche en Sciences Neurologiques, Université de Montréal, Succursale Centreville, Montréal, Quebec, Canada H3C 3J7

Hippocampal CA3 pyramidal neurons receive two types of excitatory afferent innervation: mossy fibers (MFs) from granule cells of the dentate gyrus and recurrent collateral fibers (CFs) from other CA3 pyramidal neurons. At CF–CA3 pyramidal neuron synapses, membrane depolarization paired with low (0.33 Hz) presynaptic stimulation generated a heterogeneous response that ranged from long-term potentiation (LTP), long-term depression (LTD), to no alteration of synaptic strength. However, the same induction paradigm applied at MF–CA3 pyramidal neuron synapses consistently induced LTD. This novel form of LTD was independent of NMDARs, mGluRs, cannabinoid receptors, opioid receptors, or coincident synaptic activity, but was dependent on postsynaptic Ca²⁺ elevation through L-type Ca²⁺ channels and release from inositol 1,4,5-trisphosphate receptor-sensitive intracellular stores. Ca²⁺ imaging of both proximal and distal CA3 pyramidal neuron dendrites demonstrated that the depolarizing induction paradigm differentially elevated intracellular Ca²⁺ levels. L-type Ca²⁺ channel activation was observed only at the most proximal locations where mossy fibers make synapses. Depolarization-induced LTD did not occlude the conventional 1 Hz-induced LTD or vice versa, suggesting independent mechanisms underlie each form of plasticity. The paired-pulse ratio and coefficient of variation of synaptic transmission were unchanged after LTD induction, suggesting that the expression locus of LTD is postsynaptic. Moreover, peak-scaled nonstationary variance analysis indicated that depolarization-induced LTD correlated with a reduction in postsynaptic AMPA receptor numbers without a change in AMPA receptor conductance. Our results suggest that this novel form of LTD is selectively expressed at proximal dendritic locations closely associated with L-type Ca²⁺ channels.

Key words: LTD; depolarization; L-type Ca²⁺ channels; glutamate receptor; hippocampus; mossy fiber

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Received July 24, 2003; revised September 8, 2003; accepted September 9, 2003.

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