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The Journal of Neuroscience, December 24, 2008, 28(52):14042-14055; doi:10.1523/JNEUROSCI.4848-08.2008

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Cellular/Molecular
Bidirectional Hebbian Plasticity at Hippocampal Mossy Fiber Synapses on CA3 Interneurons

Emilio J. Galván,¹ Eduardo Calixto,² and Germán Barrionuevo¹

¹Department of Neuroscience, University of Pittsburgh, Pittsburgh, Pennsylvania 15260, and ²División de Investigaciones en Neurociencias, Instituto Nacional de Psiquiatría, 14370 Mexico D.F., Mexico

Correspondence should be addressed to Germán Barrionuevo, Department of Neuroscience, A210 Langley Hall, University of Pittsburgh, Pittsburgh, PA 15260. Email: german{at}pitt.edu

Hippocampal area CA3 is critically involved in the formation of nonoverlapping neuronal subpopulations ("pattern separation") to store memory representations as distinct events. Efficient pattern separation relies on the strong and sparse excitatory input from the mossy fibers (MFs) to pyramidal cells and feedforward inhibitory interneurons. However, MF synapses on CA3 pyramidal cells undergo long-term potentiation (LTP), which, if unopposed, will degrade pattern separation because MF activation will now recruit additional CA3 pyramidal cells. Here, we demonstrate MF LTP in stratum lacunosum-moleculare (L-M) interneurons induced by the same stimulation protocol that induces MF LTP in pyramidal cells. This LTP was NMDA receptor (NMDAR) independent and occurred at MF Ca²⁺-impermeable AMPA receptor synapses. LTP was prevented by with voltage clamping the postsynaptic cell soma during high-frequency stimulation (HFS), intracellular injections of the Ca²⁺ chelator BAPTA (20 mM), or bath applications of the L-type Ca²⁺ channel blocker nimodipine (10 µM). We propose that MF LTP in L-M interneurons preserves the sparsity of pyramidal cell activation, thus allowing CA3 to maintain its role in pattern separation. In the presence of the mGluR1 antagonist LY367385 [(S)-(+)-a-amino-4-carboxy-2-methylbenzeneacetic acid] (100 µM), the same HFS that induces MF LTP in naive slices triggered NMDAR-independent MF LTD. This LTD, like LTP, required activation of the L-type Ca²⁺ channel and also was induced after blockade of IP₃ receptors with heparin (4 mg/ml) or the selective depletion of receptor-gated Ca²⁺ stores with ryanodine (10 or 100 µM). We conclude that L-M interneurons are endowed with Ca²⁺ signaling cascades suitable for controlling the polarity of MF long-term plasticity induced by joint presynaptic and postsynaptic activities.

Key words: mossy fiber; LTP; LTD; calcium-impermeable AMPARs; CA3 interneurons; feedforward inhibition

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Received Oct. 8, 2008; revised Oct. 23, 2008; accepted Oct. 27, 2008.

Correspondence should be addressed to Germán Barrionuevo, Department of Neuroscience, A210 Langley Hall, University of Pittsburgh, Pittsburgh, PA 15260. Email: german{at}pitt.edu

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