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The Journal of Neuroscience, December 15, 1999, 19(24):10664-10671

Heterogeneity of Synaptic Plasticity at Unitary CA3-CA1 and CA3-CA3 Connections in Rat Hippocampal Slice Cultures

Dominique Debanne^{1, 2}, Beat H. Gähwiler¹, and Scott M. Thompson³

¹ Brain Research Institute, University of Zurich, CH-8057 Zurich, Switzerland, ² Unité de Neurocybernétique Cellulaire, Centre National de la Recherche Scientifique, Unité Propre de Recherche 9041, F-13009 Marseille, France, and ³ Department of Physiology, University of Maryland School of Medicine, Baltimore, Maryland 21201

Long-term potentiation (LTP) of unitary EPSPs, generated by pairs of monosynaptically connected CA3 and CA1 pyramidal cells, was compared with LTP of extracellularly evoked, multi-unitary EPSPs in rat hippocampal slice cultures. LTP was induced by repeated, synchronous pairing of low-frequency presynaptic and postsynaptic activity. Three differences were observed. First, LTP of multi-unitary EPSPs displayed two phases: transient (<5 min) and sustained. Potentiation of unitary EPSPs displayed both phases in 42% of experiments; the remainder showed sustained potentiation only. Unitary EPSPs displaying transient-sustained and only sustained potentiation could be recorded from single postsynaptic cells, indicating that excitatory synapses on a given cell are heterogeneous with respect to short-term plasticity. Second, whereas LTP of multi-unitary EPSPs never resulted in greater than twofold increases in amplitude (mean potentiation of 175% of control), maximal LTP of unitary EPSPs was as great as 13-fold (mean potentiation of 250%). Third, LTP could not be induced in 24% of unitary EPSPs. We provide here the first evidence for the coexistence of potentiatable and nonpotentiatable synapses on individual postsynaptic neurons. Thirty-seven percent of connections not displaying LTP exhibited long-term depression (LTD), suggesting that the connections were already maximally potentiated. In the remaining 63% of these pairs, neither LTP nor LTD could be induced, despite the existence of a pharmacologically identified, NMDA receptor-mediated EPSP component. In conclusion, there is considerable heterogeneity in the amplitude and time course of LTP expression at different synaptic connections. A substantial proportion of apparently nonplastic synapses probably accounts for the weaker potentiation displayed by compound EPSPs.

Key words: excitatory synapse; hippocampus; long-term potentiation; long-term depression; synaptic plasticity

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Copyright © 1999 Society for Neuroscience  0270-6474/99/192410664-08$05.00/0

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