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Efficient induction of long-term potentiation and depression under behaviorally relevant activity conditions

Gayle M. Wittenberg and Samuel S.-H. Wang

Princeton University

The relative timing of pre- and post-synaptic action potentials has been shown to influence both the sign and magnitude of synaptic plasticity. Such spike timing-dependent plasticity has been observed in a number of synapses. However, neural activity also has structure on longer time scales. One example is the hippocampal theta rhythm, which in rats occurs during active spatial exploration and has a characteristic frequency of 5-10 oscillations per second. Here we report how the induction of hippocampal CA3-CA1 synaptic plasticity depends on neural events with realistic overall temporal structure. We found that the induction of spike timing-dependent long-term potentiation (LTP) required two events that are likely to occur during theta rhythm: burst firing in the postsynaptic CA1 neuron and sustained pairing at 5 Hz. Low-frequency pairing (0.5 Hz) of single presynaptic action potentials followed by single postsynaptic action potentials was insufficient to generate LTP. This surprising finding was observed if the patch pipette contained a physiological, potassium-based recording solution, but not if the pipette contained a cesium-based recording solution (Nishiyama et al. 2000 Nature 408:584-588). Reversing the firing order within each pairing resulted in long-term depression (LTD). These results suggest that key features of behaviorally relevant neural activity, in this case burst firing associated with the theta rhythm, can be essential for gating synaptic plasticity.