Transient and sustained types of long‐term potentiation in the CA1 area of the rat hippocampus

Synaptic potentiation induced by high frequency stimulation was investigated by recording field excitatory postsynaptic potentials (f-EPSPs) in rat hippocampal slices. Potentiation consisted of a transient period of decaying f-EPSPs (short-term potentiation, STP) that led to a plateau of continuously potentiated f-EPSPs (long-term potentiation, LTP). Here we show that a previously unknown type of transient, use-dependent, long-lasting potentiation (t-LTP) can account for STP. t-LTP could be stored for more than 6 h and its decay was caused by synaptic activation. Both the expression and the decay of t-LTP were input specific. t-LTP was induced differently from conventional LTP in that the amplitude of t-LTP was dependent upon the stimulation frequency, whereas the magnitude of LTP was dependent on the number of stimuli in the induction train. The decay of t-LTP could not be prevented by the blockage of glutamate receptors, but was prevented by the blockage of stimulus-evoked neurotransmitter release, suggesting that t-LTP is expressed presynaptically. Paired-pulse stimulation experiments showed that the decay of t-LTP was mediated by a decrease in the probability of neurotransmitter release. The decline of t-LTP could be prolonged by the activation of NMDA receptors. Hence, both single and paired-pulse stimuli prolonged the decline of the t-LTP. This decline could be prevented by high frequency burst stimulation (200 Hz). We conclude that t-LTP allows dynamic modulation of synaptic transmission by providing not only spatial association but also temporal convergence between synaptic inputs. Therefore, t-LTP might be a substrate for the encoding of synaptic memory.