Induction of synaptic potentiation in hippocampus by patterned stimulation involves two events.

Electrical stimulation of axons in the hippocampus with short high-frequency bursts that resemble in vivo activity patterns produces stable potentiation of postsynaptic responses when the bursts occur at intervals of 200 milliseconds but not 2 seconds. When a burst was applied to one input and a second burst applied to a different input to the same target neuron 200 milliseconds later, only the synapses activated by the second burst showed stable potentiation. This effect was observed even when the two inputs innervated completely different regions of the postsynaptic cells; but did not occur when the inputs were stimulated simultaneously or when the second burst was delayed by 2 seconds. Intracellular recordings indicated that the first burst extended the decay phase of excitatory postsynaptic potentials evoked 200 milliseconds later. These results suggest that a single burst of axonal stimulation produces a transient, spatially diffuse "priming" effect that prolongs responses to subsequent bursts, and that these altered responses trigger spatially restricted synaptic modifications. The similarity of the temporal parameters of the priming effect and the theta rhythm that dominates the hippocampal electroencephalogram (EEG) during learning episodes suggests that this priming may be involved in behaviorally induced synaptic plasticity.

[1]  C. H. Vanderwolf,et al.  Hippocampal electrical activity and voluntary movement in the rat. , 1969, Electroencephalography and clinical neurophysiology.

[2]  J. B. Ranck,et al.  Studies on single neurons in dorsal hippocampal formation and septum in unrestrained rats. I. Behavioral correlates and firing repertoires. , 1973, Experimental neurology.

[3]  T. Bliss,et al.  Long‐lasting potentiation of synaptic transmission in the dentate area of the anaesthetized rabbit following stimulation of the perforant path , 1973, The Journal of physiology.

[4]  J. Winson,et al.  Patterns of hippocampal theta rhythm in the freely moving rat. , 1974, Electroencephalography and clinical neurophysiology.

[5]  B. McNaughton,et al.  Synaptic enhancement in fascia dentata: Cooperativity among coactive afferents , 1978, Brain Research.

[6]  G. Lynch,et al.  Long‐term potentiation and depression of synaptic responses in the rat hippocampus: localization and frequency dependency. , 1978, The Journal of physiology.

[7]  W. Levy,et al.  Synapses as associative memory elements in the hippocampal formation , 1979, Brain Research.

[8]  T. H. Brown,et al.  Passive electrical constants in three classes of hippocampal neurons. , 1981, Journal of neurophysiology.

[9]  T. H. Brown,et al.  Long-term synaptic potentiation in the superior cervical ganglion. , 1982, Science.

[10]  Kevin S. Lee Sustained enhancement of evoked potentials following brief, high-frequency stimulation of the cerebral cortex in vitro , 1982, Brain Research.

[11]  T. Bliss,et al.  What is the mechanism of long-term potentiation in the hippocampus? , 1982, Trends in Neurosciences.

[12]  R. Douglas,et al.  Inhibitory modulation of long-term potentiation: Evidence for a postsynaptic locus of control , 1982, Brain Research.

[13]  K. Lee Cooperativity among afferents for the induction of long-term potentiation in the CA1 region of the hippocampus , 1983, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[14]  G. Collingridge,et al.  Excitatory amino acids in synaptic transmission in the Schaffer collateral‐commissural pathway of the rat hippocampus. , 1983, The Journal of physiology.

[15]  N. Weinberger,et al.  Long term potentiation in the magnocellular medial geniculate nucleus of the anesthetized cat , 1983, Brain Research.

[16]  G. Lynch,et al.  Intracellular injections of EGTA block induction of hippocampal long-term potentiation , 1983, Nature.

[17]  J. Eccles Calcium in long-term potentiation as a model for memory , 1983, Neuroscience.

[18]  R. Dingledine N‐methyl aspartate activates voltage‐dependent calcium conductance in rat hippocampal pyramidal cells. , 1983, The Journal of physiology.

[19]  H. Wigström,et al.  Facilitated induction of hippocampal long-lasting potentiation during blockade of inhibition , 1983, Nature.

[20]  R. Racine,et al.  Long-term potentiation phenomena in the rat limbic forebrain , 1983, Brain Research.

[21]  G. Lynch,et al.  The biochemistry of memory: a new and specific hypothesis. , 1984, Science.

[22]  L. Nowak,et al.  Magnesium gates glutamate-activated channels in mouse central neurones , 1984, Nature.

[23]  A. Ganong,et al.  Long-term potentiation in the hippocampus involves activation of N-methyl-D-aspartate receptors , 1984, Brain Research.

[24]  M. Mayer,et al.  Mg2+ dependence of membrane resistance increases evoked by NMDA in hippocampal neurones , 1984, Brain Research.

[25]  H. Wigström,et al.  A synaptic potential following single volleys in the hippocampal CA1 region possibly involved in the induction of long-lasting potentiation. , 1985, Acta physiologica Scandinavica.