Long-term change in synaptic transmission in CA3 circuits followed by spontaneous rhythmic activity in rat hippocampal slices

The relevance of long-term potentiation (LTP) at excitatory synapses in CA3 circuits to generation of spontaneous epileptiform bursts in CA3 was investigated using rat hippocampal slices. CA3 pyramidal cells were antidromically stimulated through Schaffer collaterals. Evoked field potentials were extracellularly recorded from the stratum pyramidale and the stratum radiatum in CA3. Therefore, field potentials reflecting recurrent excitatory post-synaptic potentials (EPSPs) and inhibitory post-synaptic potentials (IPSPs) were positive at the stratum pyramidale and negative at the stratum radiatum. First, we tested how the amplitude of the evoked field potentials depends on a gamma-aminobutyric acid (GABA(A)) antagonist. Both of the positive and negative field potential peaks reduced in the medium containing penicillin (2 mM) or bicuculline (20 microM). This suggests that unmasked EPSPs due to suppression of IPSPs do not result in an increase in the evoked potentials. Second, CA3 pyramidal cells were antidromically stimulated by tetanic stimulation of Schaffer collaterals in order to induce LTP at synapses in CA3 circuits. Both of the positive and negative field potentials increased, suggesting that recurrent EPSPs were enhanced by tetanic stimulation. Induction of LTP at recurrent excitatory synapses was followed by spontaneous epileptiform bursts which persisted throughout experiments (approximately 1.5 h), while LTP of afferent synaptic potential evoked by hilar test stimulation was not induced. These results suggest that LTP at the afferent synapses is not necessary to spontaneous epileptiform bursts in CA3, but LTP at excitatory synapses between CA3 pyramidal cells contribute to spontaneous epileptiform bursts.

[1]  T. Freund,et al.  Differences between Somatic and Dendritic Inhibition in the Hippocampus , 1996, Neuron.

[2]  Hatsuo Hayashi,et al.  Chaotic responses of the hippocampal CA3 region to a mossy fiber stimulation in vitro , 1995, Brain Research.

[3]  J. Bouyer,et al.  Anatomical localization of cortical beta rhythms in cat , 1987, Neuroscience.

[4]  Vanderwolf Ch,et al.  Neocortical and hippocampal activation in relation to behavior: Effects of atropine, eserine, phenothiazines, and amphetamine. , 1975 .

[5]  Robert K. S. Wong,et al.  Latent synaptic pathways revealed after tetanic stimulation in the hippocampus , 1987, Nature.

[6]  R K Wong,et al.  Synchronized burst discharge in disinhibited hippocampal slice. I. Initiation in CA2-CA3 region. , 1983, Journal of neurophysiology.

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

[8]  T. Teyler,et al.  Long-term and short-term plasticity in the CA1, CA3, and dentate regions of the rat hippocampal slice , 1976, Brain Research.

[9]  J. Schneiderman,et al.  Hippocampal plasticity following epileptiform bursting produced by GABAA antagonists , 1994, Neuroscience.

[10]  J. Bouyer,et al.  Fast fronto-parietal rhythms during combined focused attentive behaviour and immobility in cat: cortical and thalamic localizations. , 1981, Electroencephalography and clinical neurophysiology.

[11]  F. Dudek,et al.  Mechanisms of neuronal synchronization during epileptiform activity. , 1999, Advances in neurology.

[12]  D. Prince,et al.  Penicillin‐induced epileptiform activity in the hippocampal in vitro preparation , 1977, Annals of neurology.

[13]  J. Swann,et al.  The dendritic origins of penicillin-induced epileptogenesis in CA3 hippocampal pyramidal cells. , 1986, Journal of neurophysiology.

[14]  J. Hablitz,et al.  Picrotoxin-induced epileptiform activity in hippocampus: role of endogenous versus synaptic factors. , 1984, Journal of neurophysiology.

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

[16]  H. Shinozaki,et al.  Activation of metabotropic glutamate receptor type 2/3 suppresses transmission at rat hippocampal mossy fibre synapses. , 1996, The Journal of physiology.

[17]  P. Somogyi,et al.  The hippocampal CA3 network: An in vivo intracellular labeling study , 1994, The Journal of comparative neurology.

[18]  F. L. D. Silva,et al.  Basic mechanisms of cerebral rhythmic activities , 1990 .

[19]  S. Nakanishi,et al.  Impairment of Hippocampal Mossy Fiber LTD in Mice Lacking mGluR2 , 1996, Science.

[20]  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.

[21]  Hatsuo Hayashi,et al.  Complexity of spatiotemporal activity of a neural network model which depends on the degree of synchronization , 1998, Neural Networks.

[22]  H. Boddeke,et al.  Synchronous 20 Hz rhythmic activity in hippocampal networks induced by activation of metabotropic glutamate receptors in vitro. , 1997, Neuroscience.

[23]  R. Traub,et al.  Enhanced NMDA conductance can account for epileptiform activity induced by low Mg2+ in the rat hippocampal slice. , 1994, The Journal of physiology.

[24]  Nobuaki Tamamaki,et al.  Crossing fiber arrays in the rat hippocampus as demonstrated by three‐dimensional reconstruction , 1991, The Journal of comparative neurology.

[25]  G. Laurent.  Dynamical representation of odors by oscillating and evolving neural assemblies , 1996, Trends in Neurosciences.

[26]  Hatsuo Hayashi,et al.  Spontaneous epileptiform bursts and long-term potentiation in rat CA3 hippocampal slices induced by chaotic stimulation of mossy fibers , 1998, Brain Research.

[27]  N. Tamamaki,et al.  Complete Axon Arborization of a Single CA3 Pyramidal Cell in the Rat Hippocampus, and its Relationship With Postsynaptic Parvalbumin‐containing Interneurons , 1993, The European journal of neuroscience.