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The Journal of Neuroscience, June 28, 2006, 26(26):7082-7092; doi:10.1523/JNEUROSCI.1666-06.2006

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Development/Plasticity/Repair
Ongoing Epileptiform Activity in the Post-Ischemic Hippocampus Is Associated with a Permanent Shift of the Excitatory–Inhibitory Synaptic Balance in CA3 Pyramidal Neurons

Jérôme Epsztein, Mathieu Milh, Rachid Id Bihi, Isabel Jorquera, Yehezkel Ben-Ari, Alfonso Represa, and Valérie Crépel

Institut de Neurobiologie de la Méditerranée, Institut National de la Santé et de la Recherche Médicale Unité 29, and Université de La Méditerranée, Parc scientifique de Luminy, 13273 Marseille Cedex 09, France

Correspondence should be addressed to Dr. Valérie Crépel, Institut de Neurobiologie de la Méditerranée, Institut National de la Santé et de la Recherche Médicale Unité 29, and Université de La Méditerranée, Parc scientifique de Luminy, BP 13, 13273 Marseille Cedex 09, France. Email: crepel{at}inmed.univ-mrs.fr

Ischemic strokes are often associated with late-onset epilepsy, but the underlying mechanisms are poorly understood. In the hippocampus, which is one of the regions most sensitive to ischemic challenge, global ischemia induces a complete loss of CA1 pyramidal neurons, whereas the resistant CA3 pyramidal neurons display a long-term hyperexcitability several months after the insult. The mechanisms of this long-term hyperexcitability remain unknown despite its clinical implication. Using chronic in vivo EEG recordings and in vitro field recordings in slices, we now report spontaneous interictal epileptiform discharges in the CA3 area of the hippocampus from post-ischemic rats several months after the insult. Whole-cell recordings from CA3 pyramidal neurons, revealed a permanent reduction in the frequency of spontaneous and miniature GABAergic IPSCs and a parallel increase in the frequency of spontaneous and miniature glutamatergic postsynaptic currents. Global ischemia also induced a dramatic loss of GABAergic interneurons and terminals together with an increase in glutamatergic terminals in the CA3 area of the hippocampus. Altogether, our results show a morpho-functional reorganization in the CA3 network several months after global ischemia, resulting in a net shift in the excitatory–inhibitory balance toward excitation that may constitute a substrate for the generation of epileptiform discharges in the post-ischemic hippocampus.

Key words: GABA; glutamate; interneuron; ischemia; interictal; stroke

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Received June 24, 2004; revised May 24, 2006; accepted May 24, 2006.

Correspondence should be addressed to Dr. Valérie Crépel, Institut de Neurobiologie de la Méditerranée, Institut National de la Santé et de la Recherche Médicale Unité 29, and Université de La Méditerranée, Parc scientifique de Luminy, BP 13, 13273 Marseille Cedex 09, France. Email: crepel{at}inmed.univ-mrs.fr

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