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The Journal of Neuroscience, September 17, 2003, 23(24):8471-8479
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Reduced Inhibition and Increased Output of Layer II Neurons in the Medial Entorhinal Cortex in a Model of Temporal Lobe Epilepsy
Masayuki Kobayashi,1,3 Xiling Wen,1 andPaul S. Buckmaster1,2 Departments of 1Comparative Medicine and 2Neurology and Neurological Sciences, Stanford University, Stanford, California 94305, and 3Department of Oral Physiology, Osaka University Graduate School of Dentistry, Osaka 565-0871, Japan
Temporal lobe epilepsy is the most common type of epilepsy in adults, and its underlying mechanisms are unclear. To investigate how the medial entorhinal cortex might contribute to temporal lobe epilepsy, we evaluated the histology and electrophysiology of slices from rats 3–7 d after an epileptogenic injury (pilocarpine-induced status epilepticus). Nissl staining, NeuN immunocytochemistry, and in situ hybridization for GAD65 mRNA were used to verify the preferential loss of glutamatergic neurons and the relative sparing of GABAergic interneurons in layer III. From slices adjacent to those that were used for anatomy, we obtained whole-cell patch recordings from layer II medial entorhinal cortical neurons. Recordings under current-clamp conditions revealed similar intrinsic electrophysiological properties (resting membrane potential, input resistance, single spike, and repetitive firing properties) to those of controls. Spontaneous IPSCs were less frequent (68% of controls), smaller in amplitude (57%), and transferred less charge (51%) than in controls. However, the frequency, amplitude, and rise time of miniature IPSCs were normal. These findings suggest that after epileptogenic injuries the layer II entorhinal cortical neurons receive less GABAA receptor-mediated synaptic input because presynaptic inhibitory interneurons become less active. To investigate the possible consequences of reduced spontaneous inhibitory input to layer II neurons, we recorded field potentials in the dentate gyrus, their major synaptic target. At 5 d after pilocarpine-induced status epilepticus the spontaneous field potentials recorded in vivo were over three times more frequent than in controls. These findings suggest that an epileptogenic injury reduces inhibition of layer II neurons and results in excessive synaptic input to the dentate gyrus.
Key words: pilocarpine; GABA; interneurons; IPSCs; GAD; dentate gyrus
Received April 16, 2003; revised July 29, 2003; accepted August 1, 2003.
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