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The Journal of Neuroscience, January 28, 2004, 24(4):853-864; doi:10.1523/JNEUROSCI.1619-03.2004

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Neurobiology of Disease
Translamellar Disinhibition in the Rat Hippocampal Dentate Gyrus after Seizure-Induced Degeneration of Vulnerable Hilar Neurons

Colin A. Zappone and Robert S. Sloviter

Departments of Pharmacology and Neurology, and the Graduate Program in Neuroscience, University of Arizona College of Medicine, Tucson, Arizona 85724

Longitudinally restricted axonal projections of hippocampal granule cells suggest that transverse segments of the granule cell layer may operate independently (the "lamellar" hypothesis). Longitudinal projections of excitatory hilar mossy cells could be viewed as antithetical to lamellar function, but only if longitudinal impulse flow effectively excites distant granule cells. We, therefore, determined the effect of focal granule cell discharges on granule cells located >2 mm along the longitudinal axis. During perforant pathway stimulation in urethane-anesthetized rats, passive diffusion of the GABA_A receptor antagonist bicuculline methiodide from the tip of a glass recording electrode evoked granule cell discharges and c-Fos expression in granule cells, mossy cells, and inhibitory interneurons, within a 400 µm radius. This focally evoked activity powerfully suppressed distant granule cell-evoked responses recorded simultaneously 2.5–4.5 mm longitudinally. Three days after kainic acid-induced status epilepticus or prolonged perforant pathway stimulation, translamellar inhibition was intact in rats with <40% hilar neuron loss but was consistently abolished after extensive (>85%) hilar cell loss. Retrograde transport of Fluoro-Gold (FG) from the rostral dentate gyrus revealed that few inhibitory interneurons were among the many retrogradely labeled hilar neurons 2.5–4.5 mm longitudinally. Although many somatostatin-positive hilar interneurons effectively transported FG from the distant septum, few of these neurons transported detectable FG from much closer hippocampal injection sites. Inhibitory basket and chandelier cells also exhibited minimal longitudinal FG transport. These findings suggest that translamellar disinhibition may result from the loss of vulnerable, longitudinally projecting mossy cells and may represent a network-level mechanism underlying postinjury hippocampal dysfunction and epileptic network hyperexcitability.

Key words: lamellar hypothesis; inhibitory interneurons; hippocampus; epilepsy; c-Fos; lateral inhibition

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Received July 18, 2003; revised November 25, 2003; accepted November 25, 2003.

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