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The Journal of Neuroscience, March 3, 2004, 24(9):2259-2269; doi:10.1523/JNEUROSCI.5191-03.2004

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Development/Plasticity/Repair
Rapid Deletion of Mossy Cells Does Not Result in a Hyperexcitable Dentate Gyrus: Implications for Epileptogenesis

Anna d. H. Ratzliff, Allyson L. Howard, Vijayalakshmi Santhakumar, Imola Osapay, and Ivan Soltesz

Department of Anatomy and Neurobiology, University of California, Irvine, California 92697

Loss of cells from the hilus of the dentate gyrus is a major histological hallmark of human temporal lobe epilepsy. Hilar mossy cells, in particular, are thought to show dramatic numerical reductions in pathological conditions, and one prominent theory of epileptogenesis is based on the assumption that mossy cell loss directly results in granule cell hyperexcitability. However, whether it is the disappearance of hilar mossy cells from the dentate gyrus circuitry after various insults or the subsequent synaptic-cellular alterations (e.g., reactive axonal sprouting) that lead to dentate hyperexcitability has not been rigorously tested, because of the lack of available techniques to rapidly remove specific classes of nonprincipal cells from neuronal networks.

We developed a fast, cell-specific ablation technique that allowed the targeted lesioning of either mossy cells or GABAergic interneurons in horizontal as well as axial (longitudinal) slices of the hippocampus. The results demonstrate that mossy cell deletion consistently decreased the excitability of granule cells to perforant path stimulation both within and outside of the lamella where the mossy cell ablation took place. In contrast, ablation of interneurons caused the expected increase in excitability, and control aspirations of the hilar neuropil or of interneurons in the presence of GABA receptor blockers caused no alteration in granule cell excitability.

These data do not support the hypothesis that loss of mossy cells from the dentate hilus after seizures or traumatic brain injury directly results in hyperexcitability.

Key words: epilepsy; mossy cell; hyperexcitability; hilar cell loss; dentate gyrus; dormant basket cell hypothesis

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Received July 1, 2003; revised January 12, 2004; accepted January 15, 2004.

This article has been cited by other articles:

				A. K. Sharma, R. Y. Reams, W. H. Jordan, M. A. Miller, H. L. Thacker, and P. W. Snyder Mesial Temporal Lobe Epilepsy: Pathogenesis, Induced Rodent Models and Lesions Toxicol Pathol, December 1, 2007; 35(7): 984 - 999. [Abstract] [PDF]

				J. Veliskova and L. Velisek {beta}-Estradiol Increases Dentate Gyrus Inhibition in Female Rats via Augmentation of Hilar Neuropeptide Y J. Neurosci., May 30, 2007; 27(22): 6054 - 6063. [Abstract] [Full Text] [PDF]

				A. L. Howard, A. Neu, R. J. Morgan, J. C. Echegoyen, and I. Soltesz Opposing Modifications in Intrinsic Currents and Synaptic Inputs in Post-Traumatic Mossy Cells: Evidence for Single-Cell Homeostasis in a Hyperexcitable Network J Neurophysiol, March 1, 2007; 97(3): 2394 - 2409. [Abstract] [Full Text] [PDF]

				J. Dyhrfjeld-Johnsen, V. Santhakumar, R. J. Morgan, R. Huerta, L. Tsimring, and I. Soltesz Topological Determinants of Epileptogenesis in Large-Scale Structural and Functional Models of the Dentate Gyrus Derived From Experimental Data J Neurophysiol, February 1, 2007; 97(2): 1566 - 1587. [Abstract] [Full Text] [PDF]

				A. M. Kerr and M. Capogna Unitary IPSPs enhance hilar mossy cell gain in the rat hippocampus J. Physiol., January 15, 2007; 578(2): 451 - 470. [Abstract] [Full Text] [PDF]

				M. E. Hofmann, B. Nahir, and C. J. Frazier Endocannabinoid-Mediated Depolarization-Induced Suppression of Inhibition in Hilar Mossy Cells of the Rat Dentate Gyrus J Neurophysiol, November 1, 2006; 96(5): 2501 - 2512. [Abstract] [Full Text] [PDF]

				V. Santhakumar, I. Aradi, and I. Soltesz Role of Mossy Fiber Sprouting and Mossy Cell Loss in Hyperexcitability: A Network Model of the Dentate Gyrus Incorporating Cell Types and Axonal Topography J Neurophysiol, January 1, 2005; 93(1): 437 - 453. [Abstract] [Full Text] [PDF]

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