Abstract
Neurogenesis in the suprapyramidal and infrapyramidal blades of the rostral dentate gyrus was investigated following kainic acid (KA)-induced status epilepticus (SE) in adult rats. Rats were injected with KA (14 mg/kg, i.p.) or saline, with convulsions terminated by an intraperitoneal injection of diazepam. Five days after the induction of SE, the rats were injected with 5-bromo-2-deoxyuridine-5-monophosphate (BrdU; 75 mg/kg, i.p), a marker of cell division. One day after the BrdU injection, the numbers of BrdU-labeled cells in the supra- and infrapyramidal blades were significantly higher in the KA-injected rats compared to the saline-injected rats. In the saline-injected rats, the number of BrdU-labeled cells in the infrapyramidal blade was greater than in the suprapyramidal blade. Twenty-eight days after the BrdU injection, the number of BrdU-labeled cells remained significantly higher in the KA-injected rats than the saline-injected rats, but only in the infrapyramidal blade. In addition, when the extent of cell death was examined with Fluoro-Jade B (a marker of dead and dying cells) 3 days after the induction of SE, degenerating cells were more numerous in the infrapyramidal blade than in the suprapyramidal blade. Our results suggest that there is an asymmetry of neurogenesis and cell death in the rostral dentate gyrus of rats following KA-induced SE.
Similar content being viewed by others
References
Acsady, L., Kamondi, A., Sik, A., Freund, T. F., and Buzsaki, G., GABAergic cells are the major postsynaptic targets of mossy fibers in the rat hippocampus.J. Neurosci., 18, 3386–3403 (1998).
Amaral, D. G., A Golgi study of cell types in the hilar region of the hippocampus in the rat.J. Comp. Neurol., 182, 851–914 (1978).
Amaral, D. G. and Campbell, M. J., Transmitter systems in the primate dentate gyrus.Hum. Neurobiol., 5, 169–180 (1986).
Ambrogini, P., Cuppini, R., Cuppini, C., Ciaroni, S., Cecchini, T., Ferri, P., Sartini, S., and Del Grande, P., Spatial learning affects immature granule cell survival in adult rat dentate gyrus.Neurosci. Lett., 286, 2124 (2000).
Bayer, S. A., Yackel, J. W., and Puri, P. S., Neurons in the rat dentate gyrus granular layer substantially increase during juvenile and adult life.Science, 216, 890892 (1982).
Bengzon, J., Kokaia, Z., Elmer, E., Nanobashvili, A., Kokaia, M., and Lindvall, O., Apoptosis and proliferation of dentate gyrus neurons after single and intermittent limbic seizures.Proc. Natl. Acad. Sci. U.S.A., 94, 10432–10437 (1997)
Biebl, M., Cooper, C. M., Winkler, J., and Kuhn, H. G., Analysis of neurogenesis and programmed cell death reveals a self- renewing capacity in the adult rat brain.Neurosci. Lett., 291, 17–20 (2000).
Blackstad, T. W., Brink, K., Hem, J., and Jeune, B., Distribution of hippocampal mossy fibers in the rat. An experimental study with silver impregnation methods.J. Comp. Neurol., 138, 433–450 (1970).
Brazel, C. Y., Nunez, J. L., Yang, Z., and Levison, S. W., Glutamate enhances survival and proliferation of neural progenitors derived from the subventricular zone.Neuroscience, 131, 55–65 (2005).
Cameron, H. A. and McKay, R., Stem cells and neurogenesis in the adult brain.Curr. Opin. Neurobiol., 8, 677–680 (1998).
Choi, Y. S., Lee, M. Y., Sung, K. W., Jeong, S. W., Choi, J. S., Park, H. J., Kim, O. N., Lee, S. B., and Kim, S. Y., Regional differences in enhanced neurogenesis in the dentate gyrus of adult rats after transient forebrain ischemia.Mol. Cells, 16, 232–238 (2003).
Christie, B. R. and Cameron, H. A., Neurogenesis in the adult hippocampus.Hippocampus, 16, 199–207 (2006).
Claiborne, B. J., Amaral, D. G., and Cowan, W. M., A light and electron microscopic analysis of the mossy fibers of the rat dentate gyrus.J. Comp. Neurol., 246, 435–458 (1986).
Covolan, L., Ribeiro, L. T., Longo, B. M., and Mello, L. E., Cell damage and neurogenesis in the dentate granule cell layer of adult rats after pilocarpine- or kainate-induced status epilepticus.Hippocampus, 10, 169–180 (2000).
Cronin, J. and Dudek, F. E., Chronic seizures and collateral sprouting of dentate mossy fibers after kainic acid treatment in rats.Brain Res., 474, 181–184 (1988).
Dong, H., Csernansky, C. A., Goico, B., and Csernansky, J. G., Hippocampal neurogenesis follows kainic acid-induced apoptosis in neonatal rats.J. Neurosci., 23, 1742–1749 (2003).
Encinas, J. M., Vaahtokari, A., and Enikolopov, G., Fluoxetine targets early progenitor cells in the adult brain.Proc. Natl. Acad. Sci. USA., 103, 8233–8238 (2006).
Freund, T. F., GABAergic septal and serotonergic median raphe afferents preferentially innervate inhibitory interneurons in the hippocampus and dentate gyrus.Epilepsy Res. Suppl., 7, 79–91 (1992).
Gage, F. H., Kempermann, G., Palmer, T. D., and Peterson, D. A., Multipotent progenitor cells in the adult dentate gyrus.J. Neurobiol., 36, 249266 (1998).
Golden, G. T., Smith, G. G., Ferraro, T. N., and Reyes, P. F., Rat strain and age differences in kainic acid induced seizures.Epilepsy Res., 20, 151–159 (1995).
Gould, E. and McEwen, B. S., Neuronal birth and death.Curr. Opin. Neurobiol., 3, 676–682 (1993).
Gray, W. P. and Sundstrom, L. E., Kainic acid increases the proliferation of granule cell progenitors in the dentate gyrus of the adult rat.Brain Res., 790, 52–59 (1998).
Grooms, S. Y., Opitz, T., Bennett, M. V., and Zukin, R. S., Status epilepticus decreases glutamate receptor 2 mRNA and protein expression in hippocampal pyramidal cells before neuronal death.Proc. Natl. Acad. Sci. U.S.A., 97, 3631–3636 (2000).
Hara, H., Onodera, H., Kogure, K., and Akaike, N., The regional difference of neuronal susceptibility in the dentate gyrus to hypoxia.Neurosci. Lett., 115, 189–194 (1990).
Jakubs, K., Nanobashvili, A., Bonde, S., Ekdahl, C. T., Kokaia, Z., Kokaia, M., and Lindvall, O., Environment matters: synaptic properties of neurons born in the epileptic adult brain develop to reduce excitability.Neuron, 52, 1047–1059 (2006).
Kempermann, G., Kuhn, H. G., and Gage, F. H., More hippocampal neurons in adult mice living in an enriched environment.Nature, 386, 493495 (1997).
Lawston, J., Borella, A., Robinson, J. K., and Whitaker-Azmitia, P. M., Changes in hippocampal morphology following chronic treatment with the synthetic cannabinoid WIN 55,212-2.Brain Res., 877, 407410 (2000).
Li, Y., Chopp, M., and Powers, C., Granule cell apoptosis and protein expression in hippocampal dentate gyrus after forebrain ischemia in the rat.J. Neurol. Sci., 150, 93–102 (1997).
Lledo, P. M., Alonso, M., and Grubb, M. S., Adult neurogenesis and functional plasticity in neuronal circuits.Nat. Rev. Neurosci., 7, 179–193 (2006).
Luk, K. C., Kennedy, T. E., and Sadikot, A. F., Glutamate promotes proliferation of striatal neuronal progenitors by an NMDA receptor-mediated mechanism.J. Neurosci., 23, 2239–2250 (2003).
Malberg, J. E., Eisch, A. J., Nestler, E. J., and Duman, R. S., Chronic antidepressant treatment increases neurogenesis in adult rat hippocampus.J. Neurosci., 20, 9104–9110 (2000).
Nácher, J., Varea, E., Miguel Blasco-Ibanez, J., Gomez-Climent, M. A., Castillo-Gomez, E., Crespo, C., Martinez-Guijarro, F. J., and McEwen B. S., N-methyl-d-aspartate receptor expression during adult neurogenesis in the rat dentate gyrus.Neuroscience, 144, 855–864 (2007).
Oleskevich, S., Descarries, L., and Lacaille, J. C., Quantified distribution of the noradrenaline innervation in the hippocampus of adult rat.J. Neurosci., 9, 3803–3015 (1989).
Oleskevich, S. and Descarries, L., Quantified distribution of the serotonin innervation in adult rat hippocampus.Neuroscience, 34, 19–33 (1990).
Osawa, M., Uemura, S., Kimura, H., and Sato, M., Amygdala kindling develops without mossy fiber sprouting and hippocampal neuronal degeneration in rats.Psychiatry Clin. Neurosci., 55, 549–557 (2001).
Parent, J. M., Yu, T. W., Leibowitz, R. T., Geschwind, D. H., Sloviter, R. S., and Lowenstein, D. H., Dentate granule cell neurogenesis is increased by seizures and contributes to aberrant network reorganization in the adult rat hippocampus.J. Neurosci., 17, 3727–3738 (1997).
Parent, J. M., Janumpalli, S., McNamara, J. O., and Lowenstein, D. H., Increased dentate granule cell neurogenesis following amygdala kindling in the adult rat.Neurosci. Lett., 247, 9–12 (1998).
Parent, J. M., Elliott, R. C., Pleasure, S. J., Barbara, N. M., and Lowenstein, D. H., Aberrant seizure-induced neurogenesis in experimental temporal lobe epilepsy.Ann. Neurol., 59, 81–91 (2006).
Paxinos, G. and Watson, C., The rat brain in stereotaxic coordinates, Fourth edition, Academic Press, San Diego (1998).
Scharff, C., Kirn, J. R., Grossman, M., Macklis, J. D., and Nottebohm, F., Targeted neuronal death affects neuronal replacement and vocal behavior in adult songbirds.Neuron, 25, 481–492 (2000).
Scharfman, H. E., Goodman, J. H., and Sollas, A. L., Granule- like neurons at the hilar/CA3 border after status epilepticus and their synchrony with area CA3 pyramidal cells: functional implications of seizure-induced neurogenesis.J. Neurosci., 20, 6144–6158 (2000).
Scharfman, H. E., Sollas, A. L., Smith, K. L., Jackson, M. B., and Goodman, J. H., Structural and functional asymmetry in the normal and epileptic rat dentate gyrus.J. Comp. Neurol., 454, 424439 (2002).
Seress, L. and Pokorny, J., Structure of the granular layer of the rat dentate gyrus. A light microscopic and Golgi study.J. Anat., 133, 181–195 (1981).
Smith, P. D., McLean, K. J., Murphy, M. A., Turnley, A. M., and Cook, M. J., Seizures, not hippocampal neuronal death, provoke neurogenesis in a mouse rapid electrical amygdala kindling model of seizures.Neuroscience, 136, 405–415 (2005).
Sperk, G., Lassmann, H., Baran, H., Seitelberger, F., and Hornykiewicz, O., Kainic acid-induced seizures: dose-relationship of behavioural, neurochemical and histopathological changes.Brain Res., 338, 289–295 (1985).
Suzuki, M., Nelson, A. D., Eickstaedt, J. B., Wallace, K., Wright, L. S., and Svendsen, C. N., Glutamate enhances proliferation and neurogenesis in human neural progenitor cell cultures derived from the fetal cortex.Eur. J. Neurosci., 24, 645–653 (2006).
Wang, Q., Yu, S., Simonyi, A., Sun, G. Y., and Sun, A. Y., Kainic acid-mediated excitotoxicity as a model for neurodegen- eration.Mol. Neurobiol., 31, 3–16 (2005).
Woodson, W., Nitecka, L., and Ben-Ari, Y., Organization of the GABAergic system in the rat hippocampal formation: a quantitative immunocytochemical study.J. Comp. Neurol., 280, 254–271 (1989).
Zhu, H., Dahlstrom, A., and Hansson, H. A., Characterization of cell proliferation in the adult dentate under normal conditions and after kainate induced seizures using ribonucleotide reductase and BrdU.Brain Res., 1036, 7–17 (2005).
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Choi, YS., Cho, KO. & Kim, S.Y. Asymmetry in enhanced neurogenesis in the rostral dentate gyrus following kainic acid-induced status epilepticus in adult rats. Arch Pharm Res 30, 646–652 (2007). https://doi.org/10.1007/BF02977661
Received:
Issue Date:
DOI: https://doi.org/10.1007/BF02977661