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Volume 17, Number 10, Issue of May 15, 1997 pp. 3727-3738
Copyright ©1997 Society for Neuroscience

Dentate Granule Cell Neurogenesis Is Increased by Seizures and Contributes to Aberrant Network Reorganization in the Adult Rat Hippocampus

Received Nov. 2, 1996; revised Feb. 11, 1997; accepted Feb. 27, 1997.

Jack M. Parent1, Timothy W. Yu2, Rebecca T. Leibowitz1, Daniel H. Geschwind3, Robert S. Sloviter4, and Daniel H. Lowenstein1, 2

1 Departments of Neurology and Anatomy, and 2 Graduate Program in Neuroscience, University of California, San Francisco, California 94143, 3 Department of Neurology, University of California, Los Angeles, California 90024, 4 Neurology Research Center, Helen Hayes Hospital, West Haverstraw, New York 10993, and Departments of Pharmacology and Neurology, Columbia University, New York, New York 10032

The dentate granule cell layer of the rodent hippocampal formation has the distinctive property of ongoing neurogenesis that continues throughout adult life. In both human temporal lobe epilepsy and rodent models of limbic epilepsy, this same neuronal population undergoes extensive remodeling, including reorganization of mossy fibers, dispersion of the granule cell layer, and the appearance of granule cells in ectopic locations within the dentate gyrus. The mechanistic basis of these abnormalities, as well as their potential relationship to dentate granule cell neurogenesis, is unknown. We used a systemic chemoconvulsant model of temporal lobe epilepsy and bromodeoxyuridine (BrdU) labeling to investigate the effects of prolonged seizures on dentate granule cell neurogenesis in adult rats, and to examine the contribution of newly differentiated dentate granule cells to the network changes seen in this model. Pilocarpine-induced status epilepticus caused a dramatic and prolonged increase in cell proliferation in the dentate subgranular proliferative zone (SGZ), an area known to contain neuronal precursor cells. Colocalization of BrdU-immunolabeled cells with the neuron-specific markers turned on after division, 64 kDa, class III beta -tubulin, or microtubule-associated protein-2 showed that the vast majority of these mitotically active cells differentiated into neurons in the granule cell layer. Newly generated dentate granule cells also appeared in ectopic locations in the hilus and inner molecular layer of the dentate gyrus. Furthermore, developing granule cells projected axons aberrantly to both the CA3 pyramidal cell region and the dentate inner molecular layer. Induction of hippocampal seizure activity by perforant path stimulation resulted in an increase in SGZ mitotic activity similar to that seen with pilocarpine administration. These observations indicate that prolonged seizure discharges stimulate dentate granule cell neurogenesis, and that hippocampal network plasticity associated with epileptogenesis may arise from aberrant connections formed by newly born dentate granule cells.

Key words: hippocampus; dentate granule cells; neurogenesis; pilocarpine; seizures; epilepsy; mossy fiber sprouting; network reorganization; synaptic plasticity




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H. Dong, C. A. Csernansky, B. Goico, and J. G. Csernansky
Hippocampal Neurogenesis Follows Kainic Acid-Induced Apoptosis in Neonatal Rats
J. Neurosci., March 1, 2003; 23(5): 1742 - 1749.
[Abstract] [Full Text] [PDF]

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 FASEB J.Home page
Y. ZHU, K. JIN, X. O. MAO, and D. A. GREENBERG
Vascular endothelial growth factor promotes proliferation of cortical neuron precursors by regulating E2F expression
FASEB J, February 1, 2003; 17(2): 186 - 193.
[Abstract] [Full Text] [PDF]

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 ASH Education BookHome page
G. Q. Daley, M. A. Goodell, and E. Y. Snyder
Realistic Prospects for Stem Cell Therapeutics
Hematology, January 1, 2003; 2003(1): 398 - 418.
[Abstract] [Full Text] [PDF]

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 J. Neurosci.Home page
S. C. Danzer, K. R. C. Crooks, D. C. Lo, and J. O. McNamara
Increased Expression of Brain-Derived Neurotrophic Factor Induces Formation of Basal Dendrites and Axonal Branching in Dentate Granule Cells in Hippocampal Explant Cultures
J. Neurosci., November 15, 2002; 22(22): 9754 - 9763.
[Abstract] [Full Text] [PDF]

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 NeurologyHome page
S. Faverjon, D. C. Silveira, D. D. Fu, B. H. Cha, C. Akman, Y. Hu, and G. L. Holmes
Beneficial effects of enriched environment following status epilepticus in immature rats
Neurology, November 12, 2002; 59(9): 1356 - 1364.
[Abstract] [Full Text] [PDF]

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 Proc. Natl. Acad. Sci. USAHome page
K. Jin, Y. Zhu, Y. Sun, X. O. Mao, L. Xie, and D. A. Greenberg
Vascular endothelial growth factor (VEGF) stimulates neurogenesis in vitro and in vivo
PNAS, September 3, 2002; 99(18): 11946 - 11950.
[Abstract] [Full Text] [PDF]

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 BrainHome page
M. C. Walker, H. S. White, and J. W. A. S. Sander
Disease modification in partial epilepsy
Brain, September 1, 2002; 125(9): 1937 - 1950.
[Abstract] [Full Text] [PDF]

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 NeurologyHome page
D. A. Rempe and T. A. Kent
Using bone marrow stromal cells for treatment of stroke
Neurology, August 27, 2002; 59(4): 486 - 486.
[Full Text] [PDF]

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 J. Neurosci.Home page
C. A. Haas, O. Dudeck, M. Kirsch, C. Huszka, G. Kann, S. Pollak, J. Zentner, and M. Frotscher
Role for Reelin in the Development of Granule Cell Dispersion in Temporal Lobe Epilepsy
J. Neurosci., July 15, 2002; 22(14): 5797 - 5802.
[Abstract] [Full Text] [PDF]

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 J. Neurosci.Home page
X. Zhang, S.-S. Cui, A. E. Wallace, D. K. Hannesson, L. C. Schmued, D. M. Saucier, W. G. Honer, and M. E. Corcoran
Relations between Brain Pathology and Temporal Lobe Epilepsy
J. Neurosci., July 15, 2002; 22(14): 6052 - 6061.
[Abstract] [Full Text] [PDF]

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 J. Neurosci.Home page
K. Jin, X. O. Mao, Y. Sun, L. Xie, L. Jin, E. Nishi, M. Klagsbrun, and D. A. Greenberg
Heparin-Binding Epidermal Growth Factor-Like Growth Factor: Hypoxia-Inducible Expression In Vitro and Stimulation of Neurogenesis In Vitro and In Vivo
J. Neurosci., July 1, 2002; 22(13): 5365 - 5373.
[Abstract] [Full Text] [PDF]

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 J. Neurosci.Home page
J. M. Parent, V. V. Valentin, and D. H. Lowenstein
Prolonged Seizures Increase Proliferating Neuroblasts in the Adult Rat Subventricular Zone-Olfactory Bulb Pathway
J. Neurosci., April 15, 2002; 22(8): 3174 - 3188.
[Abstract] [Full Text] [PDF]

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 NeuroscientistHome page
H. E. Scharfman
Book Review: Epilepsy as an Example of Neural Plasticity
Neuroscientist, April 1, 2002; 8(2): 154 - 173.
[Abstract] [PDF]

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 J. Physiol.Home page
R. Koyama, M. K. Yamada, N. Nishiyama, N. Matsuki, and Y. Ikegaya
Group II metabotropic glutamate receptor activation is required for normal hippocampal mossy fibre development in the rat
J. Physiol., February 15, 2002; 539(1): 157 - 162.
[Abstract] [Full Text] [PDF]

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 NeurologyHome page
R. S. Briellmann, R. M. Kalnins, S. F. Berkovic, and G. D. Jackson
Hippocampal pathology in refractory temporal lobe epilepsy: T2-weighted signal change reflects dentate gliosis
Neurology, January 22, 2002; 58(2): 265 - 271.
[Abstract] [Full Text] [PDF]

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 J. Neurosci.Home page
L. Vallieres, I. L. Campbell, F. H. Gage, and P. E. Sawchenko
Reduced Hippocampal Neurogenesis in Adult Transgenic Mice with Chronic Astrocytic Production of Interleukin-6
J. Neurosci., January 15, 2002; 22(2): 486 - 492.
[Abstract] [Full Text] [PDF]

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 J. Physiol.Home page
Z. Mtchedlishvili, E. H Bertram, and J. Kapur
Diminished allopregnanolone enhancement of GABAA receptor currents in a rat model of chronic temporal lobe epilepsy
J. Physiol., December 1, 2001; 537(2): 453 - 465.
[Abstract] [Full Text] [PDF]

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 NeurologyHome page
M. P. Jacobs, G. D. Fischbach, M. R. Davis, M. A. Dichter, R. Dingledine, D. H. Lowenstein, M. J. Morrell, J. L. Noebels, M. A. Rogawski, S. S. Spencer, et al.
Future directions for epilepsy research
Neurology, November 13, 2001; 57(9): 1536 - 1542.
[Abstract] [Full Text] [PDF]

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 J. Neurosci.Home page
B. Seri, J. M. Garcia-Verdugo, B. S. McEwen, and A. Alvarez-Buylla
Astrocytes Give Rise to New Neurons in the Adult Mammalian Hippocampus
J. Neurosci., September 15, 2001; 21(18): 7153 - 7160.
[Abstract] [Full Text] [PDF]

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 Proc. Natl. Acad. Sci. USAHome page
E. Gould, N. Vail, M. Wagers, and C. G. Gross
Adult-generated hippocampal and neocortical neurons in macaques have a transient existence
PNAS, August 23, 2001; (2001) 181354698.
[Abstract] [Full Text] [PDF]

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 J. Neurosci.Home page
S. Mizuhashi, N. Nishiyama, N. Matsuki, and Y. Ikegaya
Cyclic Nucleotide-Mediated Regulation of Hippocampal Mossy Fiber Development: A Target-Specific Guidance
J. Neurosci., August 15, 2001; 21(16): 6181 - 6194.
[Abstract] [Full Text] [PDF]

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 J. Neurosci.Home page
J.-Z. Chuang, T. A. Milner, and C.-H. Sung
Subunit Heterogeneity of Cytoplasmic Dynein: Differential Expression of 14 kDa Dynein Light Chains in Rat Hippocampus
J. Neurosci., August 1, 2001; 21(15): 5501 - 5512.
[Abstract] [Full Text] [PDF]

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 StrokeHome page
Y. Yagita, K. Kitagawa, T. Ohtsuki, K.-i. Takasawa, T. Miyata, H. Okano, M. Hori, and M. Matsumoto
Neurogenesis by Progenitor Cells in the Ischemic Adult Rat Hippocampus
Stroke, August 1, 2001; 32(8): 1890 - 1896.
[Abstract] [Full Text] [PDF]

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 J. Neurophysiol.Home page
J. S. Snyder, N. Kee, and J. M. Wojtowicz
Effects of Adult Neurogenesis on Synaptic Plasticity in the Rat Dentate Gyrus
J Neurophysiol, June 1, 2001; 85(6): 2423 - 2431.
[Abstract] [Full Text] [PDF]

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 StrokeHome page
W. Jiang, W. Gu, T. Brannstrom, R. Rosqvist, and P. Wester
Cortical Neurogenesis in Adult Rats After Transient Middle Cerebral Artery Occlusion
Stroke, May 1, 2001; 32(5): 1201 - 1207.
[Abstract] [Full Text] [PDF]

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 Proc. Natl. Acad. Sci. USAHome page
K. Jin, M. Minami, J. Q. Lan, X. O. Mao, S. Batteur, R. P. Simon, and D. A. Greenberg
Neurogenesis in dentate subgranular zone and rostral subventricular zone after focal cerebral ischemia in the rat
PNAS, April 10, 2001; 98(8): 4710 - 4715.
[Abstract] [Full Text] [PDF]

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 J. Neurosci.Home page
B. K. McCabe, D. C. Silveira, M. R. Cilio, B. H. Cha, X. Liu, Y. Sogawa, and G. L. Holmes
Reduced Neurogenesis after Neonatal Seizures
J. Neurosci., March 15, 2001; 21(6): 2094 - 2103.
[Abstract] [Full Text] [PDF]

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 J. Neurosci.Home page
H. J. Wenzel, C. A. Robbins, L.-H. Tsai, and P. A. Schwartzkroin
Abnormal Morphological and Functional Organization of the Hippocampus in a p35 Mutant Model of Cortical Dysplasia Associated with Spontaneous Seizures
J. Neurosci., February 1, 2001; 21(3): 983 - 998.
[Abstract] [Full Text] [PDF]

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 J. Neurosci.Home page
J. E. Malberg, A. J. Eisch, E. J. Nestler, and R. S. Duman
Chronic Antidepressant Treatment Increases Neurogenesis in Adult Rat Hippocampus
J. Neurosci., December 15, 2000; 20(24): 9104 - 9110.
[Abstract] [Full Text] [PDF]

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 NeurologyHome page
R. S. Briellmann, S. F. Berkovic, and G. D. Jackson
Men may be more vulnerable to seizure-associated brain damage
Neurology, November 28, 2000; 55(10): 1479 - 1485.
[Abstract] [Full Text] [PDF]

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 NeuroscientistHome page
J. Liu, R. Bernabeu, A. Lu, and F. R. Sharp
Neurogenesis and Gliogenesis in the Postischemic Brain
Neuroscientist, October 1, 2000; 6(5): 362 - 370.
[Abstract] [PDF]


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