Neural circuit mechanisms of posttraumatic epilepsy

Frontiers in Cellular Neuroscience

Volumn , Issue MAY, 2013, Pages

  Hunt, Robert F ^a   Boychuk, Jeffery A ^b   Smith, Bret N ^b  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF KENTUCKY   (United States)

Author keywords

Epilepsy; Epileptogenesis; Neuroinflammation; Pilocarpine; Seizures; Synapse; Traumatic brain injury

Indexed keywords

ALBUMIN; CX3C CHEMOKINE; GLUTAMIC ACID; INTERCELLULAR ADHESION MOLECULE 1; INTERLEUKIN 1BETA; INTERLEUKIN 6; ION CHANNEL; MACROPHAGE INFLAMMATORY PROTEIN 1ALPHA; MACROPHAGE INFLAMMATORY PROTEIN 1BETA; MONOCYTE CHEMOTACTIC PROTEIN 1; PROSTAGLANDIN E RECEPTOR 2; TRANSFORMING GROWTH FACTOR BETA; TUMOR NECROSIS FACTOR ALPHA; VASCULAR CELL ADHESION MOLECULE 1;

BLOOD BRAIN BARRIER; BRAIN REGION; CALCIUM TRANSPORT; CELL DEATH; DENTATE GYRUS; ENCEPHALITIS; EPILEPTOGENESIS; EXCITOTOXICITY; HIPPOCAMPUS; HUMAN; IMMUNE RESPONSE; INNATE IMMUNITY; NEOCORTEX; NERVE CELL LESION; NERVE CELL PLASTICITY; NEUROTRANSMISSION; NEUROTRANSMITTER RELEASE; NONHUMAN; PROTEIN EXPRESSION; REVIEW; SYNAPTIC INHIBITION; TEMPORAL LOBE EPILEPSY; TRAUMATIC EPILEPSY;

EID: 84878310507     PISSN: 16625102     EISSN: None     Source Type: Journal    
DOI: 10.3389/fncel.2013.00089     Document Type: Review

References (170)

1. Abbott, N. J. (2000). Inflammatory mediators and modulation of blood-brain barrier permeability. Cell Mol. Neurobiol. 20, 131-147.
2. Agrawal, A., Timothy, J., Pandit, L., and Manju, M. (2006). Post-traumatic epilepsy: an overview. Clin Neurol. Neurosurg. 108, 433-439.
3. Akassoglou, K., Probert, L., Kontogeorgos, G., and Kollias, G. (1997). Astrocyte-specific but not neuronspecific transmembrane TNF triggers inflammation and degeneration in the central nervous system of transgenic mice. J. Immunol. 158, 438-445.
4. Annegers, J. F., Hauser, A., Coan, S. P., and Rocca, W. P. (1998). A population-based study of seizures and traumatic brain injuries. N. Eng. J. Med. 338, 20-24.
5. Asikainen, I., Kaste, M., and Sarna, S. (1999). Early and late posttraumatic seizures in traumatic brain injury rehabilitation patients: brain injury factors causing late seizures and influence of seizures on longterm outcome. Epilepsia 40, 584-589.
6. Babb, T. L., Kupfer, W. R., Pretorius, J. K., Crandall, P. H., and Levesque, M. F. (1991). Synaptic reorganization by mossy fibers in human epileptic fascia dentata. Neuroscience 42, 351-363.
7. Ben-Ari, Y. (1985). Limbic seizure and brain damage produced by kainic acid: mechanisms and relevance to human temporal lobe epilepsy. Neuroscience 14, 375-403.
8. Bezbradica, J. S., and Medzhitov, R. (2009). Integration of cytokine and heterologous receptor signaling pathways. Nat. Immunol. 10, 333-339.
9. Bolkvadze, T., Pitkanen, A. (2012). Development of post-traumatic epilepsy after controlled cortical impact and lateral fluid-percussion-induced brain injury in the mouse. J. Neurotrauma. 29, 789-812
10. Buckmaster, P. S., and Dudek, F.E. (1997a). Network properties of the dentate gyrus in epileptic rats with hilar neuron loss and granule cell axon reorganization. J. Neurophysiol. 77, 2685-2596.
11. Buckmaster, P. S., and Dudek, F.E. (1997b). Neuron loss, granule cell axon reorganization, and functional changes in the dentate gyrus of epileptic kaintate treated rats. J. Comp. Neurol. 385, 385-404.
12. Buckmaster, P.S., and Dudek, F. E. (1999). In vivo intracellular analysis of granule cell axon reorganization in epileptic rats. J. Neurophysiol. 81, 712-721.
13. Buckmaster, P. S., Yamawaki, R., and Zhang, G. F. (2002). Axon arbors and synaptic connections of a vulnerable population of interneurons in the dentate gyrus in vivo. J. comp. Neurol. 445, 360-373.
14. Burns, B. D. (1951). Some properties of isolated cerebral cortex in the unanesthetized cat. J. Physiol. 112, 156-175.
15. Cacheaux, L. P., Ivens, S., David, Y., Lakhter, A. J., Bar-Klein, G., Shapira, M., Heinemann, U., Friedman, A., and Kaufer, D. (2009). Transcriptome profiling reveals TGF-beta signaling involvement in epileptogenesis. J. Neurosci. 29, 8927-8935.
16. Campbell, I. L., Abraham, C. R., Masliah, E., Kemper, P., Inglis, J. D., Oldstone, M. B., and Mucke, L. (1993). Neurologic disease induced in transgenic mice by cerebral overexpression of interleukin 6. Proc. Natl. Acad. Sci. U.S.A. 90, 10061-10065.
17. Carpio, A., Escobar, A., and Hauser, W. A. (1998). Cysticercosis and epilepsy: a critical review. Epilepsia 39, 1-25-1040.
18. Caveness, W. F., Meirowski, A. M., Rish, B. L., Mohr, J. P., Kistler, J. P., Dillon, J. D., and Weiss, G. H. (1979). The nature of posttraumatic epilepsy. J. Neurosurg. 50, 545-553.
19. Chagnac-Amitai, Y., and Connors, B. W. (1989). Horizontal spread of synchronized activity in neocortex and its control by GABA-mediated inhibition. J. Neurophysiol. 61, 747-58.
20. Choi, J., and Koh, S. (2008). Role of brain inflammation in epileptogenesis. Yonsei. Med. J. 49, 1-18.
21. Chraszcz, M., Venkatesan, C., Dragisic, T., Watterson, D. M., and Wainwright, M. S. (2010). Minozac treatment prevents increased seizure susceptibility in a mouse "two-hit" model of closed skull traumatic brain injury and electroconvulsive shock-induced seizures. J. Neurotrauma 27, 1283-95.
22. Cornford, E. M., and Oldendorf, W. H. (1986). Epilepsy and the blood-brain barrier. Adv. Neurol. 44, 787-812.
23. Crespel, A., Coubes, P., Rousset, M. C., Brana, C., Rougier, A., Rondouin, G., Bockaert, J., Baldy-Moulinier, M., and Lerner-Natoli, M. (2002). Inflammatory reactions in human medial temporal lobe epilepsy with hippocampal sclerosis. Brain Res. 952,159-169.
24. Cronin, J, and Dudek, F. E. (1988). Chronic seizures and collateral sprouting of dentate mossy fibers after kainic acid treatment in rats. Brain Res. 474, 181-184.
25. Cronin, J., Obenaus, A., Houser, C. R., and Dudek, F. E. (1992). Electrophysiology of dentate granule cells after kainite-induced synaptic reorganization of the mossy fibers. Brain Res. 573, 305-310.
26. Curia, G., Levitt, M., Fender, S.J., Miller, W.J., Ojemann, J., D'Ambrosio, R (2011). Impact of injury location and severity on posttraumatic epilepsy in the rat: role of frontal neocortex. Cerebral Cortex 21, 1574-1592
27. D'Alessandro, R., Tinuper, P., Ferrara, R., Cortelli, P., Pazzaglia, P., Sabattini, L., Frank, G., and Lugaresi, E. (1982). CT scan prediction of late post-traumatic epilepsy. J. Neurol. Neurosurg. Psychiatry 45, 1153-1155.
28. D'Ambrosio, R., Fairbanks, J. P., Fender, J. S., Born, D. E., Doyle, D. L., and Miller, J. W. (2004). Posttraumatic epilepsy following fluid percussion injury in the rat. Brain 127, 304-314.
29. D'Ambrosio, R., Fender, J. S., Fairbanks, J. P., Simon, E. A., Born, D. E., Doyle, D. L., and Miller, J. W. (2005). Progression from frontal-parietal to mesial-temporal epilepsy after fluid percussion injury in the rat. Brain 128, 174-188.
30. D'Ambrosio, R., Hakimian, S., Stewart, T., Verley, D. R., Fender, J. S., Eastman, C. L., Sheerin, A. D., Gupta, P., Diaz-Arrastia, R., Ojemann, J., and Miller, J. W. (2009). Functional definition of seizure provides new insight into post-traumatic epileptogenesis. Brain 132, 2805-2821.
31. Dardiotis, E., Karanikas, V., Paterakis, K., Fountas, K., and Hadjigeorgiou, G. M. (2012). "Traumatic brain injury and inflammation: emerging role of innate and adaptive immunity" in Brain Injury - Pathogenesis, Monitoring, Recovery and Management, ed. A Agrawal (Rijeka, Croatia: InTech), 23-38. Available from: http://www.intechopen.com/books/brain-injury-pathogenesis-monitoring-recovery-and-management/traumatic-brain-injury-and-inflammation-emerging-role-of-innate-and-adaptive-immunity.
32. David, Y., Cacheaux, L. P., Ivens, S., Lapilover, E., Heinemann, U., Kaufer, D., and Friedman, A. (2009). Astrocytic dysfunction in epileptogenesis: consequence of altered potassium and glutamate homeostasis? J. Neurosci. 29, 10588-10599.
33. Dedeurwaerdere, S., Friedman, A., Fabene, P. F., Mazarati, A., Murashima, Y. L., Vezzani, A., and Baram, T. Z. (2012). Finding a better drug for epilepsy: anti-inflammatory targets. Epilepsia 53, 1113-1118.
34. de Lanerolle, N. C., Kim, J. H., Robbins, R. J., and Spencer, D. D. (1989). Hippocampal interneuron loss and plasticity in human temporal lobe epilepsy. Brain Res. 495, 387-395.
35. Diaz-Arrastia, R., Agostini, M. A., Frol, A. B., Mickey, B., Fleckenstein, J., Bigio, E., and Van Ness, P. C. (2000). Neurophysiologic and neuroradiologic features of intractable epilepsy after traumatic brain injury in adults. Arch. Neurol. 57, 1611-1616.
36. Dichter, M. A. (2009). Posttraumatic epilepsy: the challenge of translating discoveries in the laboratory to pathways to a cure. Epilepsia 50, 41-45.
37. Dixon, C. E., Clifton, G. L., Lighthall, J. W., Yaghmai, A. A., and Hayes, L. (1991). A controlled cortical impact model of traumatic brain injury in the rat. J. Neurosci. Methods 3, 253-262.
38. Dixon, C. E., and Kline, A. E. (2009). Controlled cortical impact injury model. In: Animal models of acute neurological injuries (Chen J, Xu ZC, Xu XM, Zhang JH, eds.). Totowa, NJ: Humana Press. pp. 385-391.
39. Dudek, F. E., and Spitz, M. (1997). Hypothetical mechanisms for the cellular and neurophysiologic basis of secondary epileptogenesis: proposed role of synaptic reorganization. J. Clin. Neurophysiol. 14, 90-101.
40. Dudek, F. E., and Sutula, T. P. (2007). Epileptogenesis in the dentate gyrus: a critical perspective. Prog Brain Res. 163, 755-773.
41. Dunn, A. J. (2006). Effects of cytokines and infections on brain neurochemistry. Clin. Neurosci. Res. 6, 52-68.
42. Echegoyen, J., Armstrong, C., Morgan, R. J., and Soltesz, I. (2009). Single application of a CB1 receptor antagonist rapidly following head injury prevents long-term hyperexcitability in a rat model. Epilepsy Res. 85, 123-127.
43. Englander, J. E., Bushnik, T., Duong, T. T., Cifu, D. X., Zafonte, R., Wright, J., Hughes, R., and Bergman, W. (2003). Analyzing the risk factors for late posttraumatic seizures: a prospective, multicenter investigation. Arch. Phys. Med. Rehabil. 84, 365-373.
44. Fabene, P. F., Mora G. N., Martinello, M., Rossi, B., Merigo, F., Ottoboni, L., Bach, S., Angiari, S., Benati, D., Chakir, A., Zanetti, L., Schio, F., Osculati, A., Marzola, P., Nicolato, E., Homeister, J. W., Xia, L., Lowe, J. B., McEver, R. P., Osculati, F., Sbarbati, A., Butcher, E. C., and Constantin, G. (2008). A role for leukocyte-endothelial adhesion mechanisms in epilepsy. Nat. Med. 14, 1377-1383.
45. A receptors. Nat. Rev. Neurosci. 6, 215-229.
46. Fattori, E., Lazzaro, D., Musiani, P., Modesti, A., Alonzi, T., Ciliberto, G. (1995). IL-6 expression in neurons of transgenic mice causes reactive astrocytosis and increase in ramified microglial cells but no neuronal damage. Eur. J. Neurosci. 7, 2441-2449.
47. Faul, M., Xu, L., Wald, M. M., and Coronado, V. G. (2010). Traumatic brain injury in the United States: emergency department visits, hospitalizations, and deaths. Atlanta (GA): Centers for Disease Control and Prevention, National Center for Injury Prevention and Control.
48. Ferrari, C. C., Depino, A. M., Prada, F., Muraro, N., Campbell, S., Podhajcer, O., Perry, V. H., Anthony, D. C., and Pitossi, F.J. (2004). Reversible demyelination, blood-brain barrier breakdown, and pronounced neutrophil recruitment induced by chronic IL-1 expression in the brain. Am. J. Pathol. 165, 1827-1837.
49. Frey, L. C. (2003). Epidemiology of posttraumatic epilepsy: a critical review. Epilepsia 44: S11-S17.
50. Glykys, J., and Mody, I. (2007). The main source of ambient GABA responsible for tonic inhibition in the mouse hippocampus. J Physiol. 582, 1163-1178.
51. Golarai, G., Greenwood, A. C., Feeney, D. M., and Connor, J. A. (2001). Physiological and structural evidence for hippocampal involvement in persistent seizure susceptibility after traumatic brain injury. J. Neurosci. 21, 8523-8537.
52. Grady, M. S., Charleston, J. S., Maris, D., Witgen, B. M., and Lifshitz, J. (2003). Neuronal and glial cell number in the hippocampus after experimental traumatic brain injury: analysis by stereological estimation. J Neurotrauma 20, 929-941.
53. nd ed (Evans RW, ed.) New York. Oxford University Press. pp.45-94.
54. Gupta, A., Elgammal, F. S., Proddutur, A., Shah, S., and Santhakumar, V. (2012). Decrease in tonic inhibition contributes to increase in dentate semilunar granule cell excitability after brain injury. J Neurosci. 32, 2523-37.
55. Gurkoff, G. G., Giza, C. C., Shin, D., Auvin, S., Sankar, R., and Hovda, D. A. (2009). Acute neuroprotection to pilocarpine-induced seizures is not sustained after traumatic brain injury in the developing rat. Neuroscience 164, 862-876.
56. Halabisky, B., Parada, I., Buckmaster, P. S., and Prince, D. A. (2010). Excitatory input onto hilar somatostatin interneurons is increased in a chronic model of epilepsy. J. Neurophysiol. 104, 2214-2223.
57. Hall, E. D., Sullivan, P. G., Gibson, T. R., Pavel, K. M., Thompson, B. M., and Scheff, S. W. (2005). Spatial and temporal characteristics of neurodegeneration after controlled cortical impact in mice: more than a focal brain injury. J. Neurotrauma. 22, 252-265.
58. Hall, E. D., Bryant, Y. D., Cho, W., Sullivan, P. G. (2008). Evolution of post-traumatic neurodegeneration after controlled cortical impact traumatic brain injury in mice and rats as assessed by the de Olmos silver and fluorojade staining methods. J. Neurotrauma 25, 235-247.
59. Haltiner, A. M., Temkin, N. R., and Dikmen, S. S. (1997). Risk of seizure recurrence after the first late posttraumatic seizure. Arch. Phys. Med. Rehabil. 78, 835-840.
60. Hama, T., Kushima, Y., Miyamoto, M., Kubota, M., Takei, N., and Hatanaka, H. (1991). Interleukin-6 improves the survival of mesencephalic catecholaminergic and septal cholinergic neurons from postnatal, two-week-old rats in cultures. Neuroscience 40, 445-452.
61. Hanisch, U. K. (2002). Microglia as a source and target of cytokines. Glia 40, 140-155.
62. Hauser, W. A., Annegers, J. F., and Kurland, L. T. (1991). Prevalence of epilepsy in Rochester, Minnesota: 1940-1980. Epilepsia 32, 429-445.
63. Hauser, W. A., and Hesdorffer, D. C. (1990). Epilepsy: frequency, causes, and consequences. New York: Demos.
64. Hellier, J. L., Patrylo, P. R., Buckmaster, P. S., and Dudek, F. E. (1998). Recurrent spontaneous motor seizures after repeated low-dose systemic treatment with kainate: assessment of a rat model of temporal lobe epilepsy. Epilepsy Res. 31, 73-84.
65. Herman, S. T. (2002). Epilepsy after brain insult: targeting epileptogenesis. Neurology 59, S21-S26.
66. Houser, C. R., Miyashiro, J. E., Swartz, B. E., Walsh, G. O., Rich, J. R., and Delgado-Escueta, A. V. (1990). Altered patterns of dynorphin immunoreactivity suggest mossy fiber reorganization in human hippocampal epilepsy. J. Neurosci. 10, 267-282.
67. Huber, J. D., Egleton, R. D., and Davis, T. P. (2001). Molecular physiology and pathophysiology of tight junctions in the blood-brain barrier. Trends Neurosci. 24, 719-725.
68. Hudak, A. M., Trivedi, K., Harper, C. R., Booker, K., Caesar, R. R., Agostini, M., Van Ness, P. C., and Diaz-Arrastia, R. (2004). Evaluation of seizure-like episodes in survivors of moderate and severe traumatic brain injury. J. Head Trauma Rehabil. 19, 290-295.
69. Hunt, R. F., Haselhorst, L. A., Schoch, K. M., Bach, E. C., Rios-Pilier, J., Scheff, S. W., Saatman, K. E., and Smith, B. N. (2012). Posttraumatic mossy fiber sprouting is related to the degree of cortical damage in three mouse strains. Epilepsy Res. 99, 167-70.
70. Hunt, R. F., Scheff, S. W., and Smith, B. N. (2009). Posttraumatic epilepsy after controlled cortical impact injury in mice. Exp. Neurol. 215, 243-252.
71. Hunt, R. F., Scheff, S. W., and Smith, B. N. (2010). Regionally localized recurrent excitation in the dentate gyrus of a cortical contusion model of posttraumatic epilepsy. J. Neurophysiol. 103, 1490-1500.
72. Hunt, R. F., Scheff, S. W., and Smith, B. N. (2011). Synaptic reorganization of inhibitory hilar interneuron circuitry after traumatic brain injury in mice. J. Neurosci. 31, 6880-6890.
73. Ivens, S., Kaufer, D., Flores, L. P., Bechmann, I., Zumsteg, D., Tomkins, O., Seiffert E., Heinemann, U., and Friedman, A. (2007). TGF-beta receptor-mediated albumin uptake into astrocytes is involved in neocortical epileptogenesis. Brain 130, 535-547.
74. Jiang, J., Ganesh, T., Du, Y., Quan, Y., Serrano, G., Qui, M., Speigel, I., Rojas, A., Lelutiu, N., and Dingledine, R. (2012). Small molecule antagonist reveals seizure-induced mediation of neuronal injury by prostaglandin E2 receptor subtype EP2. Proc. Natl. Acad. Sci. U.S.A. 109, 3149-3154.
75. Jiang, J., Quan, Y., Ganesh, T., Pouliot, W. A., Dudek, F. E., and Dingledine, R. (2013). Inhibition of the prostaglandin receptor EP2 following status epilepticus reduces delayed mortality and brain inflammation. Proc. Natl. Acad. Sci. U.S.A. 110, 3591-3596.
76. Kalueff, A. V., Lehtimaki, K. A., Ylinen, A., Honkaniemi, J., and Peltola, J. (2004). Intranasal administration of human IL-6 increases the severity of chemically induced seizures in rats. Neurosci. Lett. 365, 106-110.
77. Kasantikul, V., Brown, W. J., Oldendorf, W. H., and Crandall, P. C. (1983). Ultrastructural parameters of limbic microvasculature in human psychomotor epilepsy. Clin. Neuropathol. 2, 171-178.
78. Kharatishvili, I., Immonen, R., Gröhn, O., and Pitkänen, A. (2007). Quantitative diffusion MRI of hippocampus as a surrogate marker for post-traumatic epileptogenesis. Brain 130, 3155-3158.
79. Kharatishvili, I., Nissinen, J. P., McIntosh, T. K., and Pitkänen, A. (2006). A model of posttraumatic epilepsy induced by lateral fluid-percussion brain injury in rats. Neuroscience 140, 685-697.
80. Kim, S. Y., Buckwalter, M., Soreq, H., Vezzani, A., and Kaufer, D. (2012). Blood-brain barrier dysfunction-induced inflammatory signaling in brain pathology and epileptogenesis. Epilepsia 53, 37-44.
81. Kochanek, P. M., Vagni, V. A., Janesko, K. L., Washington, C. B., Crumrine, P. K., Garman, R. H., Jenkins, L. W., Clark, R. S., Homanics, G. E., Dixon, C. E., Schnermann, J., and Jackson, E. K. (2006). Adenosine A1 receptor knock-out mice develop lethal status epilepticus after experimental traumatic brain injury. J Cerebral Blood Flow Met. 26, 565-575.
82. Korn, A., Golan, H., Melamed, I., Pascual-Marqui, R., and Friedman, A. (2005). Focal cortical dysfunction and blood-brain barrier disruption in patients with Postconcussion syndrome. J. Clin. Neurophysiol. 22, 1-9.
83. Kotila, M., and Waltimo, O. (2005). Epilepsy and stroke. Epilepsia 33, 495-498.
84. Laurer, H., Lenzlinger, P. M., and McIntosh, T. K. (2000). Modles of traumatic brain injury. Eur. J. Trauma 26, 95-100.
85. Librizzi, L., Noè, F., Vezzani, A., de Curtis, M., and Ravizza, T. (2012). Seizure-induced brain-borne inflammation sustains seizure recurrence and blood-brain barrier damage. Ann. Neurol. 72, 82-90.
86. Lifshitz, J. (2009). Fluid percussion injury model, Ch 32. In: Animal models of acute neurological injuries (Chen J, Xu ZC, Xu XM, Zhang JH, eds.). Totowa, NJ: Humana Press. pp. 369-384.
87. Lighthall, J. W. (1988). Controlled cortical impact: a new experimental brain injury model. J Neurotrauma 5, 1-15.
88. Lothman, E. W., Bertram III E. H., Stringer, J. L. (1991). Functional anatomy of hippocampal seizures. Prog. Neurobiol. 37, 1-82.
89. Lowenstein, D. H., Thomas, M. J., Smith, D. H., McIntosh, T. K. (1992). Selective vulnerability of dentate hilar neurons following traumatic brain injury: a potential mechanistic link between head trauma and disorders of the hippocampus. J. Neurosci. 12, 4846-4853.
90. Lu, X. C., Hartings, J. A., Si, Y., Balbir, A., Cao, Y., and Tortella, F. C. (2011). Electrocortical pathology in a rat model of penetrating ballistic-like brain injury. J. Neurotrauma. 28, 71-83.
91. Lucas, S. M., Rothwell, N. J., and Gibson, R. M. (2006). The role of inflammation in CNS injury and disease. Br. J. Pharmacol. 147, 232-240.
92. Lynch, M., and Sutula, T. (2000). Recurrent excitatory connectivity in the dentate gyrus of kindled and kainic acid-treated rats. J. Neurophysiol. 83, 693-704.
93. Majores, M., Eils, J., Wiestler, O. D., and Becker, A. J. (2004). Molecular profiling of temporal lobe epilepsy: comparison of data from human tissue samples and animal models. Epilepsy Res. 60, 173-178.
94. Marchi, N., Angelov, L., Masaryk, T., Fazio, V., Granata, T., Hernandez, N., Hallene, K., Diglaw, T., Franic, L., Najm, I., and Janigro, D. (2007). Seizure promoting effect of blood-brain barrier disruption. Epilepsia 48, 732-742.
95. Marmarou, C. R., Prieto, R., Taya, K., Young, H. F., and Marmarou A (2009). Marmarou weight drop injury model, Ch 34. In: Animal models of acute neurological injuries (Chen J, Xu ZC, Xu XM, Zhang JH, eds.). Totowa, NJ: Humana Press.
96. McCormick, D. A., and Contreras, D. (2001). On the cellular and network bases of epileptic seizures. Annu. Rev. Physiol. 63, 815-846.
97. Mendelow, D. A., Crawford, P. J. (1997). Primary and secondary brain injury. In: Head Injury. (Reilly P, Bullock R, eds.). London: Chapman & Hall. pp 71-88.
98. Miller, L. G., Galpern, W. R., Dunlap, K., Dinarello, C.A., and Turner, T.J. (1991). Interleukin-1 augments gamma-aminobutyric acid A receptor function in brain. Mol. Pharmacol. 39, 105-108.
99. Morganti-Kossmann, M.C., Rancan, M., Otto, V. I., Stahel, P. F., and Kossmann, T. (2001). Role of cerebral inflammation after traumatic brain injury: a revisited concept. Shock 16, 165-177.
100. A receptor-mediated tonic inhibition in dentate granule cells after traumatic brain injury. Neurobiol. Dis. 38, 464-475.
101. Nadler, J. V. (2003). The recurrent mossy fiber pathway of the epileptic brain. Neurochem. Res. 28, 1649-1658.
102. Nadler, J.V., Perry, B.W., Cotman, C.W. (1980). Selective reinnervation of hippocampal area CA1 and the fascia dentata after destruction of CA3-CA4 afferents with kainic acid. Brain Res. 182, 1-9.
103. Nelson, K. B., and Ellenberg, J. H. (1976). Predictors of epilepsy in children who have experienced febrile seizures. N. Engl. J. Med. 295, 1029-1033.
104. Nilsson, P., Ronne-Engstrom, E., Flink, R., Ungersted, U., Carlson, H., and Hillered, L. (2004). Epileptic seizure activity in the acute phase following cortical impact trauma in rat. Brain Res. 637, 227-232.
105. Norris, C. M., and Scheff, S. W. (2009). Recovery of Afferent Function and Synaptic Strength in Hippocampal CA1 following Traumatic Brain Injury. J Neurotrauma. 26, 2269-2278.
106. Pacifici, R., Paris, L., Di Carlo, S., Bacosi, A., Pichini, S., and Zuccaro, P. (1995). Cytokine production in blood mononuclear cells from epileptic patients. Epilepsia 36, 384-387.
107. Patrylo, P. R., and Dudek, F. E. (1998). Physiological unmasking of new glutamatergic pathways in the dentate gyrus of hippocampal slices from kainate-induced epileptic rats. J. Neurophysiol. 79, 418-429.
108. Pavlov, I., Huusko, N., Nissinen, J., Sperk, G., Pitkänen, A., and Walker, M. C. (2009). Phasic but not tonic inhibition is decreased in dentate gyrus granule cells in fluid-percussion brain injury model of posttraumatic epilepsy in rats. Neuroscience 194, 208-219.
109. Pavlovsky, L., Seiffert, E., Heinemann, U., Korn, A., Golan, H., and Friedman, A. (2005). Persistent BBB disruption may underlie alpha interferon-induced seizures. J. Neurol. 252, 42-46.
110. Pitkanen, A. and McIntosh, T. K. (2006). Animal models of posttraumatic epilepsy. J Neurotrauma. 23, 241-261.
111. Plata-Salamán, C. R., and Ffrench-Mullen, J.M. (1992). Interleukin-1 beta depresses calcium currents in CA1 hippocampal neurons at pathophysiological concentrations. Brain Res. Bull. 29, 221-223.
112. th ed. Noebels JL, Avoli M, Rogawski MA, et al., eds. Bethesda (MD): National Center for Biotechnology Information, US (2012).
113. Prince, D. A., and Tseng, G. F. (1993). Epileptogenesis in chronically injured cortex: in vitro studies. J Neurophysiol. 69, 1276-1291.
114. Qiu, Z., Sweeney, D. D., Netzeband, J.G., and Gruol, D. L. (1998). Chronic interleukin-6 alters NMDA receptor-mediated membrane responses and enhances neurotoxicity in developing CNS neurons. J. Neurosci. 18, 10445-10456.
115. Quadbeck, G. and Helmchen, H. (1958). Proneness to convulsions & hemato-encephalic barrier permeability. Dtsch. Z. Nervenheilkd. 177, 295-308.
116. Racine, R. J. (1979). Modification of seizure activity by electrical stimulation: II. Motor seizures. Electrorencephalogr. Clin. Neurophysiol. 32, 281-294.
117. Raible, D. J., Frey, L. C., Cruz Del Angel, Y., Russek, S. J., and Brooks-Kayal, A. R. (2012). GABA(A) receptor regulation after experimental traumatic brain injury. J. Neurotrauma. 29, 2548-2554.
118. Ransohoff, R. M. (2002). Chemokines in neurological trauma models. Ann. N. Y. Acad. Sci. 961, 346-349.
119. Ravizza, T., and Vezzani, A. (2006). Status epilepticus induces time-dependent neuronal and astrocytic expression of interleukin-1 receptor type I in the rat limbic system. Neuroscience 137, 301-308.
120. Ravizza, T., Gagliardi, B., Noe, F., Boer, K., Aronica, E., and Vezzani, A. (2008). Innate and adaptive immunity during epileptogenesis and spontaneous seizures: evidence from experimental models and human temporal lobe epilepsy. Neurobiol. Dis. 29, 142-160.
121. Rovegno, M., Soto, P. A., Sáez, J. C., and von Bernhardi, R. (2011). Biological mechanisms involved in the spread of traumatic brain damage. Med. Intensiva. 36, 37-44.
122. Saatman, K. E., Feeco, K. J., Pape, R. L., and Raghupathi, R. (2006). Differential behavioral and histopathological responses to graded cortical impact injury in mice. J. Neurotrauma 23, 1241-1253.
123. Salazar, A. M., Jabbari, B., Vance, S. C., Grafman, J., Amin, D., Dillon, J. D. (1985). Epilepsy after penetrating head injury. I. Clinical correlates: a report of the Vietnam Head Injury Study. Neurology 35, 1406-1414.
124. Santhakumar, V., Bender, R., Frotscher, M., Ross, S. T., Hollrigel, G. S., Toth, Z., and Soltesz, I. (2000). Granule cell hyperexcitability in the early post-traumatic rat dentate gyrus: the 'irritable mossy cell' hypothesis. J. Physiol. 524, 117-134.
125. Santoshkumar, B., Chong, J. J., Blume, W. T., McLachlan, R. S., Young, G. B., Diosy, D. C., Burneo, J. G., Mirsattari, S. M. (2009). Prevelence of benign epileptiform variants. Clin. Neurophysiol. 120, 856-861.
126. Schäfers, M., and Sorkin, L. (2008). Effect of cytokines on neuronal excitability. Neurosci. Lett. 437, 188-193.
127. Scheff, S. W., Baldwin, S. A., Brown, R. W., and Kraemer, P. J. (1997). Morris water maze deficits in rats following traumatic brain injury: lateral controlled cortical impact. J. Neurotrauma 14, 615-627.
128. Scheff, S. W., Price, D. A., Hicks, R. R., Baldwin, S. A., Robinson, S., and Brackney, C. (2005). Synaptogenesis in the Hippocampal CA1 Field following Traumatic Brain Injury. J. Neurotrauma 22, 719-732.
129. Schevon, C. A., Weiss, S. A., McKhann, G. Jr., Goodman, R. R., Yuste, R., Emerson, R. G., and Trevelyan, A. J. (2012). Evidence of an inhibitory restraint of seizure activity in humans. Nat. Commun. 3, 1060.
130. Schmidt, O. I., Heyde, C.E., Ertel, W., and Stahel, P. F. (2005). Closed head injury-an inflammatory disease? Brain Res. Rev. 48, 388-399.
131. Seiffert, E., Dreier, J. P., Ivens, S., Bechmann, I., Tomkins, O., Heinemann, U., and Friedman, A. (2004). Lasting blood-brain barrier disruption induces epileptic focus in the rat somatosensory cortex. J. Neurosci. 24, 7829-7836.
132. Semah, F., Picot, M. C., Adam, C., Broglin, D., Arzimanoglou, A., Bazin, B., Cavalcanti, D., and Baulac, M. (1998). Is the underlying cause of epilepsy a major prognostic factor for recurrence? Neurology 51, 1256-1262.
133. Shibley, H., and Smith, B. N. (2002). Pilocarpine-induced status epilepticus results in mossy fiber sprouting and spontaneous seizures in C57BL/6 and CD-1 mice. Epilepsy Res. 49, 109-120.
134. Shlosberg, D., Benifla, M., Kaufer, D., and Friedman, A. (2010). Blood-brain barrier breakdown as a therapeutic target in traumatic brain injury. Nat. Rev. Neurol. 6, 393-403.
135. Sloviter, R. S. (1992). Possible functional consequences of synaptic reorganization in the dentate gyrus of kainite-treated rats. Neurosci. Lett. 137, 91-96.
136. Starnes, H. F. Jr., Pearce, M. K., Tewari, A., Yim, J. H., Zou, J.C., and Abrams, J. S. (1990). Anti-IL-6 monoclonal antibodies protect against lethal Escherichia coli infection and lethal tumor necrosis factoralpha challenge in mice. J. Immunol. 145, 4185-4191.
137. Statler, K. D., Swank, S., Abildskov, T., Bigler, E. D., and White HS (2008). Traumatic brain injury during development reduces minimal clonic seizure thresholds at maturity. Epilepsy Res. 80, 163-170.
138. Statler, K. D., Scheerlinck, P., Pouliot, W., Hamilton, M., White, H. S., and Dudek, F. E. (2009). A potential model of pediatric posttraumatic epilepsy. Epilepsy Res. 86, 221-223.
139. Sullivan, P. G., Thompson, M. B., and Scheff, S.W. (1999). Cyclosporin A attenuates acute mitochondrial dysfunction following traumatic brain injury. Exp. Neurol. 160, 226-234.
140. Sutula, T., Cascino, G., Cavazos, J., Parada, I., and Ramirez, L. (1989). Mossy fiber synaptic reorganization in the epileptic human temporal lobe. Ann. Neurol. 26, 321-330.
141. Sutula, T. P., Dudek, F. E. (2007). Unmasking recurrent excitation generated by mossy fiber sprouting in the epileptic dentate gyrus: an emergent property of a complex system. Prog. Brain Res. 163, 541-563.
142. Swartz, B. E., Houser, C. R., Tomiyasu, U., Walsh, G. O., DeSalles, A., Rich, J. R., and Delgado-Escueta, A. (2006). Hippocampal cell loss in posttraumatic human epilepsy. Epilepsia 47, 1373-1382.
143. Tauck, D. L., and Nadler, J. V. (1985). Evidence of functional mossy fiber sprouting in hippocampal formation of kainic acid-treated rats. J. Neurosci. 5, 1016-1022.
144. Teasdale, G. M., and Bannan, P. E. (1997). Neuroprotection in head injury. In: Head Injury. (Reilly P, Bullock R, eds.). London: Chapman & Hall. pp 423-438.
145. Temkin, N. R. (2009). Preventing and treating posttraumatic seizures: the human experience, Epilepsia 50, 10-13.
146. Tomkins, O., Kaufer, D., Korn, A., Shelef, I., Golan, H., Reichenthal, E., Soreq, H., and Friedman, A. (2001). Frequent blood-brain barrier disruption in the human cerebral cortex. Cell Mol. Neurobiol. 21, 675-691.
147. Tomkins, O., Shelef, I., Kaizerman, I., Eliushin, A., Afawi, Z., Misk, A., Gidon, M., Cohen, A., Zumteg, D., and Friedman, A. (2008). Blood-brain barrier disruption in post-traumatic epilepsy. J. Neurol. Neurosurg Psychiatry 79, 774-777.
148. Topolnik, L., Steriade, M., and Timofeev, I. (2003). Partial cortical deafferentation promotes development of paroxysmal activity. Cereb. Cortex 13, 883-893.
149. Toth, Z., Hollrigel, G. S., Gorcs, T., and Soltesz, I. (1997). Instantaneous perturbation of dentate interneuronal networks by a pressure wave-transient delivered to the neocrotex. J Neurosci. 17, 8106-8117.
150. Traub, R. D. and Wong, R. K. S. (1982). Cellular mechanisms of neuronal synchronization in epilepsy. Science 216, 745-747.
151. Trevelyan, A. J., Sussillo, D. & Yuste, R. M. (2007). Feedforward inhibition contributes to the control of the speed of epileptiform propagation. J. Neurosci. 27, 3383-3387.
152. Tyurin, V. A., Tyurina, Y. Y., Borisenko, G. G., Sokolova, T. V., Ritov, V. B., Quinn, P.J., Rose, M., Kochanek, P., Graham, S. H., and Kagan, V. E. (2000). Oxidative stress following traumatic brain injury in rats: quantitation of biomarkers and detection of free radical intermediates. J. Neurochem. 75, 2178-2189.
153. van Vliet, E. A., Araujo, S. D. C., Redeker, S., van Schaik, R., Aronica, E., and Gorter, J. A. (2007). Blood-brain barrier leakage may lead to progression of temporal lobe epilepsy. Brain 130, 521-534.
154. van Vliet, E. A., Forte, G., Holtman, L., den Burger, J. C., Sinjewel, A., de Vries, H. E., Aronica, E., Gorter, J. A. (2012). Inhibition of mammalian target of rapamycin reduces epileptogenesis and bloodbrain barrier leakage but not microglia activation. Epilepsia 53, 1254-1263.
155. Vezzani, A., Moneta, D., Conti, M., Richichi, C., Ravizza, T., De Luigi, A., De Simoni, M. G., Sperk, G., Andell-Jonsson, S., Lundkvist, J., Iverfeldt, K., and Bartfai, T. (2000). Powerful anticonvulsant action of IL-1 receptor antagonist on intracerebral injection and astrocytic overexpression in mice. Proc. Natl. Acad. Sci. U.S.A. 97, 11534-11539.
156. Vezzani, A., Moneta, D., Richichi, C., Aliprandi, M., Burrows, S. J., Ravizza, T., Perego, C., and De Simoni, M. G. (2002). Functional role of inflammatory cytokines and anti inflammatory molecules in seizures and epileptogenesis. Epilepsia 43, 30-35.
157. Vezzani, A., Balosso, S., and Ravizza, T. (2008). The role of cytokines in the pathophysiology of epilepsy. Brain Behav. Immun. 22, 797-803.
158. Vezzani, A., Aronica, E., Mazarati, A., and Pittman, Q. J. (2011). Epilepsy and brain inflammation. Exp. Neurol. [Epub ahead of print] doi:10.1016/j.expneurol.2011.09.033.
159. Vezzani, A., French, J., Bartfai, T., and Baram, T. Z. (2011). The role of inflammation in epilepsy. Nat. Rev. Neurol. 7, 31-40.
160. Werner, C., and Engelhard, K. (2007). Pathophysiology of traumatic brain injury. Br. J. Anaesth. 99, 4-9.
161. Winokur, R. S., Kubal, T., Liu, D., Davis, S. F., and Smith, B. N. (2004). Recurrent excitation in the dentate gyrus of a murine model of temporal lobe epilepsy. Epilepsy Res. 58, 93-105.
162. Wolburg, H., and Lippoldt, A. (2002). Tight junctions of the blood-brain barrier: development, composition and regulation. Vascul. Pharmacol. 38, 323-337.
163. Wuarin, J. P., and Dudek, F. E. (1996). Electrographic seizures and new recurrent excitatory circuits in the dentate gyrus of hippocampal slices from kainate-treated epileptic rat. J. Neurosci. 16, 4438-4448.
164. Wuarin JP, Dudek FE (2001). Excitatory synaptic input to granule cells increases with time after kainate treatment. J. Neurophysiol. 85, 1067-1077.
165. Yang, L., Afroz, S., Michelson, H. B., Goodman, J. H., Valsamis, H. A., and Ling, D. S. (2010). Spontaneous epileptiform activity in rat neocortex after controlled cortical impact injury. J. Neurotrauma. 27, 1541-1548
166. Yamada, M., and Hatanaka, H. (1994). Interleukin-6 protects cultured rat hippocampal neurons against glutamate-induced cell death. Brain Res. 643, 173-180.
167. Zalcman, S., Green-Johnson, J. M., Murray, L., Nance, D. M., Dyck, D., Anisman, A., and Greenberg, A. H. (1994). Cytokine-specific central monoamine alterations induced by interleukin-1, -2 and -6. Brain Res. 643, 40-49.
168. Zhang, N., and Houser, C. R. (1999). Ultrastructural localization of dynorphin in the dentate gyrus in human temporal lobe epilepsy: a study of reorganized mossy fiber synapses. J. Comp. Neurol. 405, 472-490.
169. Zhang, W., Yamawaki, R., Wen, X., Uhl, J., Diaz, J., Prince, D. A., and Buckmaster, P. S. (2009). Surviving hilar somatostatin interneurons enlarge, sprout axons, and form new synapses with granule cells in a mouse model of temporal lobe epilepsy. J. Neurosci. 29, 14247-14256.
170. Zlokovic, B.V. (2008). The blood-brain barrier in health and chronic neurodegenerative disorders. Neuron 57, 178-201.