Post-traumatic seizure susceptibility is attenuated by hypothermia therapy

European Journal of Neuroscience

Volumn 32, Issue 11, 2010, Pages 1912-1920

  Atkins, Coleen M ^a   Truettner, Jessie S ^a   Lotocki, George ^a   Sanchez Molano, Juliana ^a   Kang, Yuan ^a   Alonso, Ofelia F ^a   Sick, Thomas J ^a   Dietrich, W Dalton ^a   Bramlett, Helen M ^a,b  

^a UNIVERSITY OF MIAMI MILLER SCHOOL OF MEDICINE   (United States)

^b VETERANS AFFAIRS MEDICAL CENTER   (United States)

Author keywords

Epilepsy; Mossy fiber; Rat; Traumatic brain injury

Indexed keywords

PENTETRAZOLE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BRAIN INJURY; BRAIN TEMPERATURE; CONTROLLED STUDY; DENTATE GYRUS; EPILEPTOGENESIS; INDUCED HYPOTHERMIA; INFLAMMATION; MALE; MOSSY FIBER; NONHUMAN; PRIORITY JOURNAL; RAT; RISK FACTOR; SEIZURE; SEIZURE SUSCEPTIBILITY; SPRAGUE DAWLEY RAT; SURVIVAL; TRAUMATIC BRAIN INJURY; TRAUMATIC EPILEPSY;

ANIMALS; BODY TEMPERATURE; BRAIN INJURIES; EPILEPSY, POST-TRAUMATIC; HIPPOCAMPUS; HYPOTHERMIA, INDUCED; MALE; RATS; RATS, SPRAGUE-DAWLEY;

EID: 78649692875     PISSN: 0953816X     EISSN: 14609568     Source Type: Journal    
DOI: 10.1111/j.1460-9568.2010.07467.x     Document Type: Article

References (104)

1. Amaral, D.G. (1978) A Golgi study of cell types in the hilar region of the hippocampus in the rat. J. Comp. Neurol., 182, 851-914.
2. Andre, V., Pineau, N., Motte, J.E., Marescaux, C. & Nehlig, A. (1998) Mapping of neuronal networks underlying generalized seizures induced by increasing doses of pentylenetetrazol in the immature and adult rat: a c-Fos immunohistochemical study. Eur. J. Neurosci., 10, 2094-2106.
3. Annegers, J.F., Hauser, W.A., Coan, S.P. & Rocca, W.A. (1998) A population-based study of seizures after traumatic brain injuries. N. Engl. J. Med., 338, 20-24.
4. Atkins, C.M., Oliva, A.A.. Jr, Alonso, O.F., Chen, S., Bramlett, H.M., Hu, B.R. & Dietrich, W.D. (2007a) Hypothermia treatment potentiates ERK1/2 activation after traumatic brain injury. Eur. J. Neurosci., 26, 810-819.
5. Atkins, C.M., Oliva, A.A. Jr, Alonso, O.F., Pearse, D.D., Bramlett, H.M. & Dietrich, W.D. (2007b) Modulation of the cAMP signaling pathway after traumatic brain injury. Exp. Neurol., 208, 145-158.
6. Austin, J.E. & Buckmaster, P.S. (2004) Recurrent excitation of granule cells with basal dendrites and low interneuron density and inhibitory postsynaptic current frequency in the dentate gyrus of macaque monkeys. J. Comp. Neurol., 476, 205-218.
7. Babb, T.L., Kupfer, W.R., Pretorius, J.K., Crandall, P.H. & Levesque, M.F. (1991) Synaptic reorganization by mossy fibers in human epileptic fascia dentata. Neuroscience, 42, 351-363.
8. Barnes, G., Puranam, R.S., Luo, Y. & McNamara, J.O. (2003) Temporal specific patterns of semaphorin gene expression in rat brain after kainic acid-induced status epilepticus. Hippocampus, 13, 1-20.
9. Bautista, R.E. & Glen, E.T. (2009) Seizure severity is associated with quality of life independent of seizure frequency. Epilepsy Behav., 16, 325-329.
10. 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.
11. Bernard, S.A., Gray, T.W., Buist, M.D., Jones, B.M., Silvester, W., Gutteridge, G. & Smith, K. (2002) Treatment of comatose survivors of out-of-hospital cardiac arrest with induced hypothermia. N. Engl. J. Med., 346, 557-563.
12. Borges, K., Gearing, M., McDermott, D.L., Smith, A.B., Almonte, A.G., Wainer, B.H. & Dingledine, R. (2003) Neuronal and glial pathological changes during epileptogenesis in the mouse pilocarpine model. Exp. Neurol., 182, 21-34.
13. Bramlett, H.M., Green, E.J., Dietrich, W.D., Busto, R., Globus, M.Y. & Ginsberg, M.D. (1995) Posttraumatic brain hypothermia provides protection from sensorimotor and cognitive behavioral deficits. J. Neurotrauma, 12, 289-298.
14. Bramlett, H.M., Dietrich, W.D., Green, E.J. & Busto, R. (1997) Chronic histopathological consequences of fluid-percussion brain injury in rats: effects of post-traumatic hypothermia. Acta Neuropathol. (Berl.), 93, 190-199.
15. Braun, H., Schafer, K. & Hollt, V. (2002) βIII tubulin-expressing neurons reveal enhanced neurogenesis in hippocampal and cortical structures after a contusion trauma in rats. J. Neurotrauma, 19, 975-983.
16. Buckmaster, P.S. & Dudek, F.E. (1997) Neuron loss, granule cell axon reorganization, and functional changes in the dentate gyrus of epileptic kainate-treated rats. J. Comp. Neurol., 385, 385-404.
17. Buckmaster, P.S. & Jongen-Relo, A.L. (1999) Highly specific neuron loss preserves lateral inhibitory circuits in the dentate gyrus of kainate-induced epileptic rats. J. Neurosci., 19, 9519-9529.
18. Cavazos, J.E., Das, I. & Sutula, T.P. (1994) Neuronal loss induced in limbic pathways by kindling: evidence for induction of hippocampal sclerosis by repeated brief seizures. J. Neurosci., 14, 3106-3121.
19. Cilio, M.R., Sogawa, Y., Cha, B.H., Liu, X., Huang, L.T. & Holmes, G.L. (2003) Long-term effects of status epilepticus in the immature brain are specific for age and model. Epilepsia, 44, 518-528.
20. Clifton, G.L., Jiang, J.Y., Lyeth, B.G., Jenkins, L.W., Hamm, R.J. & Hayes, R.L. (1991) Marked protection by moderate hypothermia after experimental traumatic brain injury. J. Cereb. Blood Flow Metab., 11, 114-121.
21. Coulter, D.A., Rafiq, A., Shumate, M., Gong, Q.Z., DeLorenzo, R.J. & Lyeth, B.G. (1996) Brain injury-induced enhanced limbic epileptogenesis: anatomical and physiological parallels to an animal model of temporal lobe epilepsy. Epilepsy Res., 26, 81-91.
22. Cronin, J. & Dudek, F.E. (1988) Chronic seizures and collateral sprouting of dentate mossy fibers after kainic acid treatment in rats. Brain Res., 474, 181-184.
23. D'Ambrosio, R., Maris, D.O., Grady, M.S., Winn, H.R. & Janigro, D. (1999) Impaired K(+) homeostasis and altered electrophysiological properties of post-traumatic hippocampal glia. J. Neurosci., 19, 8152-8162.
24. D'Ambrosio, R., Fairbanks, J.P., Fender, J.S., Born, D.E., Doyle, D.L. & Miller, J.W. (2004) Post-traumatic epilepsy following fluid percussion injury in the rat. Brain, 127, 304-314.
25. D'Ambrosio, R., Fender, J.S., Fairbanks, J.P., Simon, E.A., Born, D.E., Doyle, D.L. & Miller, J.W. (2005) Progression from frontal-parietal to mesial-temporal epilepsy after fluid percussion injury in the rat. Brain, 128, 174-188.
26. Dash, P.K., Mach, S.A. & Moore, A.N. (2001) Enhanced neurogenesis in the rodent hippocampus following traumatic brain injury. J. Neurosci. Res., 63, 313-319.
27. Diaz-Arrastia, R., Agostini, M.A., Frol, A.B., Mickey, B., Fleckenstein, J., Bigio, E. & Van Ness, P.C. (2000) Neurophysiologic and neuroradiologic features of intractable epilepsy after traumatic brain injury in adults. Arch. Neurol., 57, 1611-1616.
28. Dietrich, W.D., Alonso, O., Busto, R., Globus, M.Y. & Ginsberg, M.D. (1994) Post-traumatic brain hypothermia reduces histopathological damage following concussive brain injury in the rat. Acta Neuropathol. (Berl.), 87, 250-258.
29. Dietrich, W.D., Atkins, C.M. & Bramlett, H.M. (2009) Protection in animal models of brain and spinal cord injury with mild to moderate hypothermia. J. Neurotrauma, 26, 301-312.
30. Dinocourt, C., Gallagher, S.E. & Thompson, S.M. (2006) Injury-induced axonal sprouting in the hippocampus is initiated by activation of trkB receptors. Eur. J. Neurosci., 24, 1857-1866.
31. Dudek, F.E., Obenaus, A., Schweitzer, J.S. & Wuarin, J.P. (1994) Functional significance of hippocampal plasticity in epileptic brain: electrophysiological changes of the dentate granule cells associated with mossy fiber sprouting. Hippocampus, 4, 259-265.
32. Erakovic, V., Zupan, G., Varljen, J., Laginja, J. & Simonic, A. (2001) Altered activities of rat brain metabolic enzymes caused by pentylenetetrazol kindling and pentylenetetrazol--induced seizures. Epilepsy Res., 43, 165-173.
33. Freund, T.F. & Buzsaki, G. (1996) Interneurons of the hippocampus. Hippocampus, 6, 347-470.
34. Gao, X., Deng-Bryant, Y., Cho, W., Carrico, K.M., Hall, E.D. & Chen, J. (2008) Selective death of newborn neurons in hippocampal dentate gyrus following moderate experimental traumatic brain injury. J. Neurosci. Res., 86, 2258-2270.
35. Gao, G., Oda, Y., Wei, E.P. & Povlishock, J.T. (2010) The adverse pial arteriolar and axonal consequences of traumatic brain injury complicated by hypoxia and their therapeutic modulation with hypothermia in rat. J. Cereb. Blood Flow Metab., 30, 628-637.
36. Garga, N. & Lowenstein, D.H. (2006) Posttraumatic epilepsy: a major problem in desperate need of major advances. Epilepsy Curr., 6, 1-5.
37. Golarai, G., Greenwood, A.C., Feeney, D.M. & Connor, J.A. (2001) Physiological and structural evidence for hippocampal involvement in persistent seizure susceptibility after traumatic brain injury. J. Neurosci., 21, 8523-8537.
38. Graber, K.D. & Prince, D.A. (2004) A critical period for prevention of posttraumatic neocortical hyperexcitability in rats. Ann. Neurol., 55, 860-870.
39. Grady, M.S., Charleston, J.S., Maris, D., Witgen, B.M. & 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.
40. Griesemer, D. & Mautes, A.M. (2007) Closed head injury causes hyperexcitability in rat hippocampal CA1 but not in CA3 pyramidal cells. J. Neurotrauma, 24, 1823-1832.
41. Gunn, A.J., Battin, M., Gluckman, P.D., Gunn, T.R. & Bennet, L. (2005) Therapeutic hypothermia: from lab to NICU. J. Perinat. Med., 33, 340-346.
42. Hachimi-Idrissi, S., Corne, L. & Huyghens, L. (2001) The effect of mild hypothermia and induced hypertension on long term survival rate and neurological outcome after asphyxial cardiac arrest in rats. Resuscitation, 49, 73-82.
43. Hayashi, N. (2009) Management of pitfalls for the successful clinical use of hypothermia treatment. J. Neurotrauma, 26, 445-453.
44. Herman, S.T. (2002) Epilepsy after brain insult: targeting epileptogenesis. Neurology, 59, S21-S26.
45. Holtmaat, A.J., Gorter, J.A., De Wit, J., Tolner, E.A., Spijker, S., Giger, R.J., Lopes da Silva, F.H. & Verhaagen, J. (2003) Transient downregulation of Sema3A mRNA in a rat model for temporal lobe epilepsy. A novel molecular event potentially contributing to mossy fiber sprouting. Exp. Neurol., 182, 142-150.
46. Houser, C.R., Miyashiro, J.E., Swartz, B.E., Walsh, G.O., Rich, J.R. & Delgado-Escueta, A.V. (1990) Altered patterns of dynorphin immunoreactivity suggest mossy fiber reorganization in human hippocampal epilepsy. J. Neurosci., 10, 267-282.
47. Hudak, A.M., Trivedi, K., Harper, C.R., Booker, K., Caesar, R.R., Agostini, M., Van Ness, P.C. & 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.
48. Hunt, R.F., Scheff, S.W. & Smith, B.N. (2009) Posttraumatic epilepsy after controlled cortical impact injury in mice. Exp. Neurol., 215, 243-252.
49. Hunt, R.F., Scheff, S.W. & 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.
50. Huttmann, K., Sadgrove, M., Wallraff, A., Hinterkeuser, S., Kirchhoff, F., Steinhauser, C. & Gray, W.P. (2003) Seizures preferentially stimulate proliferation of radial glia-like astrocytes in the adult dentate gyrus: functional and immunocytochemical analysis. Eur. J. Neurosci., 18, 2769-2778.
51. Indulekha, C.L., Sanalkumar, R., Thekkuveettil, A. & James, J. (2010) Seizure induces activation of multiple subtypes of neural progenitors and growth factors in hippocampus with neuronal maturation confined to dentate gyrus. Biochem. Biophys. Res. Commun., 393, 864-871.
52. Jessberger, S., Romer, B., Babu, H. & Kempermann, G. (2005) Seizures induce proliferation and dispersion of doublecortin-positive hippocampal progenitor cells. Exp. Neurol., 196, 342-351.
53. Jessberger, S., Zhao, C., Toni, N., Clemenson, G.D. Jr, Li, Y. & Gage, F.H. (2007) Seizure-associated, aberrant neurogenesis in adult rats characterized with retrovirus-mediated cell labeling. J. Neurosci., 27, 9400-9407.
54. Jiang, J.Y., Lyeth, B.G., Clifton, G.L., Jenkins, L.W., Hamm, R.J. & Hayes, R.L. (1991) Relationship between body and brain temperature in traumatically brain-injured rodents. J. Neurosurg., 74, 492-496.
55. Jiang, J.Y., Xu, W., Li, W.P., Gao, G.Y., Bao, Y.H., Liang, Y.M. & Luo, Q.Z. (2006) Effect of long-term mild hypothermia or short-term mild hypothermia on outcome of patients with severe traumatic brain injury. J. Cereb. Blood Flow Metab., 26, 771-776.
56. Kharatishvili, I. & Pitkanen, A. (2010) Association of the severity of cortical damage with the occurrence of spontaneous seizures and hyperexcitability in an animal model of posttraumatic epilepsy. Epilepsy Res., 90, 47-59.
57. Kharatishvili, I., Nissinen, J.P., McIntosh, T.K. & Pitkanen, A. (2006) A model of posttraumatic epilepsy induced by lateral fluid-percussion brain injury in rats. Neuroscience, 140, 685-697.
58. Lehmkuhle, M.J., Thomson, K.E., Scheerlinck, P., Pouliot, W., Greger, B. & Dudek, F.E. (2009) A simple quantitative method for analyzing electrographic status epilepticus in rats. J. Neurophysiol., 101, 1660-1670.
59. Loscher, W. & Schmidt, D. (2002) New horizons in the development of antiepileptic drugs. Epilepsy Res., 50, 3-16.
60. Lotocki, G., De Rivero Vaccari, J.P., Perez, E.R., Alonso, O.F., Curbelo, K., Keane, R.W. & Dietrich, W.D. (2006) Therapeutic hypothermia modulates TNFR1 signaling in the traumatized brain via early transient activation of the JNK pathway and suppression of XIAP cleavage. Eur. J. Neurosci., 24, 2283-2290.
61. 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.
62. Lukoyanov, N.V., Sa, M.J., Madeira, M.D. & Paula-Barbosa, M.M. (2004) Selective loss of hilar neurons and impairment of initial learning in rats after repeated administration of electroconvulsive shock seizures. Exp. Brain Res., 154, 192-200.
63. Lyeth, B.G., Jiang, J.Y. & Liu, S. (1993) Behavioral protection by moderate hypothermia initiated after experimental traumatic brain injury. J. Neurotrauma, 10, 57-64.
64. Margulies, S. & Hicks, R. (2009) Combination therapies for traumatic brain injury: prospective considerations. J. Neurotrauma, 26, 925-939.
65. Marion, D. & Bullock, M.R. (2009) Current and future role of therapeutic hypothermia. J. Neurotrauma, 26, 455-467.
66. Marion, D.W., Penrod, L.E., Kelsey, S.F., Obrist, W.D., Kochanek, P.M., Palmer, A.M., Wisniewski, S.R. & DeKosky, S.T. (1997) Treatment of traumatic brain injury with moderate hypothermia. N. Engl. J. Med., 336, 540-546.
67. Mayer, S.A. (2002) Hypothermia for neuroprotection after cardiac arrest. Curr Neurol Neurosci Rep, 2, 525-526.
68. Morimoto, K., Fahnestock, M. & Racine, R.J. (2004) Kindling and status epilepticus models of epilepsy: rewiring the brain. Prog. Neurobiol., 73, 1-60.
69. Nadler, J.V. (2003) The recurrent mossy fiber pathway of the epileptic brain. Neurochem. Res., 28, 1649-1658.
70. Nitta, N., Heinrich, C., Hirai, H. & Suzuki, F. (2008) Granule cell dispersion develops without neurogenesis and does not fully depend on astroglial cell generation in a mouse model of temporal lobe epilepsy. Epilepsia, 49, 1711-1722.
71. Parent, J.M., Yu, T.W., Leibowitz, R.T., Geschwind, D.H., Sloviter, R.S. & Lowenstein, D.H. (1997) Dentate granule cell neurogenesis is increased by seizures and contributes to aberrant network reorganization in the adult rat hippocampus. J. Neurosci., 17, 3727-3738.
72. Parent, J.M., Tada, E., Fike, J.R. & Lowenstein, D.H. (1999) Inhibition of dentate granule cell neurogenesis with brain irradiation does not prevent seizure-induced mossy fiber synaptic reorganization in the rat. J. Neurosci., 19, 4508-4519.
73. Paxinos, G. & Watson, C. (2005) The Rat Brain in Stereotaxic Coordinates. Elsevier Academic Press, Burlington, MA, USA.
74. Polderman, K.H. (2008) Induced hypothermia and fever control for prevention and treatment of neurological injuries. Lancet, 371, 1955-1969.
75. Polderman, K.H. (2009) Mechanisms of action, physiological effects, and complications of hypothermia. Crit. Care Med., 37, S186-S202.
76. Polderman, K.H. & Herold, I. (2009) Therapeutic hypothermia and controlled normothermia in the intensive care unit: practical considerations, side effects, and cooling methods. Crit. Care Med., 37, 1101-1120.
77. Potts, M.B., Rola, R., Claus, C.P., Ferriero, D.M., Fike, J.R. & Noble-Haeusslein, L.J. (2009) Glutathione peroxidase overexpression does not rescue impaired neurogenesis in the injured immature brain. J. Neurosci. Res., 87, 1848-1857.
78. Racine, R.J. (1972) Modification of seizure activity by electrical stimulation. II. Motor seizure. Electroencephalogr. Clin. Neurophysiol., 32, 281-294.
79. Represa, A., Niquet, J., Pollard, H., Khrestchatisky, M. & Ben-Ari, Y. (1994) From seizures to neo-synaptogenesis: intrinsic and extrinsic determinants of mossy fiber sprouting in the adult hippocampus. Hippocampus, 4, 270-274.
80. Ribak, C.E., Tran, P.H., Spigelman, I., Okazaki, M.M. & Nadler, J.V. (2000) Status epilepticus-induced hilar basal dendrites on rodent granule cells contribute to recurrent excitatory circuitry. J. Comp. Neurol., 428, 240-253.
81. Rola, R., Mizumatsu, S., Otsuka, S., Morhardt, D.R., Noble-Haeusslein, L.J., Fishman, K., Potts, M.B. & Fike, J.R. (2006) Alterations in hippocampal neurogenesis following traumatic brain injury in mice. Exp. Neurol., 202, 189-199.
82. Ross, S.T. & Soltesz, I. (2000) Selective depolarization of interneurons in the early posttraumatic dentate gyrus: involvement of the Na(+)/K(+)-ATPase. J. Neurophysiol., 83, 2916-2930.
83. Sahay, A., Kim, C.H., Sepkuty, J.P., Cho, E., Huganir, R.L., Ginty, D.D. & Kolodkin, A.L. (2005) Secreted semaphorins modulate synaptic transmission in the adult hippocampus. J. Neurosci., 25, 3613-3620.
84. 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.
85. Santhakumar, V., Bender, R., Frotscher, M., Ross, S.T., Hollrigel, G.S., Toth, Z. & Soltesz, I. (2000) Granule cell hyperexcitability in the early post-traumatic rat dentate gyrus: the 'irritable mossy cell' hypothesis. J. Physiol., 524 Pt 1, 117-134.
86. Santhakumar, V., Ratzliff, A.D., Jeng, J., Toth, Z. & Soltesz, I. (2001) Long-term hyperexcitability in the hippocampus after experimental head trauma. Ann. Neurol., 50, 708-717.
87. Seress, L. & Gallyas, F. (2000) The use of a sodium tungstate developer markedly improves the electron microscopic localization of zinc by the Timm method. J. Neurosci. Methods, 100, 33-39.
88. Shankaran, S., Laptook, A.R., Ehrenkranz, R.A., Tyson, J.E., McDonald, S.A., Donovan, E.F., Fanaroff, A.A., Poole, W.K., Wright, L.L., Higgins, R.D., Finer, N.N., Carlo, W.A., Duara, S., Oh, W., Cotten, C.M., Stevenson, D.K., Stoll, B.J., Lemons, J.A., Guillet, R. & Jobe, A.H. (2005) Whole-body hypothermia for neonates with hypoxic-ischemic encephalopathy. N. Engl. J. Med., 353, 1574-1584.
89. Shapiro, L.A., Figueroa-Aragon, S. & Ribak, C.E. (2007) Newly generated granule cells show rapid neuroplastic changes in the adult rat dentate gyrus during the first five days following pilocarpine-induced seizures. Eur. J. Neurosci., 26, 583-592.
90. Sloviter, R.S. (1992) Possible functional consequences of synaptic reorganization in the dentate gyrus of kainate-treated rats. Neurosci. Lett., 137, 91-96.
91. Sloviter, R.S. (1994) The functional organization of the hippocampal dentate gyrus and its relevance to the pathogenesis of temporal lobe epilepsy. Ann. Neurol., 35, 640-654.
92. Sun, D., Colello, R.J., Daugherty, W.P., Kwon, T.H., McGinn, M.J., Harvey, H.B. & Bullock, M.R. (2005) Cell proliferation and neuronal differentiation in the dentate gyrus in juvenile and adult rats following traumatic brain injury. J. Neurotrauma, 22, 95-105.
93. Sun, D., McGinn, M.J., Zhou, Z., Harvey, H.B., Bullock, M.R. & Colello, R.J. (2007) Anatomical integration of newly generated dentate granule neurons following traumatic brain injury in adult rats and its association to cognitive recovery. Exp. Neurol., 204, 264-272.
94. Sutula, T., He, X.X., Cavazos, J. & Scott, G. (1988) Synaptic reorganization in the hippocampus induced by abnormal functional activity. Science, 239, 1147-1150.
95. Sutula, T., Cascino, G., Cavazos, J., Parada, I. & Ramirez, L. (1989) Mossy fiber synaptic reorganization in the epileptic human temporal lobe. Ann. Neurol., 26, 321-330.
96. Suzuki, T., Bramlett, H.M. & Dietrich, W.D. (2003) The importance of gender on the beneficial effects of posttraumatic hypothermia. Exp. Neurol., 184, 1017-1026.
97. Swartz, B.E., Houser, C.R., Tomiyasu, U., Walsh, G.O., DeSalles, A., Rich, J.R. & Delgado-Escueta, A. (2006) Hippocampal cell loss in posttraumatic human epilepsy. Epilepsia, 47, 1373-1382.
98. Temkin, N.R. (2009) Preventing and treating posttraumatic seizures: the human experience. Epilepsia, 50(Suppl 2), 10-13.
99. Temkin, N.R., Jarell, A.D. & Anderson, G.D. (2001) Antiepileptogenic agents: how close are we? Drugs, 61, 1045-1055.
100. Urrea, C., Castellanos, D.A., Sagen, J., Tsoulfas, P., Bramlett, H.M. & Dietrich, W.D. (2007) Widespread cellular proliferation and focal neurogenesis after traumatic brain injury in the rat. Restor Neurol Neurosci, 25, 65-76.
101. Vespa, P.M., Nuwer, M.R., Nenov, V., Ronne-Engstrom, E., Hovda, D.A., Bergsneider, M., Kelly, D.F., Martin, N.A. & Becker, D.P. (1999) Increased incidence and impact of nonconvulsive and convulsive seizures after traumatic brain injury as detected by continuous electroencephalographic monitoring. J. Neurosurg., 91, 750-760.
102. Walter, C., Murphy, B.L., Pun, R.Y., Spieles-Engemann, A.L. & Danzer, S.C. (2007) Pilocarpine-induced seizures cause selective time-dependent changes to adult-generated hippocampal dentate granule cells. J. Neurosci., 27, 7541-7552.
103. Zhang, X., Cui, S.S., Wallace, A.E., Hannesson, D.K., Schmued, L.C., Saucier, D.M., Honer, W.G. & Corcoran, M.E. (2002) Relations between brain pathology and temporal lobe epilepsy. J. Neurosci., 22, 6052-6061.
104. Zhou, Y., Gunput, R.A. & Pasterkamp, R.J. (2008) Semaphorin signaling: progress made and promises ahead. Trends Biochem. Sci., 33, 161-170.