Neurobehavioral consequences of stressor exposure in rodent models of epilepsy

Progress in Neuro-Psychopharmacology and Biological Psychiatry

Volumn 34, Issue 5, 2010, Pages 808-815

  Heinrichs, Stephen C ^a  

^a REGIS COLLEGE   (United States)

Author keywords

Anxiety; Behavior; CRF; Epilepsy; Rodent; Seizure

Indexed keywords

CORTICOTROPIN RELEASING FACTOR; GLUTAMATE DECARBOXYLASE 65;

AGGRESSION; AMYGDALOID NUCLEUS; ANXIETY; ARTICLE; BEHAVIOR CONTROL; COPING BEHAVIOR; EMOTIONALITY; ENVIRONMENTAL STRESS; EPILEPSY; EPILEPTOGENESIS; EXPLORATORY BEHAVIOR; FOCAL EPILEPSY; GENERALIZED EPILEPSY; GENETIC PREDISPOSITION; HIPPOCAMPUS; HYPOTHALAMUS HYPOPHYSIS ADRENAL SYSTEM; KINDLING; LOCUS CERULEUS; MENTAL STRESS; MOTOR CORTEX; NERVE CELL NETWORK; NEUROMODULATION; NONHUMAN; NORADRENERGIC SYSTEM; SEXUAL BEHAVIOR;

ANIMALS; BEHAVIOR, ANIMAL; DISEASE MODELS, ANIMAL; EPILEPSY; HUMANS; MICE; RATS; STRESS, PSYCHOLOGICAL;

EID: 77953726761     PISSN: 02785846     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.pnpbp.2009.11.002     Document Type: Article

References (122)

1. Adamec R.E. Amygdala kindling and anxiety in the rat. NeuroReport 1990, 1(3-4):255-258.
2. Adamec R.E. Does kindling model anything clinically relevant?. Biol Psychiatry 1990, 27(3):249-279.
3. An S.J., Park S.K., et al. Altered corticotropin-releasing factor (CRF) receptor immunoreactivity in the gerbil hippocampal complex following spontaneous seizure. Neurochem Int 2003, 43(1):39-45.
4. Aston-Jones G., Bloom F.E. Activity of norepinephrine-containing locus coeruleus neurons in behaving rats anticipates fluctuations in the sleep-waking cycle. J Neurosci 1981, 1(8):876-886.
5. Aston-Jones G., Bloom F.E. Nonrepinephrine-containing locus coeruleus neurons in behaving rats exhibit pronounced responses to non-noxious environmental stimuli. J Neurosci 1981, 1(8):887-900.
6. Aston-Jones G., Rajkowski J., Kubiak P. Conditioned responses of monkey locus coeruleus neurons anticipate acquisition of discriminative behavior in a vigilance task. Neuroscience 1997, 80(3):697-715.
7. Aston-Jones G., Rajkowski J., Cohen J. Role of locus coeruleus in attention and behavioral flexibility. Biol Psychiatry 1999, 46(9):1309-1320.
8. Aston-Jones G., Chen S., Zhu Y., Oshinsky M.L. A neural circuit for circadian regulation of arousal. Nat Neurosci 2001, 4(7):732-738.
9. Balcombe J.P., Barnard N.D., Sandusky C. Laboratory routines cause animal stress. Contemp Top Lab Anim Sci 2004, 43(6):42-51.
10. Bandler R., Keay K.A., Floyd N., Price J. Central circuits mediating patterned autonomic activity during active vs. passive emotional coping. Brain Res Bull 2000, 53(1):95-104.
11. Banko M.L., Allen K.M., Dolina S., Neumann P.E., Seyfried T.N. Genomic imprinting and audiogenic seizures in mice. Behav Genet 1997, 27(5):465-475.
12. Baram T.Z., Hatalski C.G. Neuropeptide-mediated excitability: a key triggering mechanism for seizure generation in the developing brain. Trends Neurosci 1998, 21(11):471-476.
13. Baram T.Z., Yi S., Avishai-Eliner S., Schultz L. Development neurobiology of the stress response: multilevel regulation of corticotropin-releasing hormone function. Ann N Y Acad Sci 1997, 814:252-265.
14. Baram T.Z., Mitchell W.G., Brunson K., Haden E. Infantile spasms: hypothesis-driven therapy and pilot human infant experiments using corticotropin-releasing hormone receptor antagonists. Dev Neurosci 1999, 21(3-5):281-289.
15. Barry D.I., Wanscher B., Kragh J., Bolwig T.G., Kokaia M., Brundin P., Bjorklund A., Lindvall O. Grafts of fetal locus coeruleus neurons in rat amygdala-piriform cortex suppress seizure development in hippocampal kindling. Exp Neurol 1989, 106(2):125-132.
16. Belzung C. Rodent models of anxiety-like behaviors: are they predictive for compounds acting via non-benzodiazepine mechanisms?. Curr Opin Investig Drugs 2001, 2(8):1108-1111.
17. Belzung C., Griebel G. Measuring normal and pathological anxiety-like behaviour in mice: a review. Behav Brain Res 2001, 125(1-2):141-149.
18. Bhatnagar S., Dallman M. Neuroanatomical basis for facilitation of hypothalamic-pituitary-adrenal responses to a novel stressor after chronic stress. Neuroscience 1998, 84(4):1025-1039.
19. Bowman E.S. Relationship of remote and recent life events to the onset and course of non-epileptic seizures. Non-epileptic seizures 2000, 269-283. Butterworth-Heinemann, Boston. J.R. Gates, A.J. Rowan (Eds.).
20. Brooks-Kayal A.R. Rearranging receptors. Epilepsia 2005, 46(Suppl 7):29-38.
21. Brown R.A., Walling S.G., Milway J.S., Harley C.W. Locus ceruleus activation suppresses feedforward interneurons and reduces beta-gamma electroencephalogram frequencies while it enhances theta frequencies in rat dentate gyrus. J Neurosci 2005, 25(8):1985-1991.
22. Chance W.T., Dayal R., Friend L.A., Sheriff S. Possible role of CRF peptides in burn-induced hypermetabolism. Life Sci 2006, 78(7):694-703.
23. Compan V., Zhou M., et al. Attenuated response to stress and novelty and hypersensitivity to seizures in 5-HT4 receptor knock-out mice. J Neurosci 2004, 24(2):412-419.
24. de Kloet E.R., Karst H., Joels M. Corticosteroid hormones in the central stress response: quick-and-slow. Front Neuroendocrinol 2008, 29(2):268-272.
25. Depaulis A., Helfer V., Deransart C., Marescaux C. Anxiogenic-like consequences in animal models of complex partial seizures. Neurosci Biobehav Rev 1997, 21(6):767-774.
26. Drage M.G., Holmes G.L., Seyfried T.N. Hippocampal neurons and glia in epileptic EL mice. J Neurocytol 2002, 31(8-9):681-692.
27. Eells J.B., Clough R.W., Browning R.A., Jobe P.C. Comparative fos immunoreactivity in the brain after forebrain, brainstem, or combined seizures induced by electroshock, pentylenetetrazol, focally induced and audiogenic seizures in rats. Neuroscience 2004, 123(1):279-292.
28. Eggers A.E. Temporal lobe epilepsy is a disease of faulty neuronal resonators rather than oscillators, and all seizures are provoked, usually by stress. Med Hypotheses 2007, 69(6):1284-1289.
29. Ehlers C.L., Henriksen S.J., Wang M., Rivier J., Vale W., Bloom F.E. Corticotropin releasing factor produces increases in brain excitability and convulsive seizures in rats. Brain Res 1983, 278(1-2):332-336.
30. Feeney D.M., Gullotta F.P., Gilmore W. Hyposexuality produced by temporal lobe epilepsy in the cat. Epilepsia 1998, 39(2):140-149.
31. Fenoglio K.A., Brunson K.L., Avishai-Eliner S., Chen Y., Baram T.Z. Region-specific onset of handling-induced changes in corticotropin-releasing factor and glucocorticoid receptor expression. Endocrinology 2004, 145(6):2702-2706.
32. Fenoglio K.A., Chen Y., Baram T.Z. Neuroplasticity of the hypothalamic-pituitary-adrenal axis early in life requires recurrent recruitment of stress-regulating brain regions. J Neurosci 2006, 26(9):2434-2442.
33. Ferraro T.N., Golden G.T., Smith G.G., Berrettini W.H. Differential susceptibility to seizures induced by systemic kainic acid treatment in mature DBA/2J and C57BL/6J mice. Epilepsia 1995, 36(3):301-307.
34. File S.E., Lippa A.S., Beer B., Lippa M.T. Animal tests of anxiety. Current protocols in neuroscience 2004, 8.3.1-8.3.22. Wiley, New York. J. Crawley, C.R. Gerfen, M.A. Rogawski (Eds.).
35. Foote S.L., Bloom F.E., Aston J.G. Nucleus locus ceruleus: new evidence of anatomical and physiological specificity. Physiol Rev 1983, 63(844):844-914.
36. Forcelli P.A., Orefice L.L., Heinrichs S.C. Neural, endocrine and electroencephalographic hyperreactivity to human contact: a diathesis-stress model of seizure susceptibility in El mice. Brain Res 2007, 1144:248-256.
37. Frucht M.M., Quigg M., Schwaner C., Fountain N.B. Distribution of seizure precipitants among epilepsy syndromes. Epilepsia 2000, 41(12):1534-1539.
38. Fuller J.L., Collins R.L. Mice unilaterally sensitized for audiogenic seizures. Science 1968, 162(859):1295.
39. Garcia-Cairasco N., Oliveira J.A., Wakamatsu H., Bueno S.T., Guimaraes F.S. Reduced exploratory activity of audiogenic seizures susceptible Wistar rats. Physiol Behav 1998, 64(5):671-674.
40. Genizi J., Pillar G., Ravid S., Shahar E. Apparent life-threatening events: neurological correlates and the mandatory work-up. J Child Neurol 2008, 23(11):1305-1307.
41. Geschwind N. Interictal behavioral changes in epilepsy. Epilepsia 1983, 24(Suppl 1):S23-S30.
42. Giorgi F.S., Ferrucci M., Lazzeri G., Pizzanelli C., Lenzi P., Alessandrl M.G., Murri L., Fornai F. A damage to locus coeruleus neurons converts sporadic seizures into self-sustaining limbic status epilepticus. Eur J NeuroSci 2003, 17(12):2593-2601.
43. Giorgi F.S., Mauceli G., Blandini F., Ruggieri S., Paparelli A., Murri L., Fornai F. Locus coeruleus and neuronal plasticity in a model of focal limbic epilepsy. Epilepsia 2006, 47(Suppl 5):21-25.
44. Groticke I., Hoffmann K., Loscher W. Behavioral alterations in the pilocarpine model of temporal lobe epilepsy in mice. Exp Neurol 2007, 207(2):329-349.
45. Hannesson D.K., Howland J., Pollock M., Mohapel P., Wallace A.E., Corcoran M.E. Dorsal hippocampal kindling produces a selective and enduring disruption of hippocampally mediated behavior. J Neurosci 2001, 21(12):4443-4450.
46. Hannesson D.K., Howland J.G., Pollock M., Mohapel P., Wallace A.E., Corcoran M.E. Anterior perirhinal cortex kindling produces long-lasting effects on anxiety and object recognition memory. Eur J NeuroSci 2005, 21(4):1081-1090.
47. Hannesson D.K., Pollock M.S., Howland J.G., Mohapel P., Wallace A.E., Corcoran M.E. Amygdaloid kindling is anxiogenic but fails to alter object recognition or spatial working memory in rats. Epilepsy Behav 2008, 13(1):52-61.
48. Heinrichs S.C., Koob G.F. Corticotropin-releasing factor in brain: a role in activation, arousal, and affect regulation. J Pharmacol Exp Ther 2004, 311(2):427-440.
49. Heinrichs S.C., Seyfried T.N. Behavioral seizure correlates in animal models of epilepsy: a road map for assay selection, data interpretation, and the search for causal mechanisms. Epilepsy Behav 2006, 8(1):5-38.
50. Henry K.R., Bowman R.E. The dilute locus, pyridoxine deficiency, and audiogenic seizures in mice. Proc Soc Exp Biol Med 1968, 128(3):635-638.
51. Herman J.P., Cullinan W.E. Neurocircuitry of stress: central control of the hypothalamo-pituitary-adrenocortical axis. Trends Neurosci 1997, 20(2):78-84.
52. Iturrian W.B., Fink G.B. Influence of age and brief auditory conditioning upon experimental seizures in mice. Dev Psychobiol 1969, 2(1):10-18.
53. Jobe P.C. Common pathogenic mechanisms between depression and epilepsy: an experimental perspective. Epilepsy Behav 2003, 4(Suppl 3):S14-S24.
54. Jobe P.C., Picchioni A.L., Chin L. Role of brain norepinephrine in audiogenic seizure in the rat. J Pharmacol Exp Ther 1973, 184:1-10.
55. Joels M. Functional actions of corticosteroids in the hippocampus. Eur J Pharmacol 2008, 583(2-3):312-321.
56. Joels M., Karst H., Krugers H.J., Lucassen P.J. Chronic stress: implications for neuronal morphology, function and neurogenesis. Front Neuroendocrinol 2007, 28(2-3):72-96.
57. Joels M., Krugers H.J., Lucassen P.J., Karst H. Corticosteroid effects on cellular physiology of limbic cells. Brain Res 2009, 1293:91-100.
58. Kalynchuk L.E. Long-term amygdala kindling in rats as a model for the study of interictal emotionality in temporal lobe epilepsy. Neurosci Biobehav Rev 2000, 24(7):691-704.
59. Kalynchuk L.E., Pinel J.P., Treit D., Barnes S.J., McEachern J.C., Kippin T.E. Persistence of the interictal emotionality produced by long-term amygdala kindling in rats. Neuroscience 1998, 85(4):1311-1319.
60. Karst H., de Kloet E.R., Joels M. Episodic corticosterone treatment accelerates kindling epileptogenesis and triggers long-term changes in hippocampal CA1 cells, in the fully kindled state. Eur J NeuroSci 1999, 11(3):889-898.
61. Kash S.F., Johnson R.S., Tecott L.H., Noebels J.L., Mayfield R.D., Hanahan D., Baekkeskov S. Epilepsy in mice deficient in the 65-kDa isoform of glutamic acid decarboxylase. Proc Natl Acad Sci USA 1997, 94(25):14060-14065.
62. Kash S.F., Tecott L.H., Hodge C., Baekkeskov S. Increased anxiety and altered responses to anxiolytics in mice deficient in the 65-kDa isoform of glutamic acid decarboxylase. Proc Natl Acad Sci USA 1999, 96(4):1698-1703.
63. Kitchigina V., Vankov A., Harley C., Sara S.J. Novelty-elicited, noradrenaline-dependent enhancement of excitability in the dentate gyrus. Eur J NeuroSci 1997, 9(1):41-47.
64. Kling M.A., Smith M.A., Glowa J.R., Pluznik D., Demas J., DeBellis M.D., Gold P.W., Schulkin J. Facilitation of cocaine kindling by glucocorticoids in rats. Brain Res 1993, 629(1):163-166.
65. Ko K.H., Dailey J.W., Jobe P.C. Evaluation of monoaminergic receptors in the genetically epilepsy prone rat. Experientia 1984, 40(1):70-73.
66. Koh S., Storey T.W., Santos T.C., Mian A.Y., Cole A.J. Early-life seizures in rats increase susceptibility to seizure-induced brain injury in adulthood. Neurology 1999, 53(5):915-921.
67. Koob G.F. Corticotropin-releasing factor, norepinephrine, and stress. Biol Psychiatry 1999, 46(9):1167-1180.
68. Koutsogiannopoulos S., Adelson F., Lee V., Andermann F. Stressors at the onset of adult epilepsy: implications for practice. Epileptic Disord 2009, 11(1):42-47.
69. Ledoux J.A., Iwata J., Clechetti P., Reis D.J. Different projections of the central amygdaloid nucleus mediate autonomic and behavioral correlates of conditioned fear. J. Neurosci. 1988, 8:2517-2529.
70. Leussis M.P., Heinrichs S.C. Temporal ontogeny of circuit activation prior to the onset of seizure susceptibility in EL/Suz mice. Neuroscience 2007, 145(1):33-41.
71. Levine D.N. Sherrington's "The Integrative action of the nervous system": a centennial appraisal. J Neurol Sci 2007, 253(1-2):1-6.
72. Maciejewski-Lenoir D., Heinrichs S.C., Liu X.-J., Ling N., Tucker A., Xie Q., Lappi D.A., Grigoriadis D.E. Selective impairment of corticotropin-releasing factor1 (CRF1) receptor-mediated function using CRF coupled to saporin. Endocrinology 2000, 141(2):498-504.
73. McCarthy J.R., Heinrichs S.C., Grigoriadis D.E. Recent advances with the CRF1 receptor: design of small molecule inhibitors, receptor subtypes and clinical indications. Curr Pharm Des 1999, 5(5):289-315.
74. McEwen B.S. Allostasis, allostatic load, and the aging nervous system: role of excitatory amino acids and excitotoxicity. Neurochem Res 2000, 25(9-10):1219-1231.
75. McEwen B.S. Effects of adverse experiences for brain structure and function. Biol Psychiatry 2000, 48(8):721-731.
76. McEwen B.S. Plasticity of the hippocampus: adaptation to chronic stress and allostatic load. Ann N Y Acad Sci 2001, 933:265-277.
77. McEwen B.S., Magarinos A.M. Stress and hippocampal plasticity: implications for the pathophysiology of affective disorders. Hum Psychopharmacol 2001, 16(Supplement 1):S7-S19.
78. Mellanby J., Strawbridge P., Collingridge G.I., George G., Rands G., Stroud C., Thompson P. Behavioural correlates of an experimental hippocampal epileptiform syndrome in rats. J Neurol Neurosurg Psychiatry 1981, 44(12):1084-1093.
79. Michaud D.S., McLean J., Keith S.E., Ferrarotto C., Hayley S., Khan S.A., Anisman H., Merali Z. Differential impact of audiogenic stressors on Lewis and Fischer rats: behavioral, neurochemical, and endocrine variations. Neuropsychopharmacology 2003, 28(6):1068-1081.
80. Midzyanovskaya I.S., Shatskova A.B., Sarkisova K.Y., van Luijtelaar G., Tuomisto L., Kuznetsova G.D. Convulsive and nonconvulsive epilepsy in rats: effects on behavioral response to novelty stress. Epilepsy Behav 2005, 6(4):543-551.
81. Miller J.W., Turner G.M., Gray B.C. Anticonvulsant effects of the experimental induction of hippocampal theta activity. Epilepsy Res 1994, 18(3):195-204.
82. Murashima Y.L., Kassamo K., Suzuki J. Developmental and seizure-related regional differences in immediate early gene expression and GABAergic abnormalities in the brain of EL mice. Epilepsy Res 1996, 26(1):3-14.
83. Murashima Y.L., Yoshii M., Suzuki J. Ictogenesis and epileptogenesis in EL mice. Epilepsia 2002, 43(Suppl 5):130-135.
84. Nakagawa Y., Asano Y., Awatsu N., Sawada M., Nakano K. Enhanced Fos expression in the hippocampus of El mice after short-term vestibular stimulation. Neurosci Lett 1999, 271(2):105-108.
85. Nitz D.A., McNaughton B.L. Hippocampal EEG and unit activity responses to modulation of serotonergic median raphe neurons in the freely behaving rat. Learn Mem 1999, 6(2):153-167.
86. Park S.K., Choi D.I., Hwang I.K., An S.J., Suh J.G., Oh Y.S., Won M.H., Kang T.C. The differential expression of corticotropin releasing factor and its binding protein in the gerbil hippocampal complex following seizure. Neurochem Int 2003, 42(1):57-65.
87. Pascual J., Heinrichs S.C. Olfactory neophobia and seizure susceptibility phenotypes in an animal model of epilepsy are normalized by impairment of brain corticotropin releasing factor. Epilepsia 2007, 48(4):827-833.
88. Pericic D., Lazic J., Svob Strac D. Anticonvulsant effects of acute and repeated fluoxetine treatment in unstressed and stressed mice. Brain Res 2005, 1033(1):90-95.
89. Persinger M.A. Maintained hypersexuality between male rats following chronically induced limbic seizures: implications for bisexuality in complex partial epileptic seizures. Psychol Rep 1994, 74(2):647-652.
90. Piekut D.T., Phipps B. Increased corticotropin-releasing factor immunoreactivity in select brain sites following kainate elicited seizures. Brain Res 1998, 781(1-2):100-113.
91. Piekut D.T., Phipps B. Corticotropin-releasing factor: immunolabeled fibers in brain regions with localized kainate neurotoxicity. Acta Neuropathol 1999, 98(6):622-628.
92. Price M.L., Kirby L.G., Valentino R.J., Lucki I. Evidence for corticotropin-releasing factor regulation of serotonin in the lateral septum during acute swim stress: adaptation produced by repeated swimming. Psychopharmacology (Berlin) 2002, 162(4):406-414.
93. Radulovic J., Fischer A., Katerkamp U., Spiess J. Role of regional neurotransmitter receptors in corticotropin-releasing factor (CRF)-mediated modulation of fear conditioning. Neuropharmacology 2000, 39(4):707-710.
94. Rajkowski J., Kubiak P., Aston-Jones G. Locus coeruleus activity in monkey: phasic and tonic changes are associated with altered vigilance. Brain Res Bull 1994, 35(5-6):607-616.
95. Reynolds E.R., Stauffer E.A., Feeney L., Rojahn E., Jacobs B., McKeever C. Treatment with the antiepileptic drugs phenytoin and gabapentin ameliorates seizure and paralysis of Drosophila bang-sensitive mutants. J Neurobiol 2004, 58(4):503-513.
96. Rinaldi D., Larrigaldie V., Chapouthier G., Martin B. Unexpected absence of correlation between the genetic mechanisms regulating beta-carboline-induced seizures and anxiety manifested in an elevated plus-maze test. Behav Brain Res 2001, 125(1-2):159-165.
97. Roberts A.J., Crabbe J.C., Keith L.D. Corticosterone increases severity of acute withdrawal from ethanol, pentobarbital, and diazepam in mice. Psychopharmacology (Berlin) 1994, 115(1-2):278-284.
98. Rosen J.B., Hamerman E., Sitcoske M., Glowa J.R., Schulkin J. Hyperexcitability: exaggerated fear-potentiated startle produced by partial amygdala kindling. Behav Neurosci 1996, 110(1):43-50.
99. Ross K.C., Coleman J.R. Developmental and genetic audiogenic seizure models: behavior and biological substrates. Neurosci Biobehav Rev 2000, 24:639-653.
100. Sara S.J., Vankov A., Herve A. Locus coeruleus-evoked responses in behaving rats: a clue to the role of noradrenaline in memory. Brain Res Bull 1994, 35(5-6):457-465.
101. Schreiber R.A., Graham J.M. Audiogenic priming in DBA/2J and C57BL/6J mice: interactions among age, prime-to-test interval and index of seizure. Dev Psychobiol 1976, 9(1):57-66.
102. Schridde U., van Luijtelaar G. Corticosterone increases spike-wave discharges in a dose- and time-dependent manner in WAG/Rij rats. Pharmacol Biochem Behav 2004, 78(2):369-375.
103. Seyfried T.N. Audiogenic seizures in mice. Fed Proc 1979, 38(10):2399-2404.
104. Seyfried T.N. Genetic heterogeneity for the development of audiogenic seizures in mice. Brain Res 1983, 271(2):325-329.
105. Shekhar A., Truitt W., Rainnie D., Sajdyk T. Role of stress, corticotrophin releasing factor (CRF) and amygdala plasticity in chronic anxiety. Stress 2005, 8(4):209-219.
106. Sherrington C.S. The integrative action of the nervous system 1906, Charles Scribner and Sons, New York.
107. Silveira D.C., Liu Z., de LaCalle S., Lu J., Klein P., Holmes G.L., Herzog A.G. Activation of the locus coeruleus after amygdaloid kindling. Epilepsia 1998, 39(12):1261-1264.
108. Slawecki C.J., Somes C., Rivier J.E., Ehlers C.L. Neurophysiological effects of intracerebroventricular administration of urocortin. Peptides (New York) 1999, 20(2):211-218.
109. Snyder M. Revised epilepsy stressor inventory. J Neurosci Nurs 1993, 25(1):9-13.
110. Suzuki J. Investigations of epilepsy with a mutant animal (EL mouse) model. Epilepsia 2004, 45(Suppl 8):2-5.
111. Suzuki J., Nakamoto Y. Abnormal plastic phenomena of sensory-precipitated epilepsy in the mutant El mouse. Exp Neurol 1982, 75(2):440-452.
112. Swinkels W.A., Engelsman M., Kasteleijn-Nolst Trenite D.G., Baal M.G., de Haan G.J., Oosting J. Influence of an evacuation in February 1995 in The Netherlands on the seizure frequency in patients with epilepsy: a controlled study. Epilepsia 1998, 39(11):1203-1207.
113. Tai S.K., Huang F.D., Moochhala S., Khanna S. Hippocampal theta state in relation to formalin nociception. Pain 2006, 121(1-2):29-42.
114. Temkin N.R., Davis G.R. Stress as a risk factor for seizures among adults with epilepsy. Epilepsia 1984, 25(4):450-456.
115. Todorova M.T., Burwell T.J., Seyfried T.N. Environmental risk factors for multifactorial epilepsy in EL mice. Epilepsia 1999, 40(12):1697-1707.
116. Tsuda H., Ito M., Oguro K., Mutoh K., Shiraishi H., Shirasaka Y., Mikawa H. Age- and seizure-related changes in noradrenaline and dopamine in several brain regions of epileptic El mice. Neurochem Res 1993, 18(2):111-117.
117. Turner L.H., Lim C.E., Heinrichs S.C. Antisocial and seizure susceptibility phenotypes in an animal model of epilepsy are normalized by impairment of brain corticotropin-releasing factor. Epilepsy Behav 2007, 10(1):8-15.
118. Venit E.L., Shepard B.D., Seyfried T.N. Oxygenation prevents sudden death in seizure-prone mice. Epilepsia 2004, 45(8):993-996.
119. Walling S.G., Harley C.W. Locus ceruleus activation initiates delayed synaptic potentiation of perforant path input to the dentate gyrus in awake rats: a novel beta-adrenergic- and protein synthesis-dependent mammalian plasticity mechanism. J Neurosci 2004, 24(3):598-604.
120. Weiss S.R., Post R.M., Gold P.W., Chrousos G., Sullivan T.L., Walker D., Pert A. CRF-induced seizures and behavior: interaction with amygdala kindling. Brain Res 1986, 372(2):345-351.
121. Weiss G.K., Lewis J., Jimenez-Rivera C., Vigil A., Corcoran M.E. Antikindling effects of locus coeruleus stimulation: mediation by ascending noradrenergic projections. Exp Neurol 1990, 108(2):136-140.
122. Wieraszko A., Seyfried T.N. Influence of audiogenic seizures on synaptic facilitation in mouse hippocampal slices is mediated by N-methyl-D-aspartate receptor. Epilepsia 1993, 34(6):979-984.