Sex and hormonal influences on seizures and epilepsy

Hormones and Behavior

Volumn 63, Issue 2, 2013, Pages 267-277

  Velíšková, Jana ^a   DeSantis, Kara A ^a,b  

^a NEW YORK MEDICAL COLLEGE   (United States)

^b STATE UNIVERSITY OF NEW YORK   (United States)

Author keywords

Allopreganalone; Anticonvulsant drugs; Epilepsy; Estradiol; Neuronal excitability; Progesterone; Seizure induced damage; Sex differences

Indexed keywords

ESTRADIOL; ESTRADIOL BENZOATE; ESTRIOL; ESTRONE; PROGESTERONE; SEPRANOLONE; SEX HORMONE;

AICARDI SYNDROME; DISEASE PREDISPOSITION; EPILEPSY; EPILEPTIC DISCHARGE; FEBRILE CONVULSION; FOLLICULAR PHASE; GENERALIZED EPILEPSY; HORMONE SUBSTITUTION; HUMAN; INFANTILE SPASM; LANDAU KLEFFNER SYNDROME; LENNOX GASTAUT SYNDROME; LUTEAL PHASE; MYOCLONUS EPILEPSY; NERVE CELL EXCITABILITY; NERVE CELL LESION; NEUROPROTECTION; NONHUMAN; OHTAHARA SYNDROME; PRIORITY JOURNAL; PULSE RATE; RETT SYNDROME; REVIEW; SEIZURE; SEX DIFFERENCE;

ANIMALS; DISEASE SUSCEPTIBILITY; EPILEPSY; ESTRADIOL; FEMALE; HORMONES; HUMANS; MALE; PROGESTERONE; SEIZURES; SEX FACTORS;

EID: 84872908023     PISSN: 0018506X     EISSN: 10956867     Source Type: Journal    
DOI: 10.1016/j.yhbeh.2012.03.018     Document Type: Review

References (184)

1. Abbasi F., Krumholz A., Kittner S.J., Langenberg P. Effects of menopause on seizures in women with epilepsy. Epilepsia 1999, 40:205-210.
2. Abbott R.J., Browning M.C., Davidson D.L. Serum prolactin and cortisol concentrations after grand mal seizures. J. Neurol. Neurosurg. Psychiatry 1980, 43:163-167.
3. Aguirre C., Jayaraman A., Pike C., Baudry M. Progesterone inhibits estrogen-mediated neuroprotection against excitotoxicity by down-regulating estrogen receptor-beta. J. Neurochem. 2010, 115:1277-1287.
4. Amado D., Cavalheiro E.A. Hormonal and gestational parameters in female rats submitted to the pilocarpine model of epilepsy. Epilepsy Res. 1998, 32:266-274.
5. Backstrom T. Epileptic seizures in women related to plasma estrogen and progesterone during the menstrual cycle. Acta Neurol. Scand. 1976, 54:321-347.
6. Bandler B., Dykens J.W., Kaufman I.C., Schleifer M., Shapiro L.N. Seizures and the menstrual cycle. Am. J. Psychiatry 1957, 113:704-708.
7. Barker J.M., Galea L.A. Sex and regional differences in estradiol content in the prefrontal cortex, amygdala and hippocampus of adult male and female rats. Gen. Comp. Endocrinol. 2009, 164:77-84.
8. Bauer J. Catamenial epilepsy and menopause. Epilepsia 2001, 42:572.
9. Bauer J. Interactions between hormones and epilepsy in female patients. Epilepsia 2001, 42(Suppl. 3):20-22.
10. Bauer J., Isojarvi J.I., Herzog A.G., Reuber M., Polson D., Tauboll E., Genton P., van der Ven H., Roesing B., Luef G.J., Galimberti C.A., van Parys J., Flugel D., Bergmann A., Elger C.E. Reproductive dysfunction in women with epilepsy: recommendations for evaluation and management. J. Neurol. Neurosurg. Psychiatry 2002, 73:121-125.
11. Berzaghi Mda P., Amado D., Cavalheiro E.A. Pregnancy decreases the frequency of spontaneous recurrent seizures in rats with kainic acid lesions of the hippocampus. Epilepsy Res. 1987, 1:142-144.
12. Bhanot R., Wilkinson M. Repeated convulsions induce pseudopregnancy in the intact rat and inhibit steroid-mediated gonadotrophin secretion in the ovariectomized rat. J. Endocrinol. 1982, 95:43-48.
13. Bhanot R., Wilkinson M. Differential effects of flurothyl- and electro-convulsive shock on sexual maturation and prolactin release in the rat. Exp. Brain Res. 1984, 56:32-39.
14. Biagini G., Panuccio G., Avoli M. Neurosteroids and epilepsy. Curr. Opin. Neurol. 2010, 23:170-176.
15. Bilo L., Meo R., Valentino R., Buscaino G.A., Striano S., Nappi C. Abnormal pattern of luteinizing hormone pulsatility in women with epilepsy. Fertil. Steril. 1991, 55:705-711.
16. Bohacek J., Daniel J.M. The ability of oestradiol administration to regulate protein levels of oestrogen receptor alpha in the hippocampus and prefrontal cortex of middle-aged rats is altered following long-term ovarian hormone deprivation. J. Neuroendocrinol. 2009, 21:640-647.
17. Bohacek J., Bearl A.M., Daniel J.M. Long-term ovarian hormone deprivation alters the ability of subsequent oestradiol replacement to regulate choline acetyltransferase protein levels in the hippocampus and prefrontal cortex of middle-aged rats. J. Neuroendocrinol. 2008, 20:1023-1027.
18. Briellmann R.S., Berkovic S.F., Jackson G.D. Men may be more vulnerable to seizure-associated brain damage. Neurology 2000, 55:1479-1485.
19. Burakgazi E., Pollard J., Harden C. The effect of pregnancy on seizure control and antiepileptic drugs in women with epilepsy. Rev. Neurol. Dis. 2011, 8:16-22.
20. Burt Solorzano C.M., Beller J.P., Abshire M.Y., Collins J.S., McCartney C.R., Marshall J.C. Neuroendocrine dysfunction in polycystic ovary syndrome. Steroids 2012, 77(4):332-337.
21. Christensen J., Kjeldsen M.J., Andersen H., Friis M.L., Sidenius P. Gender differences in epilepsy. Epilepsia 2005, 46:956-960.
22. Clarke M., Gill J., Noronha M., McKinlay I. Early infantile epileptic encephalopathy with suppression burst: Ohtahara syndrome. Dev. Med. Child Neurol. 1987, 29:520-528.
23. Cramer J.A., Gordon J., Schachter S., Devinsky O. Women with epilepsy: hormonal issues from menarche through menopause. Epilepsy Behav. 2007, 11:160-178.
24. do Vale T.G., da Silva A.V., Lima D.C., de Lima E., Torres L.B., Cossa A.C., de Oliveira E.M., Cabral F.R., Cavalheiro E.A., Naffah-Mazzacoratti Mda G., Amado D. Seizures during pregnancy modify the development of hippocampal interneurons of the offspring. Epilepsy Behav. 2010, 19:20-25.
25. Drislane F.W., Coleman A.E., Schomer D.L., Ives J., Levesque L.A., Seibel M.M., Herzog A.G. Altered pulsatile secretion of luteinizing hormone in women with epilepsy. Neurology 1994, 44:306-310.
26. Duncan I.W. The effect of audiogenic seizures in rats on the adrenal weight, ascorbic acid, cholesterol, and corticosteroids. J. Biol. Chem. 1957, 229:563-568.
27. Edwards H.E., Burnham W.M., Ng M.M., Asa S., MacLusky N.J. Limbic seizures alter reproductive function in the female rat. Epilepsia 1999, 40:1370-1377.
28. Edwards H.E., MacLusky N.J., Burnham W.M. The effect of seizures and kindling on reproductive hormones in the rat. Neurosci. Biobehav. Rev. 2000, 24:753-762.
29. Engel J., Williamson P.D., Wieser H.-G. Mesial temporal lobe epilepsy. Epilepsy: a Comprehensive Textbook 1997, 2417-2426. Lippincot-Raven Publishers, Philadelphia. J. Engel, T.A. Pedley (Eds.).
30. Forsgren L., Sidenvall R., Blomquist H.K., Heijbel J. A prospective incidence study of febrile convulsions. Acta Paediatr. Scand. 1990, 79:550-557.
31. Foy M.R., Baudry M., Akopian G.K., Thompson R.F. Regulation of hippocampal synaptic plasticity by estrogen and progesterone. Vitam. Horm. 2010, 82:219-239.
32. Frye C.A. Role of androgens in epilepsy. Expert Rev. Neurother. 2006, 6:1061-1075.
33. Frye C.A. Effects and mechanisms of progestogens and androgens in ictal activity. Epilepsia 2010, 51(Suppl. 3):135-140.
34. Frye C.A., Bayon L.E. Cyclic withdrawal from endogenous and exogenous progesterone increases kainic acid and perforant pathway induced seizures. Pharmacol. Biochem. Behav. 1999, 62:315-321.
35. Frye C.A., Rhodes M.E. Estrogen-priming can enhance progesterone's anti-seizure effects in part by increasing hippocampal levels of allopregnanolone. Pharmacol. Biochem. Behav. 2005, 81:907-916.
36. Frye C.A., Walf A. Progesterone, administered before kainic acid, prevents decrements in cognitive performance in the Morris Water Maze. Dev. Neurobiol. 2011, 71:142-152.
37. Frye C.A., Manjarrez J., Camacho-Arroyo I. Infusion of 3alpha,5alpha-THP to the pontine reticular formation attenuates PTZ-induced seizures [in process citation]. Brain Res. 2000, 881:98-102.
38. Frye C.A., Rhodes M.E., Walf A., Harney J. Progesterone reduces pentylenetetrazol-induced ictal activity of wild-type mice but not those deficient in type I 5alpha-reductase. Epilepsia 2002, 43(Suppl. 5):14-17.
39. Galanopoulou A.S., Alm E.M., Velíšková J. Estradiol reduces seizure-induced hippocampal injury in ovariectomized female but not in male rats. Neurosci. Lett. 2003, 342:201-205.
40. Galli R., Luisi M., Pizzanelli C., Monteleone P., Casarosa E., Iudice A., Murri L. Circulating levels of allopregnanolone, an anticonvulsant metabolite of progesterone, in women with partial epilepsy in the postcritical phase. Epilepsia 2001, 42:216-219.
41. Gevorkyan E.S., Nazaryan K.B., Kostanyan A.A. Modifying effect of estradiol and progesterone on epileptic activity of the rat brain. Neurosci. Behav. Physiol. 1989, 19:412-415.
42. Giuliani F.A., Yunes R., Mohn C.E., Laconi M., Rettori V., Cabrera R. Allopregnanolone induces LHRH and glutamate release through NMDA receptor modulation. Endocrine 2011, 40:21-26.
43. Gordon A. Epilepsy in its relation to menstrual periods. NY Med. J. 1909, XC:733-735.
44. Gottfried-Blackmore A., Sierra A., Jellinck P.H., McEwen B.S., Bulloch K. Brain microglia express steroid-converting enzymes in the mouse. J. Steroid Biochem. Mol. Biol. 2008, 109:96-107.
45. Grosso S., Luisi S., Mostardini R., Farnetani M., Cobellis L., Morgese G., Balestri P., Petraglia F. Inter-ictal and post-ictal circulating levels of allopregnanolone, an anticonvulsant metabolite of progesterone, in epileptic children. Epilepsy Res. 2003, 54:29-34.
46. Grosso S., Luisi S., Berardi R., Mostardini R., Cordelli D.M., Morgese G., Petraglia F., Balestri P. Post-ictal circulating levels of allopregnanolone in children with partial or generalized seizures. Epilepsy Res. 2005, 63:97-102.
47. Guerrero R., Aso T., Brenner P.F., Cekan Z., Landgren B.M., Hagenfeldt K., Diczfalusy E. Studies on the pattern of circulating steroids in the normal menstrual cycle. I. Simultaneous assays of progesterone, pregnenolone, dehydroepiandrosterone, testosterone, dihydrotestosterone, androstenedione, oestradiol and oestrone. Acta Endocrinol. (Copenh) 1976, 81:133-149.
48. Harden C.L. Polycystic ovaries and polycystic ovary syndrome in epilepsy: evidence for neurogonadal disease. Epilepsy Curr. 2005, 5:142-146.
49. Harden C.L. Sexuality in men and women with epilepsy. CNS Spectr. 2006, 11:13-18.
50. Harden C.L. Hormone replacement therapy: will it affect seizure control and AED levels?. Seizure 2008, 17:176-180.
51. Harden C., MacLusky N.J. Aromatase inhibitors as add-on treatment for men with epilepsy. Expert Rev. Neurother. 2005, 5:123-127.
52. Harden C.L., Pulver M.C., Ravdin L., Jacobs A.R. The effect of menopause and perimenopause on the course of epilepsy. Epilepsia 1999, 40:1402-1407.
53. Harden C.L., Koppel B.S., Herzog A.G., Nikolov B.G., Hauser W.A. Seizure frequency is associated with age at menopause in women with epilepsy. Neurology 2003, 61:451-455.
54. Harden C.L., Herzog A.G., Nikolov B.G., Koppel B.S., Christos P.J., Fowler K., Labar D.R., Hauser W.A. Hormone replacement therapy in women with epilepsy: a randomized, double-blind, placebo-controlled study. Epilepsia 2006, 47:1447-1451.
55. Harden C.L., Nikolov B.G., Kandula P., Labar D.R., Pannullo S. Effect of levetiracetam on testosterone levels in male patients. Epilepsia 2010, 51:2348-2351.
56. Hauser W.A., Annegers J.F., Kurland L.T. Prevalence of epilepsy in Rochester, Minnesota: 1940-1980. Epilepsia 1991, 32:429-445.
57. Herzog A.G. Polycystic ovarian syndrome in women with epilepsy: epileptic or iatrogenic?. Ann. Neurol. 1996, 39:559-560.
58. Herzog A.G. Psychoneuroendocrine aspects of temporolimbic epilepsy. Part II: epilepsy and reproductive steroids. Psychosomatics 1999, 40:102-108.
59. Herzog A.G. Hormonal therapies: progesterone. Neurotherapeutics 2009, 6:383-391.
60. Herzog A.G., Frye C.A. Seizure exacerbation associated with inhibition of progesterone metabolism. Ann. Neurol. 2003, 53:390-391.
61. Herzog A.G., Seibel M.M., Schomer D., Vaitukaitis J., Geschwind N. Temporal lobe epilepsy: an extrahypothalamic pathogenesis for polycystic ovarian syndrome?. Neurology 1984, 34:1389-1393.
62. Herzog A.G., Seibel M.M., Schomer D.L., Vaitukaitis J.L., Geschwind N. Reproductive endocrine disorders in men with partial seizures of temporal lobe origin. Arch. Neurol. 1986, 43:347-350.
63. Herzog A.G., Seibel M.M., Schomer D.L., Vaitukaitis J.L., Geschwind N. Reproductive endocrine disorders in women with partial seizures of temporal lobe origin. Arch. Neurol. 1986, 43:341-346.
64. Herzog A.G., Drislane F.W., Schomer D.L., Levesque L.A., Ives J., Blume H.W., Dubuisson D., Cosgrove G.R. Abnormal pulsatile secretion of luteinizing hormone in men with epilepsy: relationship to laterality and nature of paroxysmal discharges. Neurology 1990, 40:1557-1561.
65. Herzog A.G., Klein P., Ransil B.J. Three patterns of catamenial epilepsy. Epilepsia 1997, 38:1082-1088.
66. Hoffman G.E., Moore N., Fiskum G., Murphy A.Z. Ovarian steroid modulation of seizure severity and hippocampal cell death after kainic acid treatment. Exp. Neurol. 2003, 182:124-134.
67. Jacono J.J., Robertson J.M.D. The effects of estrogen, progesterone, and ionized calcium on seizures during the menstrual cycle of epileptic women. Epilepsia 1987, 28:571-577.
68. Janszky J., Schulz R., Janszky I., Ebner A. Medial temporal lobe epilepsy: gender differences. J. Neurol. Neurosurg. Psychiatry 2004, 75:773-775.
69. Jensen E.V., Jacobson H.I., Walf A.A., Frye C.A. Estrogen action: a historic perspective on the implications of considering alternative approaches. Physiol. Behav. 2010, 99:151-162.
70. Joshi S., Rajasekaran K., Kapur J. GABAergic transmission in temporal lobe epilepsy: the role of neurosteroids. Exp. Neurol. 2011.
71. Kalinin V.V., Zheleznova E.V. Chronology and evolution of temporal lobe epilepsy and endocrine reproductive dysfunction in women: relationships to side of focus and catameniality. Epilepsy Behav. 2007, 11:185-191.
72. Kalkbrenner K.A., Standley C.A. Estrogen modulation of NMDA-induced seizures in ovariectomized and non-ovariectomized rats. Brain Res. 2003, 964:244-249.
73. Klein P., Serje A., Pezzullo J.C. Premature ovarian failure in women with epilepsy. Epilepsia 2001, 42:1584-1589.
74. Klein P., van Passel-Clark L.M., Pezzullo J.C. Onset of epilepsy at the time of menarche. Neurology 2003, 60:495-497.
75. Konkle A.T., McCarthy M.M. Developmental time course of estradiol, testosterone, and dihydrotestosterone levels in discrete regions of male and female rat brain. Endocrinology 2011, 152:223-235.
76. Koonce C.J., Walf A.A., Frye C.A. Type 1 5alpha-reductase may be required for estrous cycle changes in affective behaviors of female mice. Behav. Brain Res. 2012, 226:376-380.
77. Laidlaw J. Catamenial epilepsy. Lancet 1956, 2:1235-1237.
78. Lambert J.J., Cooper M.A., Simmons R.D., Weir C.J., Belelli D. Neurosteroids: endogenous allosteric modulators of GABA(A) receptors. Psychoneuroendocrinology 2009, 34(Suppl. 1):S48-S58.
79. Larner A.J. Epileptic seizures in AD patients. Neuromolecular Med. 2010, 12:71-77.
80. Lavaque E., Sierra A., Azcoitia I., Garcia-Segura L.M. Steroidogenic acute regulatory protein in the brain. Neuroscience 2006, 138:741-747.
81. Lawrence C., Martin B.S., Sun C., Williamson J., Kapur J. Endogenous neurosteroid synthesis modulates seizure frequency. Ann. Neurol. 2010, 67:689-693.
82. Ledoux V.A., Smejkalova T., May R.M., Cooke B.M., Woolley C.S. Estradiol facilitates the release of neuropeptide Y to suppress hippocampus-dependent seizures. J. Neurosci. 2009, 29:1457-1468.
83. Lima D.C., Vale T.G., Arganaraz G.A., Varella P.P., Frussa-Filho R., Cavalheiro E.A., Naffah-Mazzacoratti Mda G., Amado D. Behavioral evaluation of adult rats exposed in utero to maternal epileptic seizures. Epilepsy Behav. 2010, 18:45-49.
84. Lonsdale D., Nylen K., McIntyre Burnham W. The anticonvulsant effects of progesterone and its metabolites on amygdala-kindled seizures in male rats. Brain Res. 2006, 1101:110-116.
85. Luchetti S., Huitinga I., Swaab D.F. Neurosteroid and GABA-A receptor alterations in Alzheimer's disease, Parkinson's disease and multiple sclerosis. Neuroscience 2011, 191:6-21.
86. Lukkes J.L., Engelman G.H., Zelin N.S., Hale M.W., Lowry C.A. Post-weaning social isolation of female rats, anxiety-related behavior, and serotonergic systems. Brain Res. 2012, 1443:1-17.
87. Luthvigsson P., Olafsson E., Sigurthardottir S., Hauser W.A. Epidemiologic features of infantile spasms in Iceland. Epilepsia 1994, 35:802-805.
88. Majewska M.D. Neurosteroids: endogenous bimodal modulators of the GABAA receptor. Mechanism of action and physiological significance. Prog. Neurobiol. 1992, 38:379-395.
89. Mathern G.W., Babb T.L., Leite J.P., Pretorius K., Yeoman K.M., Kuhlman P.A. The pathogenic and progressive features of chronic human hippocampal epilepsy. Epilepsy Res. 1996, 26:151-161.
90. McCarthy M.M., Arnold A.P. Reframing sexual differentiation of the brain. Nat. Neurosci. 2011, 14:677-683.
91. McEwen B. Estrogen actions throughout the brain. Recent Prog. Horm. Res. 2002, 57:357-384.
92. McHugh J.C., Delanty N. Epidemiology and classification of epilepsy: gender comparisons. Int. Rev. Neurobiol. 2008, 83:11-26.
93. Mejias-Aponte C.A., Jimenez-Rivera C.A., Segarra A.C. Sex differences in models of temporal lobe epilepsy: role of testosterone. Brain Res. 2002, 944:210-218.
94. Miranda P., Williams C.L., Einstein G. Granule cells in aging rats are sexually dimorphic in their response to estradiol. J. Neurosci. 1999, 19:3316-3325.
95. Morali G., Montes P., Gonzalez-Burgos I., Velazquez-Zamora D.A., Cervantes M. Cytoarchitectural characteristics of hippocampal CA1 pyramidal neurons of rats, four months after global cerebral ischemia and progesterone treatment. Restor. Neurol. Neurosci. 2012, 30:1-8.
96. Moran M.H., Smith S.S. Progesterone withdrawal I: pro-convulsant effects. Brain Res. 1998, 807:84-90.
97. Morrell M.J. Hormones and epilepsy through the lifetime. Epilepsia 1992, 33:S49-S61.
98. Morrell M.J. Antiepileptic drugs, seizures, and birth defects. Int. Pediatr. 1995, 10:58-65.
99. Morrell M.J. Hormones, reproductive health, and epilepsy. The Treatment of Epilepsy: Principles and Practice 1997, 179-187. Williams & Wilkins, Baltimore. E. Wyllie (Ed.).
100. Morrell M.J. Pregnancy and antiepileptic drugs. Curr. Neurol. Neurosci. Rep. 2001, 1:359-360.
101. Moura P.J., Petersen S.L. Estradiol acts through nuclear- and membrane-initiated mechanisms to maintain a balance between GABAergic and glutamatergic signaling in the brain: implications for hormone replacement therapy. Rev. Neurosci. 2010, 21:363-380.
102. Mouridsen S.E. The Landau-Kleffner Syndrome: a review. Eur. Child Adolesc. Psychiatry 1995, 4:223-228.
103. Nakamura N.H., McEwen B.S. Changes in interneuronal phenotypes regulated by estradiol in the adult rat hippocampus: a potential role for neuropeptide Y. Neuroscience 2005, 136:357-369.
104. Nakamura N.H., Rosell D.R., Akama K.T., McEwen B.S. Estrogen and ovariectomy regulate mRNA and protein of glutamic acid decarboxylases and cation-chloride cotransporters in the adult rat hippocampus. Neuroendocrinology 2004, 80:308-323.
105. Nakamura N.H., Rosell D.R., Akama K.T., McEwen B.S. Estrogen and ovariectomy regulate mRNA and protein of glutamic acid decarboxylases and cation-chloride cotransporters in the adult rat hippocampus. Neuroendocrinology 2005, 80:308-323.
106. Neal-Perry G.S., Zeevalk G.D., Santoro N.F., Etgen A.M. Attenuation of preoptic area glutamate release correlates with reduced luteinizing hormone secretion in middle-aged female rats. Endocrinology 2005, 146:4331-4339.
107. Newmark M.E., Penry J.K. Catamenial epilepsy: a review. Epilepsia 1980, 21:281-300.
108. Nicoletti F., Speciale C., Sortino M.A., Summa G., Caruso G., Patti F., Canonico P.L. Comparative effects of estradiol benzoate, the antiestrogen clomiphene citrate, and the progestin medroxyprogesterone acetate on kainic acid-induced seizures in male and female rats. Epilepsia 1985, 26:252-257.
109. Nordli D.R. Idiopathic generalized epilepsies recognized by the International League Against Epilepsy. Epilepsia 2005, 46(Suppl. 9):48-56.
110. Novaes, G.F., Amado, D., Scorza, F.A., Cysneiros, R.M., in press. Social behavior impairment in offspring exposed to maternal seizures in utero. J. Neural Transm.
111. Ortiz G.G., Sanchez-Ruiz Y., Tan D.X., Reiter R.J., Benitez-King G., Beas-Zarate C. Melatonin, vitamin E, and estrogen reduce damage induced by kainic acid in the hippocampus: potassium-stimulated GABA release. J. Pineal Res. 2001, 31:62-67.
112. Osborne D.M., Frye C.A. Estrogen increases latencies to seizures and levels of 5alpha-pregnan-3alpha-ol-20-one in hippocampus of wild-type, but not 5alpha-reductase knockout, mice. Epilepsy Behav. 2009, 16:411-414.
113. Pack A.M. Treatment of epilepsy to optimize bone health. Curr. Treat. Options. Neurol. 2011, 13:346-354.
114. Peebles C.T., McAuley J.W., Moore J.L., Malone H.J., Reeves A.L. Hormone replacement therapy in a postmenopausal woman with epilepsy. Ann. Pharmacother. 2000, 34:1028-1031.
115. Pennell P.B. Pregnancy in women who have epilepsy. Neurol. Clin. 2004, 22:799-820.
116. Pericic D., Bujas M. Sex differences in bicuculline-induced convulsions: interaction with stress and ligands of benzodiazepine binding sites. Brain Res. 1997, 752:279-284.
117. Pericic D., Bujas M. Sex differences in the response to GABA antagonists depend on the route of drug administration. Exp. Brain Res. 1997, 115:187-190.
118. Pericic D., Manev H., Lakic N. Sex differences in the response of rats to drugs affecting GABAergic transmission. Life Sci. 1985, 36:541-547.
119. Pericic D., Manev H., Geber J. Sex-related differences in the response of mice, rats and cats to the administration of picrotoxin. Life Sci. 1986, 38:905-913.
120. Quigg M., Kiely J.M., Shneker B., Veldhuis J.D., Bertram E.H. Interictal and postictal alterations of pulsatile secretions of luteinizing hormone in temporal lobe epilepsy in men. Ann. Neurol. 2002, 51:559-566.
121. Quigg M., Smithson S.D., Fowler K.M., Sursal T., Herzog A.G. Laterality and location influence catamenial seizure expression in women with partial epilepsy. Neurology 2009, 73:223-227.
122. Raffo E., de Vasconcelos A.P., Boehrer A., Desor D., Nehlig A. Neurobehavioral maturation of offspring from epileptic dams: study in the rat lithium-pilocarpine model. Exp. Neurol. 2009, 219:414-423.
123. Reddy D.S. The role of neurosteroids in the pathophysiology and treatment of catamenial epilepsy. Epilepsy Res. 2009, 85:1-30.
124. Reddy D.S. Neurosteroids: endogenous role in the human brain and therapeutic potentials. Prog. Brain Res. 2010, 186:113-137.
125. Reddy D.S., Mohan A. Development and persistence of limbic epileptogenesis are impaired in mice lacking progesterone receptors. J. Neurosci. 2011, 31:650-658.
126. Reddy D.S., Rogawski M.A. Enhanced anticonvulsant activity of neuroactive steroids in a rat model of catamenial epilepsy. Epilepsia 2001, 42:337-344.
127. Reddy D.S., Rogawski M.A. Neurosteroid replacement therapy for catamenial epilepsy. Neurotherapeutics 2009, 6:392-401.
128. Redei E., Freeman E.W. Daily plasma estradiol and progesterone levels over the menstrual cycle and their relation to premenstrual symptoms. Psychoneuroendocrinology 1995, 20:259-267.
129. Reibel S., Andre V., Chassagnon S., Andre G., Marescaux C., Nehlig A., Depaulis A. Neuroprotective effects of chronic estradiol benzoate treatment on hippocampal cell loss induced by status epilepticus in the female rat. Neurosci. Lett. 2000, 281:79-82.
130. Ryan S.G., Chance P.F., Zou C.H., Spinner N.B., Golden J.A., Smietana S. Epilepsy and mental retardation limited to females: an X-linked dominant disorder with male sparing. Nat. Genet. 1997, 17:92-95.
131. Sachs M., Pape H.C., Speckmann E.J., Gorji A. The effect of estrogen and progesterone on spreading depression in rat neocortical tissues. Neurobiol. Dis. 2007, 25:27-34.
132. Savic I., Engel J. Sex differences in patients with mesial temporal lobe epilepsy. J. Neurol. Neurosurg. Psychiatry 1998, 65:910-912.
133. Scharfman H.E., MacLusky N.J. The influence of gonadal hormones on neuronal excitability, seizures, and epilepsy in the female. Epilepsia 2006, 47:1423-1440.
134. Scharfman H.E., Goodman J.H., Rigoulot M.A., Berger R.E., Walling S.G., Mercurio T.C., Stormes K., Maclusky N.J. Seizure susceptibility in intact and ovariectomized female rats treated with the convulsant pilocarpine. Exp. Neurol. 2005, 196:73-86.
135. Scharfman H.E., Kim M., Hintz T.M., MacLusky N.J. Seizures and reproductive function: insights from female rats with epilepsy. Ann. Neurol. 2008, 64:687-697.
136. Scharfman H.E., Malthankar-Phatak G.H., Friedman D., Pearce P., McCloskey D.P., Harden C.L., Maclusky N.J. A rat model of epilepsy in women: a tool to study physiological interactions between endocrine systems and seizures. Endocrinology 2009, 150:4437-4442.
137. Schmidt D. The effect of pregnancy on the natural history of epilepsy: review of the literature. Epilepsy, Pregnancy and Child 1982, 3-14. Raven Press, New York. D. Janz, M. Dam, A. Richens, L. Bossi (Eds.).
138. Schwartz-Giblin S., Korotzer A., Pfaff D.W. Steroid hormone effects on picrotoxin-induced seizures in female and male rats. Brain Res. 1989, 476:240-247.
139. Scott E., Zhang Q.G., Wang R., Vadlamudi R., Brann D. Estrogen neuroprotection and the critical period hypothesis. Front. Neuroendocrinol. 2012, 33(1):85-104.
140. Sierra A., Azcoitia I., Garcia-Segura L. Endogenous estrogen formation is neuroprotective in model of cerebellar ataxia. Endocrine 2003, 21:43-51.
141. Sierra A., Gottfried-Blackmore A., Milner T.A., McEwen B.S., Bulloch K. Steroid hormone receptor expression and function in microglia. Glia 2008, 56:659-674.
142. Sivaraaman K., Mintzer S. Hormonal consequences of epilepsy and its treatment in men. Curr. Opin. Endocrinol. Diabetes Obes. 2011, 18:204-209.
143. Šlamberová R., Vathy I. Estrogen differentially alters NMDA- and kainate-induced seizures in prenatally morphine- and saline-exposed adult female rats. Pharmacol. Biochem. Behav. 2000, 67:501-505.
144. Šlamberová R., Schindler C.J., Vathy I. Impact of maternal morphine and saline injections on behavioral responses to a cold water stressor in adult male and female progeny. Physiol. Behav. 2002, 75:723-732.
145. Smith M.S., Freeman M.E., Neill J.D. The control of progesterone secretion during the estrous cycle and early pseudopregnancy in the rat: prolactin, gonadotropin and steroid levels associated with rescue of the corpus luteum of pseudopregnancy. Endocrinology 1975, 96:219-226.
146. Smith S.S., Shen H., Gong Q.H., Zhou X. Neurosteroid regulation of GABA(A) receptors: focus on the alpha4 and delta subunits. Pharmacol. Ther. 2007, 116:58-76.
147. Spencer J.L., Waters E.M., Romeo R.D., Wood G.E., Milner T.A., McEwen B.S. Uncovering the mechanisms of estrogen effects on hippocampal function. Front. Neuroendocrinol. 2008, 29:219-237.
148. Sperk G., Hamilton T., Colmers W.F. Neuropeptide Y in the dentate gyrus. Prog. Brain Res. 2007, 163:285-297.
149. Stoffel-Wagner B., Beyenburg S., Watzka M., Blumcke I., Bauer J., Schramm J., Bidlingmaier F., Elger C.E. Expression of 5alpha-reductase and 3alpha-hydroxisteroid oxidoreductase in the hippocampus of patients with chronic temporal lobe epilepsy. Epilepsia 2000, 41:140-147.
150. Tauboll E., Roste L.S., Svalheim S., Gjerstad L. Disorders of reproduction in epilepsy-what can we learn from animal studies?. Seizure 2008, 17:120-126.
151. Taylor D.C. Differential rates of cerebral maturation between sexes and between hemispheres: evidence for epilepsy. Lancet 1969, 2:140-142.
152. Teyler T.J., Vardaris R.M., Lewis D., Rawitch A.B. Gonadal steroids: effects on excitability of hippocampal pyramidal cells. Science 1980, 209:1017-1019.
153. Thielen R.J., McBride W.J., Lumeng L., Li T.K. Housing conditions alter GABAA receptor of alcohol-preferring and -nonpreferring rats. Pharmacol. Biochem. Behav. 1993, 46:723-727.
154. Thomas J. Gender difference in susceptibility to picrotoxin-induced seizures is seizure- and stimulation-dependent. Brain Res. Bull. 1990, 24:7-10.
155. Tominaga K., Yamauchi A., Shuto H., Niizeki M., Makino K., Oishi R., Kataoka Y. Ovariectomy aggravates convulsions and hippocampal gamma-aminobutyric acid inhibition induced by cyclosporin A in rats. Eur. J. Pharmacol. 2001, 430:243-249.
156. Tomson T., Battino D. Pregnancy and epilepsy: what should we tell our patients?. J. Neurol. 2009, 256:856-862.
157. Tomson T., Battino D. Teratogenic effects of antiepileptic medications. Neurol. Clin. 2009, 27:993-1002.
158. Tomson T., Battino D. Antiepileptic treatment in pregnant women: morphological and behavioural effects. Handb. Exp. Pharmacol. 2011, 205:295-315.
159. Toran-Allerand C.D. Minireview: a plethora of estrogen receptors in the brain: where will it end?. Endocrinology 2004, 145:1069-1074.
160. Trevathan E., Murphy C.C., Yeargin-Allsopp M. Prevalence and descriptive epidemiology of Lennox-Gastaut syndrome among Atlanta children. Epilepsia 1997, 38:1283-1288.
161. Tsuboi T. Epidemiology of febrile and afebrile convulsions in children in Japan. Neurology 1984, 34:175-181.
162. Turkmen S., Backstrom T., Wahlstrom G., Andreen L., Johansson I.M. Tolerance to allopregnanolone with focus on the GABA-A receptor. Br. J. Pharmacol. 2011, 162:311-327.
163. Veiga S., Melcangi R.C., Doncarlos L.L., Garcia-Segura L.M., Azcoitia I. Sex hormones and brain aging. Exp. Gerontol. 2004, 39:1623-1631.
164. Velíšek L., Velíšková J., Etgen A.M., Stanton P.K., Moshé S.L. Region-specific modulation of limbic seizure susceptibility by ovarian steroids. Brain Res. 1999, 842:132-138.
165. Velíšková J. Behavioral characterization of seizures in rats. Models of Seizures and Epilepsy 2006, 601-611. Elsevier, San Diego. A. Pitkanen, P.A. Schwartzkroin, S.L. Moshé (Eds.).
166. Velíšková J. The role of estrogens in seizures and epilepsy: the bad guys or the good guys?. Neuroscience 2006, 138:837-844.
167. Velíšková J. Estrogens and epilepsy: why are we so excited?. Neuroscientist 2007, 13:77-88.
168. Velíšková J. Sex differences in seizure sensitivity. Encyclopedia of Basic Epilepsy Research 2009, 523-526. Academic Press, Oxford. P.A. Schwartzkroin (Ed.).
169. Velíšková J., Moshé S.L. Update on the role of substantia nigra pars reticulata in the regulation of seizures. Epilepsy Curr. 2006, 6:83-87.
170. Velíšková J., Velíšek L. β-Estradiol increases dentate gyrus inhibition in female rats via augmentation of hilar neuropeptide Y. J. Neurosci. 2007, 27:6054-6063.
171. Velíšková J., Velíšek L., Galanopoulou A.S., Sperber E.F. Neuroprotective effects of estrogens on hippocampal cells in adult female rats after status epilepticus. Epilepsia 2000, 41:S30-S35.
172. Velíšková J., De Jesus G., Kaur R., Velíšek L. Females, their estrogens, and seizures. Epilepsia 2010, 51(Suppl. 3):141-144.
173. Vezzani A., French J., Bartfai T., Baram T.Z. The role of inflammation in epilepsy. Nat. Rev. Neurol. 2011, 7:31-40.
174. Vincent A., Crino P.B. Systemic and neurologic autoimmune disorders associated with seizures or epilepsy. Epilepsia 2011, 52(Suppl. 3):12-17.
175. Weiland N.G. Glutamic acid decarboxylase messenger ribonucleic acid is regulated by estradiol and progesterone in the hippocampus. Endocrinology 1992, 131:2697-2702.
176. Weintraub A., Singaravelu J., Bhatnagar S. Enduring and sex-specific effects of adolescent social isolation in rats on adult stress reactivity. Brain Res. 2010, 1343:83-92.
177. Wheless J.W., Kim H.L. Adolescent seizures and epilepsy syndromes. Epilepsia 2002, 43(Suppl. 3):33-52.
178. Wilkinson M., Bhanot R., Pincock J.A., Donald L. Flurothyl-induced convulsions delay the onset of sexual maturation in the female rat. J. Endocrinol. 1982, 95:37-41.
179. Woolley C.S. Effects of estrogen in the CNS. Curr. Opin. Neurobiol. 1999, 9:349-354.
180. Woolley C.S. Estradiol facilitates kainic acid-induced, but not flurothyl-induced, behavioral seizure activity in adult female rats. Epilepsia 2000, 41:510-515.
181. Woolley C.S. Acute effects of estrogen on neuronal physiology. Annu. Rev. Pharmacol. Toxicol. 2007, 47:657-680.
182. Woolley C.S., McEwen B.S. Roles of estradiol and progesterone in regulation of hippocampal dendritic spine density during the estrous cycle in the rat. J. Comp. Neurol. 1993, 336:293-306.
183. Woolley C.S., McEwen B.S. Estradiol regulates hippocampal dendritic spine density via an N-methyl-d-aspartate receptor-dependent mechanism. J. Neurosci. 1994, 14:7680-7687.
184. Yague J.G., Azcoitia I., DeFelipe J., Garcia-Segura L.M., Munoz A. Aromatase expression in the normal and epileptic human hippocampus. Brain Res. 2010, 1315:41-52.