Sex differences in the neurobiology of epilepsy: A preclinical perspective

Neurobiology of Disease

Volumn 72, Issue PB, 2014, Pages 180-192

  Scharfman, Helen E ^a   MacLusky, Neil J ^b  

^a NEW YORK UNIVERSITY MEDICAL CENTER   (United States)

^b UNIVERSITY OF GUELPH   (Canada)

Author keywords

Androgen; Epileptogenesis; Estradiol; Estrogen; Estrous cycle; Gender; Menstrual cycle; Neurosteroid; Progesterone; Seizure; Temporal lobe epilepsy

Indexed keywords

4 AMINOBUTYRIC ACID A RECEPTOR; ANDROGEN; ANDROSTANOLONE; BRAIN DERIVED NEUROTROPHIC FACTOR; ESTRADIOL; GESTAGEN; KAINIC ACID; MUSCARINIC RECEPTOR; NEURON SPECIFIC NUCLEAR PROTEIN; NEUROPEPTIDE Y; PILOCARPINE; PROGESTERONE; RALOXIFENE; TESTOSTERONE; ANTICONVULSIVE AGENT;

ABSENCE; ACQUIRED EPILEPSY; ADULT ANIMAL; BEHAVIORAL STRESS; BRAIN INJURY; DISEASE PREDISPOSITION; DISEASE SEVERITY; EPILEPSY; EPILEPTIC STATE; EPILEPTOGENESIS; ESTRUS CYCLE; EXPERIMENTAL MOUSE; EXPERIMENTAL RAT; EXPERIMENTAL STUDY; GENERALIZED EPILEPSY; GENETIC RISK; HIGH RISK POPULATION; HIPPOCAMPAL CA3 REGION; HORMONE ACTION; HUMAN; IDIOPATHIC GENERALIZED EPILEPSY; MEDICAL RESEARCH; MEDICAL TERMINOLOGY; MENSTRUAL CYCLE; NERVE EXCITABILITY; NEUROBIOLOGY; NEUROPATHOLOGY; NEUROPROTECTION; NONHUMAN; PROTEIN EXPRESSION; REVIEW; SEIZURE; SEIZURE, EPILEPSY AND CONVULSION; SEX DIFFERENCE; SOCIAL ISOLATION; SOCIAL STRESS; ANIMAL; DRUG SCREENING; FEMALE; MALE; METABOLISM; MOUSE; PATHOLOGY; RAT; SEXUAL DEVELOPMENT;

ANIMALS; ANTICONVULSANTS; DRUG EVALUATION, PRECLINICAL; EPILEPSY; FEMALE; HUMANS; MALE; MICE; NEUROBIOLOGY; RATS; SEX CHARACTERISTICS;

EID: 84909638419     PISSN: 09699961     EISSN: 1095953X     Source Type: Journal    
DOI: 10.1016/j.nbd.2014.07.004     Document Type: Review

References (114)

1. Akman O., Moshé S.L., Galanopoulou A.S. Sex-specific consequences of early life seizures. Neurobiol. Dis. 2014, 72:153-166.
2. 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.
3. Barha C.K., Galea L.A. Influence of different estrogens on neuroplasticity and cognition in the hippocampus. Biochim. Biophys. Acta 2010, 1800:1056-1067.
4. Bath K.G., Schilit A., Lee F.S. Stress effects on BDNF expression: effects of age, sex, and form of stress. Neuroscience 2013, 239:149-156.
5. Becker J.B., Arnold A.P., Berkley K.J., Blaustein J.D., Eckel L.A., Hampson E., Herman J.P., Marts S., Sadee W., Steiner M., Taylor J., Young E. Strategies and methods for research on sex differences in brain and behavior. Endocrinology 2005, 146:1650-1673.
6. Benamer H.T., Grosset D.G. A systematic review of the epidemiology of epilepsy in Arab countries. Epilepsia 2009, 50:2301-2304.
7. Bender C., Rassetto M., de Olmos J.S., Lorenzo A. Involvement of AMPA/kainate-excitotoxicity in MK-801-induced neuronal death in the retrosplenial cortex. Neuroscience 2010, 169:720-732.
8. Blaustein J.D. An estrogen by any other name. Endocrinology 2008, 149:2697-2698.
9. Bondar G., Kuo J., Hamid N., Micevych P. Estradiol-induced estrogen receptor-α trafficking. J. Neurosci. 2009, 29:15323-15330.
10. Briggs S.W., Galanopoulou A.S. Altered GABA signaling in early life epilepsies. Neural. Plast 2011, 10.1155/2011/527605.
11. Brinton R.D. Estrogen regulation of glucose metabolism and mitochondrial function: therapeutic implications for prevention of Alzheimer's disease. Adv. Drug Deliv. Rev. 2008, 60:1504-1511.
12. Budde T., Caputi L., Kanvshkova T., Staak R., Abrahamczik C., Munsch T., Pape H.C. Impaired regulation of thalamic pacemaker channels through an imbalance of subunit expression in absence epilepsy. J. Neurosci. 2005, 25:9871-9882.
13. Burneo J.G., Tellez-Zenteno J., Wiebe S. Understanding the burden of epilepsy in Latin America: a systematic review of its prevalence and incidence. Epilepsy Res. 2005, 66:63-74.
14. Cardoso C.C., Ricardo V.P., Frussa-Filho R., Porto C.S., Abdalla F.M. Effects of 17β-estradiol on expression of muscarinic acetylcholine receptor subtypes and estrogen receptor a in rat hippocampus. Eur. J. Pharmacol. 2010, 634:192-200.
15. Casetta I., Pugliatti M., Faggioli R., Cesnik E., Simioni V., Bencivelli D., De Carlo L., Granieri E. Incidence of childhood and adolescence epilepsy: a community-based prospective study in the province of Ferrara and in Copparo, Italy, 1996-2005. Eur. J. Neurol. 2012, 19:312-316.
16. Celikkas E., Erdinc O.O., Metintas S., Fidan H.S., Arikan I., Kalyoncu C., Ozdemir G. Incidence of epilepsy in a defined area of Central Anatolia, Turkey, after 15years of age. Neuroepidemiology 2010, 35:221-225.
17. Christensen J., Kjeldsen M.J., Andersen H., Friis M.L., Sidenius P. Gender differences in epilepsy. Epilepsia 2005, 46:956-960.
18. Coenen A.M., Van Luijtelaar E.L. The WAG/Rij rat model for absence epilepsy: age and sex factors. Epilepsy Res. 1987, 1:297-301.
19. de Lacalle S. Estrogen effects on neuronal morphology. Endocrine 2006, 29:185-190.
20. de Olmos S., Bueno A., Bender C., Lorenzo A., de Olmos J. Sex differences and influence of gonadal hormones on MK-801-induced neuronal degeneration in the granular retrosplenial cortex of the rat. Brain Struct. Funct. 2008, 213:229-238.
21. Desgent S., Duss S., Sanon N.T., Lema P., Levesque M., Hebert D., Rebillard R.M., Bibeau K., Brochu M., Carmant L. Early-life stress is associated with gender-based vulnerability to epileptogenesis in rat pups. PLoS ONE 2012, 7:e42622.
22. Dominguez R., Micevych P. Estradiol rapidly regulates membrane estrogen receptor α levels in hypothalamic neurons. J. Neurosci. 2010, 30:12589-12596.
23. Duffy A.M., Schaner M.J., Wu S.H., Staniszewski A., Kumar A., Arevalo J.C., Arancio O., Chao M.V., Scharfman H.E. A selective role for ARMS/Kidins220 scaffold protein in spatial memory and trophic support of entorhinal and frontal cortical neurons. Exp. Neurol. 2011, 229:409-420.
24. 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.
25. Edwards H.E., Dortok D., Tam J., Won D., Burnham W.M. Prenatal stress alters seizure thresholds and the development of kindled seizures in infant and adult rats. Horm. Behav. 2002, 42:437-447.
26. Feinstein I., Kritzer M.F. Acute NMDA hypofunction induced by MK-801 evokes sex-specific changes in behaviors observed in open-field testing in adult male and proestrus female rats. Neuroscience 2013, 228:200-214.
27. A receptor modulation by neurosteroids in models of temporal lobe epilepsies. Epilepsia 2012, 53(Suppl. 9):89-101.
28. Fester L., Prange-Kiel J., Jarry H., Rune G.M. Estrogen synthesis in the hippocampus. Cell Tissue Res. 2011, 345:285-294.
29. Filardo E.J., Thomas P. Minireview: G protein-coupled estrogen receptor-1, GPER-1: its mechanism of action and role in female reproductive cancer, renal and vascular physiology. Endocrinology 2012, 153:2953-2962.
30. Foy M.R., Baudry M., Diaz Brinton R., Thompson R.F. Estrogen and hippocampal plasticity in rodent models. J. Alzheimers Dis. 2008, 15:589-603.
31. Freeman M.E. The neuroendocrine control of the ovarian cycle in the rat. The Physiology of Reproduction 2006, 2327-2388. Academic Press, New York. E. Knobil, J. Nieill (Eds.).
32. Fregly M.J. Attenuation of pilocarpine-induced drinking by chronic treatment with estrogens. Proc. Soc. Exp. Biol. Med. 1980, 164:178-183.
33. Frye C.A. Effects and mechanisms of progestogens and androgens in ictal activity. Epilepsia 2010, 51(Suppl. 3):135-140.
34. Galanopoulou A.S. GABA(A) receptors in normal development and seizures: friends or foes?. Curr. Neuropharmacol. 2008, 6:1-20.
35. Galanopoulou A.S. Sexually dimorphic expression of KCC2 and GABA function. Epilepsy Res. 2008, 80:99-113.
36. Giorgi F.S., Galanopoulou A.S., Moshé S.L. Sex dimorphism in seizure-controlling networks. Neurobiol. Dis. 2014, 72:144-152.
37. Gottmann K., Mittmann T., Lessmann V. BDNF signaling in the formation, maturation and plasticity of glutamatergic and GABAergic synapses. Exp. Brain Res. 2009, 199:203-234.
38. Grabenstatter H.L., Russek S.J., Brooks-Kayal A.R. Molecular pathways controlling inhibitory receptor expression. Epilepsia 2012, 53(Suppl. 9):71-78.
39. Graham F.A., Jeavons P.M. Photosensitive Epilepsy 1999, Wiley, New York.
40. Handa R.J., Pak T.R., Kudwa A.E., Lund T.D., Hinds L. An alternate pathway for androgen regulation of brain function: activation of estrogen receptor beta by the metabolite of dihydrotestosterone, 5α-androstane-3β,17β-diol. Horm. Behav. 2008, 53:741-752.
41. Harden C., MacLusky N.J. Aromatase inhibitors as add-on treatment for men with epilepsy. Expert. Rev. Neurother. 2005, 5:123-127.
42. Herink J. Atropine-induced convulsions in the septohippocampal system. I. Effects of cannula position and sex. Acta Med. (Hradec Kralove) 1998, 41:131-134.
43. Ibarra M., Vazquez M., Fagiolino P., Derendorf H. Sex related differences on valproic acid pharmacokinetics after oral single dose. J. Pharmacokinet. Pharmacodyn. 2013, 40:479-486.
44. Janszky J., Schulz R., Janszky I., Ebner A. Medial temporal lobe epilepsy: gender differences. J. Neurol. Neurosurg. Psychiatry 2004, 75:773-775.
45. Joshi S., Rajasekaran K., Kapur J. Gabaergic transmission in temporal lobe epilepsy: the role of neurosteroids. Exp. Neurol. 2013, 244:36-42.
46. Kelly M.J., Zhang C., Qiu J., Ronnekleiv O.K. Pacemaking kisspeptin neurons. Exp. Physiol. 2013, 97:1535-1543.
47. Kight K.E., McCarthy M.M. Using sex differences in the developing brain to identify nodes of influence for seizure susceptibility and epileptogenesis. Neurobiol. Dis. 2014, 72:136-143.
48. Kim D.W., Lee S.Y., Chung S.E., Cheong H.K., Jung K.Y., Korean Epilepsy S. Clinical characteristics of patients with treated epilepsy in Korea: a nationwide epidemiologic study. Epilepsia 2014, 55:67-75.
49. 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.
50. A receptor subunits in rat somatosensory thalamus and cortex in an absence epilepsy model. Neurobiol. Dis. 2007, 25:623-630.
51. Lonsdale D. Effect of thiamine tetrahydrofurfuryl disulfide on audiogenic seizures in DBA/2J mice. Dev. Pharmacol. Ther. 1982, 4:28-36.
52. Luine V., Attalla S., Mohan G., Costa A., Frankfurt M. Dietary phytoestrogens enhance spatial memory and spine density in the hippocampus and prefrontal cortex of ovariectomized rats. Brain Res. 2006, 1126:183-187.
53. Maguire J.L., Stell B.M., Rafizadeh M., Mody I. Ovarian cycle-linked changes in GABA(A) receptors mediating tonic inhibition alter seizure susceptibility and anxiety. Nat. Neurosci. 2005, 8:797-804.
54. Mann D.R., Barraclough C.A. Role of estrogen and progesterone in facilitating LH release in 4-day cyclic rats. Endocrinology 1973, 93:694-699.
55. Marino S.E., Birnbaum A.K., Leppik I.E., Conway J.M., Musib L.C., Brundage R.C., Ramsay R.E., Pennell P.B., White J.R., Gross C.R., Rarick J.O., Mishra U., Cloyd J.C. Steady-state carbamazepine pharmacokinetics following oral and stable-labeled intravenous administration in epilepsy patients: effects of race and sex. Clin. Pharmacol. Ther. 2012, 91:483-488.
56. McCarthy M.M., Arnold A.P., Ball G.F., Blaustein J.D., De Vries G.J. Sex differences in the brain: the not so inconvenient truth. J. Neurosci. 2012, 32:2241-2247.
57. McCormick D.A., Pape H.C. Properties of a hyperpolarization-activated cation current and its role in rhythmic oscillation in thalamic relay neurones. J. Physiol. 1990, 431:291-318.
58. McEwen B.S. Stress and hippocampal plasticity. Annu. Rev. Neurosci. 1999, 22:105-122.
59. McHugh J.C., Delanty N. Epidemiology and classification of epilepsy: gender comparisons. Int. Rev. Neurobiol. 2008, 83:11-26.
60. McNamara J.O., Scharfman H.E. Temporal lobe epilepsy and the BDNF receptor, TrkB. Jasper's Basic Mechanisms of the Epilepsies 2012, Oxford University Press, New York. 4th ed. J.L. Noebels, M. Avoli, M.A. Rogawski, R.W. Olsen, A.V. Delgado-Escueta (Eds.).
61. Mendez P., Azcoitia I., Garcia-Segura L.M. Interdependence of oestrogen and insulin-like growth factor-1 in the brain: potential for analysing neuroprotective mechanisms. J. Endocrinol. 2005, 185:11-17.
62. Nickel J., Jokeit H., Wunderlich G., Ebner A., Witte O.W., Seitz R.J. Gender-specific differences of hypometabolism in MTLE: implication for cognitive impairments. Epilepsia 2003, 44:1551-1561.
63. Ortiz-Gonzalez X.R., Poduri A., Roberts C.M., Sullivan J.E., Marsh E.D., Porter B.E. Focal cortical dysplasia is more common in boys than in girls. Epilepsy Behav. 2013, 27:121-123.
64. Panayiotopoulos C.P. Reflex seizures and reflex epilepsies. The Epilepsies: Seizures, Syndromes and Management 2005, Bladon Medical Publishing, Oxfordshire.
65. Pearce P.S., Friedman D., Lafrancois J.J., Iyengar S.S., Fenton A.A., Maclusky N.J., Scharfman H.E. Spike-wave discharges in adult Sprague-Dawley rats and their implications for animal models of temporal lobe epilepsy. Epilepsy. Behav. 2014, 32:121-131.
66. Pereira R.T., Porto C.S., Godinho R.O., Abdalla F.M. Effects of estrogen on intracellular signaling pathways linked to activation of muscarinic acetylcholine receptors and on acetylcholinesterase activity in rat hippocampus. Biochem. Pharmacol. 2008, 75:1827-1834.
67. Persad V., Cortez M.A., Snead O.C. A chronic model of atypical absence seizures: studies of developmental and gender sensitivity. Epilepsy Res. 2002, 48:111-119.
68. Persinger M.A., Makarec K., Bradley J.C. Characteristics of limbic seizures evoked by peripheral injections of lithium and pilocarpine. Physiol. Behav. 1988, 44:27-37.
69. h is mediated by circulating 17β-estradiol in preoptic area kisspeptin neurons. J. Neurosci. 2013, 33:10828-10839.
70. Pigeolet E., Jacqmin P., Sargentini-Maier M.L., Stockis A. Population pharmacokinetics of levetiracetam in Japanese and western adults. Clin. Pharmacokinet. 2007, 46:503-512.
71. Poolos N.P. H-channel dysfunction in generalized epilepsy: it takes two. Epilepsy Curr. 2006, 6:88-90.
72. Powell K.L., Kyi M., Reid C.A., Paradiso L., D'Abaco G.M., Kaye A.H., Foote S.J., O'Brien T.J. Genetic absence epilepsy rats from Strasbourg have increased corticothalamic expression of stargazin. Neurobiol. Dis. 2008, 31:261-265.
73. Powell K.L., Cain S.M., Ng C., Sirdesai S., David L.S., Kyi M., Garcia E., Tyson J.R., Reid C.A., Bahlo M., Foote S.J., Snutch T.P., O'Brien T.J. A Cav3.2 T-type calcium channel point mutation has splice-variant-specific effects on function and segregates with seizure expression in a polygenic rat model of absence epilepsy. J. Neurosci. 2009, 29:371-380.
74. Prange-Kiel J., Rune G.M. Direct and indirect effects of estrogen on rat hippocampus. Neuroscience 2006, 138:765-772.
75. h, in ah-type visceral ganglion neurons following ovariectomy in adult rats. PLoS ONE 2013, 8:e71184.
76. Racine R.J. Modification of seizure activity by electrical stimulation. II. Motor seizure. Electroencephalogr. Clin. Neurophysiol. 1982, 32:281-294.
77. Reddy D.S. The role of neurosteroids in the pathophysiology and treatment of catamenial epilepsy. Epilepsy Res. 2009, 85:1-30.
78. Reddy D.S. Role of hormones and neurosteroids in epileptogenesis. Front. Cell. Neurosci. 2013, 7:1-20.
79. Reddy D.S., Rogawski M.A. Neurosteroid replacement therapy for catamenial epilepsy. Neurotherapeutics 2009, 6:392-401.
80. Reddy D.S., Rogawski M.A. Neurosteroids - endogenous regulation of seizure susceptibility and role in the treatment of epilepsy. Jasper's Basic Mechanisms of the Epilepsies 2012, 982-1000. Oxford University Press, New York. 4th ed. J.L. Noebels, M. Avoli, M.A. Rogawski, R.W. Olsen, A.V. Delgado-Escueta (Eds.).
81. Reddy D.S., Kim H.Y., Rogawski M.A. Neurosteroid withdrawal model of perimenstrual catamenial epilepsy. Epilepsia 2001, 42:328-336.
82. Rodgers S.P., Bohacek J., Daniel J.M. Transient estradiol exposure during middle age in ovariectomized rats exerts lasting effects on cognitive function and the hippocampus. Endocrinology 2010, 151:1194-1203.
83. Rogawski M.A. Progesterone, neurosteroids, and the hormonal basis of catamenial epilepsy. Ann. Neurol. 2003, 53:288-291.
84. Sadaghiani M.M., Saboory E. Prenatal stress potentiates pilocarpine-induced epileptic behaviors in infant rats both time and sex dependently. Epilepsy Behav. 2010, 18:166-170.
85. Santana M.T., Jackowski A.P., Britto Fdos S., Sandim G.B., Caboclo L.O., Centeno R.S., Carrete H., Yacubian E.M. Gender and hemispheric differences in temporal lobe epilepsy: a VBM study. Seizure 2014, 23:274-279.
86. Savic I., Engel J. Sex differences in patients with mesial temporal lobe epilepsy. J. Neurol. Neurosurg. Psychiatry 1998, 65:910-912.
87. Scharfman H.E. Epilepsy. The Neurobiology of Brain Disorders 2014, Elsevier, Amsterdam. M.J. Zigmond, J.T. Coyle, L.P. Rowland (Eds.).
88. Scharfman H.E., Gray W.P. Plasticity of neuropeptide Y in the dentate gyrus after seizures, and its relevance to seizure-induced neurogenesis. EXS 2006, 193-211.
89. Scharfman H.E., Maclusky N.J. Similarities between actions of estrogen and BDNF in the hippocampus: coincidence or clue?. Trends Neurosci. 2005, 28:79-85.
90. Scharfman H.E., MacLusky N.J. Estrogen and brain-derived neurotrophic factor (BDNF) in hippocampus: complexity of steroid hormone-growth factor interactions in the adult CNS. Front. Neuroendocrinol. 2006, 27:415-435.
91. 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.
92. Scharfman H.E., MacLusky N.J. Estrogen-growth factor interactions and their contributions to neurological disorders. Headache 2008, 48(Suppl. 2):S77-S89.
93. Scharfman H.E., Mercurio T.C., Goodman J.H., Wilson M.A., MacLusky N.J. Hippocampal excitability increases during the estrous cycle in the rat: a potential role for brain-derived neurotrophic factor. J. Neurosci. 2003, 23:11641-11652.
94. 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.
95. Scharfman H.E., Hintz T.M., Gomez J., Stormes K.A., Barouk S., Malthankar-Phatak G.H., McCloskey D.P., Luine V.N., Maclusky N.J. Changes in hippocampal function of ovariectomized rats after sequential low doses of estradiol to simulate the preovulatory estrogen surge. Eur. J. Neurosci. 2007, 26:2595-2612.
96. 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.
97. 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.
98. h and HCN1 protein expression later in life. Eur. J. Neurosci. 2013, 23:3346-3358.
99. Seil F.J. Trkb receptor signaling and activity-dependent inhibitory synaptogenesis. Histol. Histopathol. 2003, 18:635-646.
100. Singh K.B. Persistent estrus rat models of polycystic ovary disease: an update. Fertil. Steril. 2005, 84(Suppl. 2):1228-1234.
101. Sisodiya S.M., Free S.L., Thom M., Everitt A.E., Fish D.R., Shorvon S.D. Evidence for nodular epileptogenicity and gender differences in periventricular nodular heterotopia. Neurology 1999, 52:336-341.
102. Smith S.S. Withdrawal properties of a neuroactive steroid: implications for GABA(A) receptor gene regulation in the brain and anxiety behavior. Steroids 2002, 67:519-528.
103. Smith S.S., Shen H., Gong Q.H., Zhou X. Neurosteroid regulation of GABA(A) receptors: focus on the α4 and δ subunits. Pharmacol. Ther. 2007, 116:58-76.
104. Smith C.C., Vedder L.C., McMahon L.L. Estradiol and the relationship between dendritic spines, NR2B containing NMDA receptors, and the magnitude of long-term potentiation at hippocampal CA3-CA1 synapses. Psychoneuroendocrinology 2009, 34(Suppl. 1):S130-S142.
105. 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.
106. Sperk G., Hamilton T., Colmers W.F. Neuropeptide Y in the dentate gyrus. Prog. Brain Res. 2007, 163:285-297.
107. Sridharan R., Murthy B.N. Prevalence and pattern of epilepsy in India. Epilepsia 1999, 40:631-636.
108. Taylor I., Hodgson B., Scheffer I.E., Mulley J., Berkovic S.F., Dibbens L. Is photosensitive epilepsy less common in males due to variation in X chromosome photopigment genes?. Epilepsia 2007, 48:1807-1809.
109. Tolmacheva E.A., van Luijtelaar G. The role of ovarian steroid hormones in the regulation of basal and stress induced absence seizures. J. Steroid Biochem. Mol. Biol. 2007, 104:281-288.
110. van Huizen F., March D., Cynader M.S., Shaw C. Muscarinic receptor characteristics and regulation in rat cerebral cortex: changes during development, aging and the oestrous cycle. Eur. J. Neurosci. 1994, 6:237-243.
111. Veliskova J., Velisek L. β-Estradiol increases dentate gyrus inhibition in female rats via augmentation of hilar neuropeptide y. J. Neurosci. 2007, 27:6054-6063.
112. Winkler A.S., Kerschbaumsteiner K., Stelzhammer B., Meindl M., Kaaya J., Schmutzhard E. Prevalence, incidence, and clinical characteristics of epilepsy-a community-based door-to-door study in northern Tanzania. Epilepsia 2009, 50:2310-2313.
113. Wirth M.J., Patz S., Wahle P. Transcellular induction of neuropeptide y expression by NT4 and BDNF. Proc. Natl. Acad. Sci. U. S. A. 2005, 102:3064-3069.
114. Yue B.W., Huguenard J.R. The role of h-current in regulating strength and frequency of thalamic network oscillations. Thalamus Relat. Syst. 2001, 1:95-103.