Estrogens influence behavioral responses in a kainic acid model of neurotoxicity

Hormones and Behavior

Volumn 48, Issue 3, 2005, Pages 291-302

  Papalexi, Eugenia ^a   Antoniou, Katerina ^b   Kitraki, Efthimia ^a  

^a UNIVERSITY OF ATHENS MEDICAL SCHOOL   (Greece)

^b UNIVERSITY OF IOANNINA   (Greece)

Author keywords

Estradiol; Hippocampus; Kainic acid; Object recognition; Open field; Rat; Water maze

Indexed keywords

ESTRADIOL; ESTROGEN; KAINIC ACID;

ANIMAL BEHAVIOR; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CELL SURVIVAL; CONTROLLED STUDY; DENTATE GYRUS; DRUG EFFECT; ESTROGEN BLOOD LEVEL; EXPLORATORY BEHAVIOR; FEMALE; HIPPOCAMPUS; HORMONAL THERAPY; HORMONE ACTION; IMMUNOREACTIVITY; MAZE TEST; MEMORY; MOSSY FIBER; NEUROFILAMENT; NEUROTOXICITY; NONHUMAN; OPEN FIELD TEST; OVARIECTOMY; PRIORITY JOURNAL; PROESTRUS; RAT; RECOGNITION; SNIFFING; SPATIAL MEMORY; STATISTICAL SIGNIFICANCE; TASK PERFORMANCE;

ANALYSIS OF VARIANCE; ANIMALS; BRAIN INJURIES; ESTRADIOL; EXPLORATORY BEHAVIOR; FEMALE; HIPPOCAMPUS; KAINIC ACID; MAZE LEARNING; MODELS, ANIMAL; NEURONS; NEUROPROTECTIVE AGENTS; NEUROTOXICITY SYNDROMES; NEUROTOXINS; OVARIECTOMY; RATS; RATS, WISTAR; RECOGNITION (PSYCHOLOGY); SPACE PERCEPTION;

EID: 23844554257     PISSN: 0018506X     EISSN: 10956867     Source Type: Journal    
DOI: 10.1016/j.yhbeh.2005.03.009     Document Type: Article

References (61)

1. K. Antoniou, G. Papathanasiou, G. Panagis, G.G. Nomikos, T. Hyphantis, and Z. Papadopoulou-Daifoti Individual responses to novelty predict qualitative differences in d-amphetamine-induced open field but not reward-related behaviors in rats Neuroscience 123 2004 613 623
2. I. Azcoitia, A. Sierra, and L.M. Garcia-Segura Estradiol prevents kainic acid-induced neuronal loss in the rat dentate gyrus NeuroReport 9 1998 3075 3079
3. C. Behl, M. Widmann, T. Trapp, and F. Holsboer 17-Beta estradiol protects neurons from oxidative stress-induced cell death in vitro Biochem. Biophys. Res. Commun. 216 1995 473 482
4. H.A. Bimonte, and V.H. Denenberg Estradiol facilitates performance as working memory load increases Psychoneuroendocrinology 24 1999 161 173
5. R.S. Bridges A quantitative analysis of the roles of dosage, sequence, and duration of estradiol and progesterone exposure in the regulation of maternal behavior in the rat Endocrinology 114 1984 930 940
6. R.L. Butcher, W.E. Collins, and N.W. Fugo Plasma concentration of LH, FSH, prolactin, progesterone and estradiol-17beta throughout the 4-day estrous cycle of the rat Endocrinology 94 1974 1704 1708
7. G.G. Buterbaugh Estradiol replacement facilitates the acquisition of seizures kindled from the anterior neocortex in female rats Epilepsy Res. 4 1989 207 215
8. G.G. Buterbaugh, and G.M. Hudson Estradiol replacement to female rats facilitates dorsal hippocampal but not ventral hippocampal kindled seizure acquisition Exp. Neurol. 111 1991 55 64
9. E.J. Chesler, and J.M. Juraska Acute administration of estrogen and progesterone impairs the acquisition of the spatial Morris water maze in ovariectomized rats Horm. Behav. 38 2000 234 242
10. J.M. Choi, R.D. Romeo, W.G. Brake, C.L. Bethea, Z. Rosenwaks, and B.S. McEwen Estradiol increases pre- and post-synaptic proteins in the CA1 region of the hippocampus in female rhesus macaques (Macaca mulatta) Endocrinology 144 2003 4734 4738
11. J.M. Daniel, and C.D. Lee Estrogen replacement in ovariectomized rats affects strategy selection in the Morris water maze Neurobiol. Learn. Mem. 82 2004 142 149
12. + in female, but not male rats Brain Res. 868 2000 95 104
13. D.E. Dluzen Neuroprotective effects of estrogen upon the nigrostriatal dopaminergic system J. Neurocytol. 29 2000 387 399
14. H. Dong, C.A. Csernansky, B. Goico, and J.G. Csernansky Hippocampal neurogenesis follows kainic acid-induced apoptosis in neonatal rats J. Neurosci. 23 2003 1742 1749
15. A. Ennaceur, and J. Delacour A new one-trial test for neurobiological studies of memory in rats. 1: behavioral data Behav. Brain Res. 31 1988 47 59
16. A.J. Fader, P.E. Johnson, and G.P. Dohanich Estrogen improves working but not reference memory and prevents amnestic effects of scopolamine of a radial-arm maze Pharmacol. Biochem. Behav. 62 1999 711 717
17. T. Fiordelisio, and A. Hernandez-Cruz Oestrogen regulates neurofilament expression in a subset of anterior pituitary cells of the adult female rat J. Neuroendocrinol. 14 2002 411 424
18. T.C. Foster, K.M. Sharrow, A. Kumar, and J. Masse Interaction of age and chronic estradiol replacement on memory and markers of brain aging Neurobiol. Aging 24 2003 839 852
19. H.N. Fugger, S.G. Cunningham, E.F. Rissman, and T.C. Foster Sex differences in the activational effect of ERalpha on spatial learning Horm. Behav. 34 1998 163 170
20. L.A. Galea, J.K. Wide, T.A. Paine, M.M. Holmes, B.K. Ormerod, and S.B. Floresco High levels of estradiol disrupt conditioned place preference learning, stimulus response learning and reference memory but have limited effects on working memory Behav. Brain Res. 126 2001 115 126
21. L.M. Garcia-Segura, I. Azcoitia, and L.L. DonCarlos Neuroprotection by estradiol Prog. Neurobiol. 63 2001 29 60
22. M.J. Gayoso, C. Primo, A. al-Majdalawi, J.M. Fernandez, M. Garrosa, and C. Iniguez Brain lesions and water-maze learning deficits after systemic administration of kainic acid to adult rats Brain Res. 653 1994 92 100
23. O.L. Gobbo, and S.M. O'Mara Post-treatment, but not pre-treatment, with the selective cyclooxygenase-2 inhibitor celecoxib markedly enhances functional recovery from kainic acid-induced neurodegeneration Neuroscience 125 2004 317 327
24. E. Gould, P. Tanapat, T. Rydel, and N. Hastings Regulation of hippocampal neurogenesis in adulthood Biol. Psychiatry 48 2000 715 720
25. P.S. Green, E.J. Perez, T. Calloway, and J.W. Simpkins Estradiol attenuation of beta-amyloid-induced toxicity: a comparison J. Neurocytol. 29 2000 419 423
26. J.E. Gresack, and K.M. Frick Environmental enrichment reduces the mnemonic and neural benefits of estrogen Neuroscience 128 2004 459 471
27. W.J. Hatton, and C.S. von Bartheld Analysis of cell death in the trochlear nucleus of the chick embryo: calibration of the optical disector counting method reveals systematic bias J. Comp. Neurol. 409 1999 169 186
28. T. Heikkinen, J. Puolivali, and H. Tanila Effects of long-term ovariectomy and estrogen treatment on maze learning in aged mice Exp. Gerontol. 39 2004 1277 1283
29. N. Hirokawa, and S. Takeda Gene targeting studies begin to reveal the function of neurofilament proteins J. Cell Biol. 143 1998 1 4
30. I.E. Holopainen, H.B. Lauren, A. Romppanen, and F.R. Lopez-Picon Changes in neurofilament protein-immunoreactivity after kainic acid treatment of organotypic hippocampal slice cultures J. Neurosci. Res. 66 2001 620 629
31. E. Kitraki, O. Kremmyda, D. Youlatos, M.N. Alexis, and C. Kittas Gender-dependent alterations in corticosteroid receptor status and spatial performance following 21 days of restraint stress Neuroscience 125 2004 47 55
32. V. Luine, and M. Rodriguez Effects of estradiol on radial arm maze performance of young and aged rats Behav. Neural Biol. 62 1994 230 236
33. V.N. Luine, S.T. Richards, V.Y. Wu, and K.D. Beck Estradiol enhances learning and memory in a spatial memory task and effects levels of monoaminergic neurotransmitters Horm. Behav. 34 1998 149 162
34. V.N. Luine, L.F. Jacome, and N.J. Maclusky Rapid enhancement of visual and place memory by estrogens in rats Endocrinology 144 2003 2836 2844
35. B.S. McEwen Gonadal and adrenal steroids regulate neurochemical and structural plasticity of the hippocampus via cellular mechanisms involving NMDA receptors Cell. Mol. Neurobiol. 16 1996 103 116
36. B.S. McEwen, and S.E. Alves Estrogen actions in the central nervous system Endocr. Rev. 20 1999 279 307
37. E.G. McGeer, P.L. McGeer, and K. Singh Kainate-induced degeneration of neostriatal neurons: dependency upon corticostriatal tract Brain Res. 139 1978 381 383
38. A. Mikulecka, Z. Hlinak, and P. Mares Behavioural effects of a subconvulsive dose of kainic acid in rats Behav. Brain Res. 101 1999 21 28
39. N.W. Milgram, D.A. Isen, D. Mandel, H. Palantzas, and M.J. Pepkowski Deficits in spontaneous behavior and cognitive function following systemic administration of kainic acid Neurotoxicology 9 1988 611 624
40. M.A. Morgan, and D.W. Pfaff Effects of estrogen on activity and fear-related behaviors in mice Horm. Behav. 40 2001 472 482
41. F. Nicoletti, C. Speciale, M.A. Sortino, G. Summa, G. Caruso, F. Patti, and P.L. Canonico 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 26 1985 252 257
42. K.C. Pang, R. Nocera, A.J. Secor, and R.M. Yoder GABAergic septohippocampal neurons are not necessary for spatial memory Hippocampus 11 2001 814 827
43. G. Paxinos, and C. Watson The Rat Brain in Stereotaxic Coordinates 4th ed. 1998 Academic Press San Diego, CA
44. S.S. Petanceska, V. Nagy, D. Frail, and S. Gandy Ovariectomy and 17beta-estradiol modulate the levels of Alzheimer's amyloid beta peptides in brain Neurology 54 2000 2212 2217
45. O. Picazo, I. Azcoitia, and L.M. Garcia-Segura Neuroprotective and neurotoxic effects of estrogens Brain Res. 990 2003 20 27
46. M.E. Prediger, G.D. Gamaro, L.M. Crema, F.U. Fontella, and C. Dalmaz Estradiol protects against oxidative stress induced by chronic variate stress Neurochem. Res. 29 2004 1923 1930
47. B. Roozendaal, R.G. Phillips, A.E. Power, S.M. Brooke, R.M. Sapolsky, and J.L. McGaugh Memory retrieval impairment induced by hippocampal CA3 lesions is blocked by adrenocortical suppression Nat. Neurosci. 4 2001 1169 1171
48. J.W. Simpkins, P.S. Green, K.E. Gridley, M. Singh, N.C. de Fiebre, and G. Rajakumar Role of estrogen replacement therapy in memory enhancement and the prevention of neuronal loss associated with Alzheimer's disease Am. J. Med. 103 1997 19S 25S
49. J.W. Simpkins, G. Rajakumar, Y.Q. Zhang, C.E. Simpkins, D. Greenwald, C.J. Yu, N. Bodor, and A.L. Day Estrogens may reduce mortality and ischemic damage caused by middle cerebral artery occlusion in the female rat J. Neurosurg. 87 1997 724 730
50. M. Singh, E.M. Meyer, W.J. Millard, and J.W. Simpkins Ovarian steroid deprivation results in a reversible learning impairment and compromised cholinergic function in female Sprague-Dawley rats Brain Res. 644 1994 305 312
51. B.M. Spruijt, and W.H. Gispen Behavioral sequences as an easily quantifiable parameter in experimental studies Physiol. Behav. 32 1984 707 710
52. C.E. Stafstrom, A. Chronopoulos, S. Thurber, J.L. Thompson, and G.L. Holmes Age-dependent cognitive and behavioral deficits after kainic acid seizures Epilepsia 34 1993 420 432
53. E. Vaucher, I. Reymond, R. Najaffe, S. Kar, R. Quirion, M.M. Miller, and K.B. Franklin Estrogen effects on object memory and cholinergic receptors in young and old female mice Neurobiol. Aging 23 2002 87 95
54. S. Wang, A. Hamberger, Q. Yang, and K.G. Haglid Changes in neurofilament protein NF-L and NF-H immunoreactivity following kainic acid-induced seizures J. Neurochem. 62 1994 739 748
55. C.E. Weaver Jr., M. Park-Chung, T.T. Gibbs, and D.H. Farb 17beta-estradiol protects against NMDA-induced excitotoxicity by direct inhibition of NMDA receptors Brain Res. 761 1997 338 341
56. M.J. West Regionally specific loss of neurons in the aging human hippocampus Neurobiol. Aging 14 1993 287 293
57. I.A. Wilson, J. Puolivali, T. Heikkinen, and P. Riekkinen Jr. Estrogen and NMDA receptor antagonism: effects upon reference and working memory Eur. J. Pharmacol. 381 1999 93 99
58. P.M. Wise, D.B. Dubal, M.E. Wilson, S.W. Rau, M. Bottner, and K.L. Rosewell Estradiol is a protective factor in the adult and aging brain: understanding of mechanisms derived from in vivo and in vitro studies Brain Res. Brain Res. Rev. 37 2001 313 319
59. C.S. Woolley Estrogen-mediated structural and functional synaptic plasticity in the female rat hippocampus Horm. Behav. 34 1998 140 148
60. C.S. Woolley Estradiol facilitates kainic acid-induced, but not flurothyl-induced, behavioral seizure activity in adult female rats Epilepsia 41 2000 510 515
61. Q. Yang, S. Wang, J.E. Karlsson, A. Hamberger, and K.G. Haglid Phosphorylated and non-phosphorylated neurofilament proteins: distribution in the rat hippocampus and early changes after kainic acid induced seizures J. Chem. Neuroanat. 9 1995 217 228