Estradiol and corticosterone independently impair spatial navigation in the Morris water maze in adult female rats

Behavioural Brain Research

Volumn 187, Issue 1, 2008, Pages 56-66

  Snihur, Adrian W K ^a   Hampson, Elizabeth ^a   Cain, Donald Peter ^a  

^a UNIVERSITY OF WESTERN ONTARIO   (Canada)

Author keywords

Adrenalectomy; Estrogen; Ovarian; Ovariectomy; Progesterone; Sex difference; Spatial learning; Stress

Indexed keywords

CORTICOSTERONE; ESTRADIOL; PROGESTERONE;

ANIMAL EXPERIMENT; ARTICLE; CONTROL GROUP; CONTROLLED STUDY; EXPERIMENTAL STUDY; FEMALE; MALE; MENTAL TASK; MENTAL TEST; MOUSE; NONHUMAN; PRIORITY JOURNAL; SEX DIFFERENCE; SPATIAL MEMORY; SWIMMING; TASK PERFORMANCE; TRAINING;

ADRENALECTOMY; ANIMALS; CORTICOSTERONE; ESTRADIOL; FEMALE; MALE; MAZE LEARNING; MUSCULOSKELETAL EQUILIBRIUM; PSYCHOMOTOR PERFORMANCE; RATS; RATS, LONG-EVANS; REVERSAL LEARNING; SEX CHARACTERISTICS; SPACE PERCEPTION; SWIMMING;

EID: 36749065507     PISSN: 01664328     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.bbr.2007.08.023     Document Type: Article

References (61)

1. 2 anesthesia used for restraint during serial blood collection vial the jugular vein. J Am Assoc Lab Anim Sci 45 3 (2006) 17-22
2. Beiko J., Lander R., Hampson E., Boon F., and Cain D.P. Contribution of sex differences in the acute response to sex differences in water maze performance in the rat. Behav Brain Res 151 (2004) 239-253
3. Berry B., McMahan R., and Gallagher M. Spatial learning and memory at defined points of the estrous cycle: effects on performance of a hippocampal-dependent task. Behav Neurosci 111 2 (1997) 267-274
4. Bimonte-Nelson H.A., Singleton R.S., Nelson M.E., Eckman C.B., Barber J., Scott T.Y., et al. Testosterone, but not nonaromatizable dihydrotestosterone, improves working memory and alters nerve growth factor levels in aged male rats. Exp Neurol 181 (2003) 301-312
5. Bowman R.E., Ferguson D., and Luine V.N. Effects of chronic restraint stress and estradiol on open field activity, spatial memory, and monoaminergic neurotransmitters in ovariectomized rats. Neuroscience 113 2 (2002) 401-410
6. Bucci D.J., Chiba A.A., and Gallagher M. Spatial learning in male and female Long-Evans rats. Behav Neurosci 109 1 (1995) 180-183
7. Cain D.P., Boon F., and Corcoran M.E. Thalamic and hippocampal mechanisms in spatial navigation: a dissociation between brain mechanisms for learning how versus learning where to navigate. Behav Brain Res 170 2 (2006) 241-256
8. Cain D.P., Humpartzoomian R., and Boon F. Retrospinal cortex lesions impair water maze strategies or spatial place learning depending on prior experience of the rat. Behav Brain Res 170 2 (2006) 316-325
9. Cain D.P., and Boon F. Detailed behavioral analysis reveals both task strategies and spatial memory impairments in rats given bilateral middle cerebral artery stroke. Brain Res 972 1-2 (2003) 64-74
10. Cain D.P. Testing the NMDA, long-term potentiation, and cholinergic hypotheses of spatial learning. Neurosci Biobehav Rev 22 2 (1998) 181-193
11. Cain D.P., Saucier D., Hargreaves E.L., Wilson E., and DeSouza J.F. Polypropylene pellets as an inexpensive reusable substitute for milk in the Morris water maze. J Neurosci Methods 49 3 (1993) 193-197
12. Carey M.P., Deterd C.H., de Koning J., Helmerhorst F., and de Kloet E.R. The influence of ovarian steroids on hypothalamo-pituitary-adrenal regulation in the female rat. J Endocrinol 144 (1995) 311-321
13. Chesler E.J., and Juraska J.M. Acute administration of estrogen and progesterone impairs the acquisition of the spatial Morris water maze in ovariectomized rats. Horm Behav 38 (2000) 234-242
14. Conrad C.D., Jackson J.L., Wieczorek L., Baran S.E., Harman J.S., Wright R.L., et al. Acute stress impairs spatial memory in male but not female rats: influence of estrous cycle. Pharm Biochem Behav 78 (2004) 569-579
15. Daniel J.M., Roberts S.L., and Dohanich G.P. Effects of ovarian hormones and environment on radial maze and water maze performance of female rats. Physiol Behav 66 (1999) 11-20
16. File S.E., and Peet L.A. The sensitivity of the rat corticosterone response to environmental manipulations and to chronic chlordiazepoxide treatment. Physiol Behav 25 5 (1980) 753-758
17. Frankfurt M., Gould E., Woolley C.S., and McEwen B.S. Gonadal steroids modify dendritic spine density in ventromedial hypothalamic neurons: a Golgi study in the adult rat. Neuroendocrinology 51 5 (1990) 530-535
18. Frick K.M., and Berger-Sweeney J. Spatial reference memory and neocortical neurochemistry vary with the estrous cycle in C57BL/6 mice. Behav Neurosci 115 1 (2001) 229-237
19. Frick K.M., Fernandez S.M., Bennett J.C., Prange-Kiel J., MacLusky N.J., and Leranth C. Behavioral training interferes with the ability of gonadal hormones to increase CA1 spine density in ovariectomized female rats. Eur J Neurosci 19 11 (2004) 3026-3032
20. Frye C.A. Estrus-associated decrements in a water maze task are limited to acquisition. Physiol Behav 57 1 (1995) 5-14
21. Fugger H.N., Cunningham S.G., Rissman E.F., and Foster T.C. Sex differences in the activational effect of ER on spatial learning. Horm Behav 34 2 (1998) 163-170
22. Galea L.A.M., Kavaliers M., Ossenkopp K.-P., and Hampson E. Gonadal hormone levels and spatial learning performance in the Morris water maze in male and female meadow voles, Microtus pennsylvanicus. Horm Behav 29 1 (1995) 106-125
23. Galea L.A., Kavaliers M., Ossenkopp K.-P., Innes D., and Hargreaves E.L. Sexually dimorphic spatial learning varies seasonally in two populations of deer mice. Brain Res 635 1-2 (1994) 18-26
24. Gaulin S.J.C., FitzGerald R.W., and Wartell M.S. Sex differences in spatial ability and activity in two vole species (Microtus ochrogaster and M. pennsylvanicus). J Comp Psychol 104 (1990) 88-93
25. Gibbs R.B. Long-term treatment with estrogen and progesterone enhances acquisition of a spatial memory task by ovariectomized aged rats. Neurobiol Aging 21 (2000) 107-116
26. Glavas M.M., Hofmann C.E., Yu W.K., and Weinberg J. Effects of prenatal ethanol exposure on hypothalamic-pituitary-adrenal regulation after adrenalectomy and corticosterone replacement. Alcohol Clin Exp Res 25 6 (2001) 890-897
27. Gresack J.E., and Frick K.M. Male mice exhibit better spatial working and reference memory than females in a water-escape radial arm maze task. Brain Res 982 1 (2003) 98-107
28. Healy S.D., Braham S.R., and Braithwaite V.A. Spatial working memory in rats: no differences between the sexes. Proc Biol Sci 266 1435 (1999) 2303-2308
29. Hennessy M.B. Sensitization of the plasma corticosterone response to novel environments. Physiol Behav 50 6 (1991) 1175-1179
30. Herman J.P., and Watson S.J. Stress regulation of mineralocorticoid receptor heteronuclear RNA in rat hippocampus. Brain Res 677 (1995) 243-249
31. Holmes M.M., Wide J.K., and Galea L.A. Low levels of estradiol facilitate, whereas high levels of estradiol impair, working memory performance on the radial arm maze. Behav Neurosci 116 5 (2002) 928-934
32. Holscher C. Stress impairs performance in spatial water maze learning tasks. Behav Brain Res 100 1-2 (1999) 225-235
33. Hu Z.T., Yuri K., Ozawa H., Lu H., and Kawata M. The in vivo time course for elimination of adrenalectomy-induced apoptotic profiles from the granule cell layer of the rat hippocampus. J Neurosci 17 (1997) 3981-3989
34. Kant G.J., Lenox R.H., Bunnell B.N., Mougey E.H., Pennington L.L., and Meyerhoff J.L. Comparison of stress response in male and female rats: pituitary cyclic AMP and plasma prolactin, growth hormone and corticosterone. Psychoneuroendocrinology 8 4 (1983) 421-428
35. Karandrea D., Kittas C., and Kitraki E. Forced swimming differentially affects male and female brain corticosteroid receptors. Neuroendocrinology 75 (2002) 217-226
36. Kavaliers M., Ossenkopp K.-P., Galea L.A., and Kolb B. Sex differences in spatial learning and prefrontal and parietal cortical dendritic morphology in the meadow vole, Microtus pennsylvanicus. Brain Res 810 1-2 (1998) 41-47
37. Kerr J.E., Beck S.G., and Handa R.J. Androgens modulate glucocorticoid receptor mRNA, but not mineralocorticoid receptor mRNA levels, in the rat hippocampus. J Neuroendocrinology 8 (1996) 439-447
38. Kolb B., Buhrmann K., McDonald R., and Sutherland R.J. Dissociation of the medial prefrontal, posterior parietal, and posterior temporal cortex for spatial navigation and recognition memory in the rat. Cereb Cortex 4 (1994) 664-680
39. Korol D.L., and Kolo L.L. Estrogen-induced changes in place and response learning in young adult female rats. Behav Neurosci 116 3 (2002) 411-420
40. McEwen B.S., and Woolley C.S. Estradiol and progesterone regulate neuronal structure and synaptic connectivity in adult as well as developing brain. Exp Gerontol 29 3-4 (1994) 431-436
41. Mitchell J.B., and Meaney M.J. Effects of corticosterone on response consolidation and retrieval in the forced swim test. Behav Neurosci 105 6 (1991) 798-803
42. Morris R.G.M. Developments of a water-maze procedure for studying spatial learning in the rat. J Neurosci Methods 11 (1984) 47-60
43. Morris R.G. Synaptic plasticity and learning: selective impairment of learning rats and blockade of long-term potentiation in vivo by the N-methyl-d-aspartate receptor antagonist AP5. J Neurosci 9 9 (1989) 3040-3057
44. Perrot-Sinal T.S., Kostenuik M.A., Ossenkopp K.-P., and Kavaliers M. Sex differences in performance in the Morris water maze and the effects of initial nonstationary hidden platform training. Behav Neurosci 110 6 (1996) 1309-1320
45. Reburn C.J., and Wynne-Edwards K.E. Cortisol and prolactin concentrations during repeated blood sample collection from freely moving, mouse-sized mammals (Phodopus spp.). Comp Med 50 2 (2000) 184-198
46. Rissanen A., Puolivali J., van Groen T., and Riekkinen P.J. In mice tonic estrogen replacement therapy improves non-spatial and spatial memory in a water maze task. J Cog Neurosci 10 6 (1999) 1369-1372
47. Roof R.L., and Havens M.D. Testosterone improves maze performance and induces development of a male hippocampus in females. Brain Res 572 (1992) 310-313
48. Sarrieau A., Vial M., McEwen B., Broer Y., Dussaillant M., Philibert D., et al. Corticosteroid receptors in rat hippocampal sections: effect of adrenalectomy and corticosterone replacement. J Steroid Biochem 24 3 (1986) 721-724
49. Servatius R.J., Ottenweller J.E., and Natelson B.H. A comparison of the effects of repeated stressor exposures and corticosterone injections on plasma cholesterol, thyroid hormones and corticosterone levels in rats. Life Sci 55 21 (1994) 1611-1617
50. Shors T.J., Pickett J., Wood G., and Paczynski M. Acute stress persistently enhances estrogen levels in the female rat. Stress 3 2 (1999) 163-171
51. Spencer R.L., Kalman B.A., Cotter C.S., and Deak T. Discrimination between changes in glucocorticoid receptor expression and activation in rat brain using Western blot analysis. Brain Res 868 2 (2000) 275-286
52. Svec F., Gordon S., and Tate D. Glucocorticoid receptor regulation: the effects of adrenalectomy, exogenous glucocorticoid, and stress on hepatic receptor number in male and female mice. Biochem Med Metab Biol 41 3 (1989) 224-233
53. Treit D., and Fundytus M. Thigmotaxis as a test for anxiolytic activity in rats. Pharm Biochem Behav 31 (1989) 959-962
54. Tritos N., Kitraki E., Philippidis H., and Stylianopoulou F. Neurotransmitter modulation of glucocorticoid receptor mRNA levels in the rat hippocampus. Neuroendocrinology 69 (1999) 324-330
55. Viau V., and Meaney M.J. Variations in the hypothalamic-pituitary-adrenal response to stress during the estrous cycle in the rat. Endocrinology 129 5 (1991) 2503-2511
56. Warren S.G., and Juraska J.M. Spatial and nonspatial learning across the rat estrous cycle. Behav Neurosci 111 (1997) 259-266
57. Whishaw I.Q. Dissociating performance and learning deficits on spatial navigation tasks in rats subjected to cholinergic muscarinic blockade. Brain Res Bull 23 4-5 (1989) 347-358
58. Whishaw I.Q., Cassel J.C., and Jarrard L.E. Rats with fimbria-fornix lesions display a place response in a swimming pool: a dissociation between getting there and knowing where. J Neurosci 15 8 (1995) 5779-5788
59. Williams C.L., and Meck W.H. The organizational effects of gonadal steroids on sexually dimorphic spatial ability. Psychoneuroendocrinology 16 1-3 (1991) 155-176
60. Woolley C.S., and McEwen B.S. Estradiol mediates fluctuation in hippocampal synapse density during the estrous cycle in the adult rat. J Neurosci 12 7 (1992) 2549-2554
61. Woolley C.S., and McEwen B.S. Roles of estradiol and progesterone in regulation of hippocampal dendritic spine density during the estrous cycle. J Comp Neurol 336 (1993) 293-306