The cognitive effects of ovariectomy and estrogen replacement are modulated by aging

Neuroscience

Volumn 119, Issue 3, 2003, Pages 821-830

  Savonenko, A V ^a   Markowska, A L ^a  

^a JOHNS HOPKINS UNIVERSITY   (United States)

Author keywords

Active avoidance; Aging; Cholinergic system; Pre pulse inhibition; Rats; Scopolamine

Indexed keywords

ESTROGEN; SCOPOLAMINE;

AGE DISTRIBUTION; AGING; ANIMAL BEHAVIOR; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; AVOIDANCE BEHAVIOR; CHOLINERGIC SYSTEM; COGNITION; CONTROLLED STUDY; DIESTRUS; ESTROGEN ACTIVITY; ESTROGEN THERAPY; FEMALE; FOREBRAIN; LEARNING; MAZE TEST; MEMORY; MODULATION; NONHUMAN; OVARIECTOMY; PRIORITY JOURNAL; PROESTRUS; RAT; REPRODUCTION; SENESCENCE;

EID: 0038520900     PISSN: 03064522     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0306-4522(03)00213-6     Document Type: Article

References (51)

1. Bolles R.C. Learning theory. 2nd edition:1979;Holt, Rinehart and Winston, New York.
2. Daniel J.M., Fader A.J., Spencer A.L., Dohanich G.P. Estrogen enhances performance of female rats during acquisition of a radial arm maze. Horm Behav. 32:1997;217-225.
3. Davis M. The role of the amygdala in fear and anxiety. Annu Rev Neurosci. 15:1992;353-375.
4. De Oca B.M., DeCola J.P., Maren S., Fanselow M.S. Distinct regions of the periaqueductal gray are involved in the acquisition and expression of defensive responses. J Neurosci. 18:1998;3426-3432.
5. Diaz-Veliz G., Butron S., Benavides M.S., Dussaubat N., Mora S. Gender, estrous cycle, ovariectomy, and ovarian hormones influence the effects of diazepam on avoidance conditioning in rats. Pharmacol Biochem Behav. 66:2000;887-892.
6. Diaz-Veliz G., Dussaubat N., Mora S. Effect of oxotremorine on the acquisition of a conditioned avoidance response is modified by the estrous cycle, ovariectomy, and estradiol replacement in rats. Pharmacol Biochem Behav. 51:1995;279-283.
7. Diaz-Veliz G., Soto V., Dussaubat N., Mora S. Influence of the estrous cycle, ovariectomy and estradiol replacement upon the acquisition of conditioned avoidance responses in rats. Physiol Behav. 46:1989;397-401.
8. Diaz-Veliz G., Urresta F., Dussaubat N., Mora S. Effects of estradiol replacement in ovariectomized rats on conditioned avoidance responses and other behaviors. Physiol Behav. 50:1991;61-65.
9. Dohanich G.P., Fader A.J., Javorsky D.J. Estrogen and estrogen-progesterone treatments counteract the effect of scopolamine on reinforced T-maze alternation in female rats. Behav Neurosci. 108:1994;988-992.
10. Fadel J., Sarter M., Bruno J.P. Age-related attenuation of stimulated cortical acetylcholine release in basal forebrain-lesioned rats. Neuroscience. 90:1999;793-802.
11. Fader A.J., Johnson P.E., Dohanich G.P. 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.
12. Farr S.A., Banks W.A., Morley J.E. Estradiol potentiates acetylcholine and glutamate-mediated post-trial memory processing in the hippocampus. Brain Res. 864:2000;263-269.
13. Farr S.A., Flood J.F., Scherrer J.F., Kaiser F.E., Taylor G.T., Morley J.E. Effect of ovarian steroids on footshock avoidance learning and retention in female mice. Physiol Behav. 58:1995;715-723.
14. Farr S.A., Uezu K., Flood J.F., Morley J.E. Septo-hippocampal drug interactions in post-trial memory processing. Brain Res. 847:1999;221-230.
15. Feder H.H. Estrous cyclicity in mammals. Adler N.T. Neuroendocrinology of reproduction physiology and behavior . 1981;179-345 Plenum Press, New York.
16. Fendt M., Fanselow M.S. The neuroanatomical and neurochemical basis of conditioned fear. Neurosci Biobehav Rev. 23:1999;743-760.
17. Flood J.F., Baker M.L., Hernandez E.N., Morley J.E. Modulation of memory processing by neuropeptide Y varies with brain injection site. Brain Res. 503:1989;73-82.
18. Flood J.F., Morley J.E., Roberts E. Pregnenolone sulfate enhances post-training memory processes when injected in very low doses into limbic system structures the amygdala is by far the most sensitive . Proc Natl Acad Sci USA. 92:1995;10806-10810.
19. Gibbs R.B. Impairment of basal forebrain cholinergic neurons associated with aging and long-term loss of ovarian function. Exp Neurol. 151:1998;289-302.
20. 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.
21. Gibbs R.B., Aggarwal P. Estrogen and basal forebrain cholinergic neurons implications for brain aging and Alzheimer's disease-related cognitive decline . Horm Behav. 34:1998;98-111.
22. Gibbs R.B., Burke A.M., Johnson D.A. Estrogen replacement attenuates effects of scopolamine and lorazepam on memory acquisition and retention. Horm Behav. 34:1998;112-125.
23. Henderson V.W., Paganini-Hill A., Emanuel C.K., Dunn M.E., Buckwalter J.G. Estrogen replacement therapy in older women comparisons between Alzheimer's disease cases and nondemented control subjects . Arch Neurol. 51:1994;896-900.
24. Henderson V.W., Watt L., Buckwalter J.G. Cognitive skills associated with estrogen replacement in women with Alzheimer's disease. Psychoneuroendocrinology. 21:1996;421-430.
25. Jezierski M.K., Sohrabji F. Neurotrophin expression in the reproductively senescent forebrain is refractory to estrogen stimulation. Neurobiol Aging. 22:2001;309-319.
26. Kawas C., Resnick S., Morrison A., Brookmeyer R., Corrada M., Zonderman A., Bacal C., Lingle D.D., Metter E. A prospective study of estrogen replacement therapy and the risk of developing Alzheimer's disease the Baltimore Longitudinal Study of Aging . Neurology. 48:1997;1517-1521.
27. LeDoux J.E. Emotional memory in search of systems and synapses . Ann NY Acad Sci. 702:1993;149-157.
28. Luine V.N. Steroid hormone modulation of hippocampal dependent spatial memory. Stress. 2:1997;21-36.
29. Markowska A.L., Olton D.S., Givens B.A.S.B. Cholinergic manipulations in the medial septal area age-related effects on working memory and hippocampal electrophysiology . J Neurosci. 15:1995;2063-2073.
30. Markowska A.L., Savonenko A.V. Effectiveness of estrogen replacement for restoration of cognitive function after long-term estrogen withdrawal in aging rats. J Neurosci. 22:2002;10985-10995.
31. McMillan P.J., Singer C.A., Dorsa D.M. The effects of ovariectomy and estrogen replacement on trkA and choline acetyltransferase mRNA expression in the basal forebrain of the adult female Sprague-Dawley rat. J Neurosci. 16:1996;1860-1865.
32. Meites J., Lu J.K.H. Reproductive ageing and neuroendocrine function. Charlton H.M. Oxford review of reproductive biology. Vol. 16:1994;215-247 Oxford University Press, New York.
33. Milner J.S. Castration and amphetamine effects on acquisition of a Sidman avoidance task in rats. Physiol Behav. 17:1976;545-548.
34. Mineka S. The role of fear in theories of avoidance learning, flooding, and extinction. Psychol Bull. 5:1979;985-1010.
35. Montes G.S., Luque E.H. Effects of ovarian steroids on vaginal smears in the rat. Acta Anat. 133:1988;192-199.
36. Muir J.L. Acetylcholine, aging, and Alzheimer's disease. Pharmacol Biochem Behav. 56:1997;687-696.
37. Mulnard R.A., Cotman C.W., Kawas C., van Dyck C.H., Sano M., Doody R., Koss E., Pfeiffer E., Jin S., Gamst A., Grundman M., Thomas R., Thal L.J. Estrogen replacement therapy for treatment of mild to moderate Alzheimer disease a randomized controlled trial: Alzheimer's Disease Cooperative Study . JAMA. 283:2000;1007-1015.
38. Packard M.G., Teather L.A. Posttraining estradiol injections enhance memory in ovariectomized rats cholinergic blockade and synergism . Neurobiol Learn Mem. 68:1997;172-188.
39. Savonenko A., Filipkowski R.K., Werka T., Zielinski K., Kaczmarek L. Defensive conditioning-related functional heterogeneity among nuclei of the rat amygdala revealed by c-Fos mapping. Neuroscience. 94:1999;723-733.
40. Savonenko A.V., Danilets A.V., Zielinski K. Studies of individual differences as a method for discriminating the stages of acquisition of a conditioned reflex. Neurosci Behav Physiol. 29:1999;295-303.
41. Seshadri S., Zornberg G.L., Derby L.E., Myers M.W., Jick H., Drachman D.A. Postmenopausal estrogen replacement therapy and the risk of Alzheimer disease. Arch Neurol. 58:2001;435-440.
42. Sfikakis A., Spyraki C., Sitaras N., Varonos D. Implication of the estrous cycle on conditioned avoidance behavior in the rat. Physiol Behav. 21:1978;441-446.
43. Sherwin B.B. Estrogenic effects on memory in women. Ann NY Acad Sci. 743:1994;213-230.
44. Simpkins J.W., Green P.S., Gridley K.E., Singh M., de Fiebre N.C., Rajakumar G. 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.
45. Singer C.A., McMillan P.J., Dobie D.J., Dorsa D.M. Effects of estrogen replacement on choline acetyltransferase and trkA mRNA expression in the basal forebrain of aged rats. Brain Res. 789:1998;343-346.
46. Singh M., Meyer E.M., Millard W.J., Simpkins J.W. Ovarian steroid deprivation results in a reversible learning impairment and compromised cholinergic function in female Sprague-Dawley rats. Brain Res. 644:1994;305-312.
47. Tropp J., Markus E.J. Effects of mild food deprivation on the estrous cycle of rats. Physiol Behav. 73:2001;553-559.
48. Van Oyen H.G., Walg H., Van De Poll N.E. Discriminated lever press avoidance conditioning in male and female rats. Physiol Behav. 26:1981;313-317.
49. Vasquez B.J., Martinez J.L. Jr, Jensen R.A., Messing R.B., Rigter H., McGaugh J.L. Learning and memory in young and aged Fischer 344 rats. Arch Gerontol Geriatr. 2:1983;279-291.
50. Voytko M.L. The effects of long-term ovariectomy and estrogen replacement therapy on learning and memory in monkeys (Macaca fascicularis). Behav Neurosci. 114:2000;1078-1087.
51. Wainer B.H., Steininger T.L., Roback J.D., Burke-Watson M.A., Mufson E.J., Kordower J. Ascending cholinergic pathways functional organization and implications for disease models . Prog Brain Res. 98:1993;9-30.