Ovarian steroids enhance object recognition in naturally cycling and ovariectomized, hormone-primed rats

Neurobiology of Learning and Memory

Volumn 86, Issue 1, 2006, Pages 35-46

  Walf, Alicia A ^a   Rhodes, Madeline E ^a   Frye, Cheryl A ^a  

^a STATE UNIVERSITY OF NEW YORK   (United States)

Author keywords

Allopregnanolone; Estrogen; Hippocampus; Learning; Memory; Prefrontal cortex; Progesterone; Selective estrogen receptor modulators

Indexed keywords

3ALPHA HYDROXY 5ALPHA PREGNAN 20 ONE; 5ALPHA PREGNANE 3ALPHA,20ALPHA DIOL; ESTRADIOL; GESTAGEN; PROGESTERONE; SELECTIVE ESTROGEN RECEPTOR MODULATOR; STEROID;

ANIMAL EXPERIMENT; ARTICLE; BEHAVIOR; BRAIN FUNCTION; CONTROLLED STUDY; DIESTRUS; ESTRADIOL BLOOD LEVEL; ESTRUS; FEMALE; HIPPOCAMPUS; LEARNING; MEMORY; NONHUMAN; OVARIECTOMY; OVARY; PREFRONTAL CORTEX; PROGESTERONE BLOOD LEVEL; RADIOIMMUNOASSAY; RAT; RECOGNITION; REGRESSION ANALYSIS; TASK PERFORMANCE; TRAINING; WORKING MEMORY;

ANALYSIS OF VARIANCE; ANIMALS; CEREBRAL CORTEX; ESTRADIOL; ESTROUS CYCLE; EXPLORATORY BEHAVIOR; FEMALE; HIPPOCAMPUS; MEMORY, SHORT-TERM; OVARIECTOMY; PROGESTERONE; RATS; RATS, LONG-EVANS; RECOGNITION (PSYCHOLOGY); STEROIDS;

EID: 33646840883     PISSN: 10747427     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.nlm.2006.01.004     Document Type: Article

References (96)

1. Arnaiz S.L., D'Amico G., Paglia N., Arismendi M., Basso N., and del Rosario Lores Arnaiz M. Enriched environment, nitric oxide production and synaptic plasticity prevent the aging-dependent impairment of spatial cognition. Molecular Aspects of Medicine 25 (2004) 91-101
2. Bi R., Foy M.R., Vouimba R.M., Thompson R.F., and Baudry M. Cyclic changes in estradiol regulate synaptic plasticity through the MAP kinase pathway. Proceedings of the National Academy of Science 98 (2001) 13391-13395
3. Bimonte H.A., and Denenberg V.H. Estradiol facilitates performance as working memory load increases. Psychoneuroendocrinology 24 (1999) 161-173
4. Bimonte-Nelson H.A., Singleton R.S., Williams B.J., and Granholm A.C. Ovarian hormones and cognition in the aged female rat: II. progesterone supplementation reverses the cognitive enhancing effects of ovariectomy. Behavioral Neuroscience 118 (2004) 707-714
5. Blank T., Nijholt I., Kye M.J., Radulovic J., and Spiess J. Small-conductance, Ca2+-activated K+ channel SK3 generates age-related memory and LTP deficits. Nature Neuroscience 6 (2003) 911-912
6. Chakraborty T.R., and Gore A.C. Aging-related changes in ovarian hormones, their receptors, and neuroendocrine function. Experimental biology and medicine 229 (2004) 977-987
7. Cheng Y.J., and Karavolas H.J. Conversion of progesterone to 5α-pregnane-3, 20-dione and 3α-hydroxy-5α-pregnan-20-one by rat medical basal hypothalami and the effects of estradiol and stage of estrous cycle on the conversion. Endocrinology 93 (1973) 1157-1162
8. 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. Hormones and Behavior 38 (2000) 234-242
9. Ciriza I., Azcoitia I., and Garcia-Segura L.M. Reduced progesterone metabolites protect rat hippocampal neurones from kainic acid excitotoxicity in vivo. Journal of Neuroendocrinology 16 (2004) 58-63
10. Daniel J.M., Fader A.J., Spencer A.L., and Dohanich G.P. Estrogen enhances performance of female rats during acquisition of a radial arm maze. Hormones and Behavior 32 (1997) 217-225
11. Davis D.M., Jacobson T.K., Aliakbari S., and Mizumori S.J. Differential effects of estrogen on hippocampal- and striatal-dependent learning. Neurobiology of Learning and Memory 84 (2005) 132-137
12. Diaz-Veliz G., Urresta F., Dussaubat N., and Mora S. Effects of estradiol replacement in ovariectomized rats on conditioned avoidance responses and other behaviors. Physiology and Behavior 50 (1991) 61-65
13. Djebaili M., Hoffman S.W., and Stein D.G. Allopregnanolone and progesterone decrease cell death and cognitive deficits after a contusion of the rat pre-frontal cortex. Neuroscience 123 (2004) 349-359
14. Djebaili M., Guo Q., Pettus E.H., Hoffman S.W., and Stein D.G. The neurosteroids progesterone and allopregnanolone reduce cell death, gliosis, and functional deficits after traumatic brain injury in rats. Journal of Neurotrauma 22 (2005) 106-118
15. Dohanich G.P., Fader A.J., and Javorsky D.J. Estrogen and estrogen-progesterone treatments counteract the effect of scopolamine on reinforced T-maze alternation in female rats. Behavioral Neuroscience 108 (1994) 988-992
16. El-Bakri N.K., Islam A., Zhu S., Elhassan A., Mohammed A., Winblad B., et al. Effects of estrogen and progesterone treatment on rat hippocampal NMDA receptors: A relationship to Morris water maze performance. Journal of cellular and molecular medicine 8 (2004) 537-544
17. Edwards D.A. Induction of estrus in female mice: Estrogen-progesterone interactions. Hormones and Behavior 1 (1970) 299-304
18. Ennaceur A., and Delacour J. A new one-trial test for neurobiological studies of memory in rats. 1: Behavioral data. Behavioural Brain Research 31 (1988) 47-59
19. Ennaceur A., Neave N., and Aggleton J.P. Spontaneous object recognition and object location memory in rats: The effects of lesions in the cingulate cortices, the medial prefrontal cortex, the cingulum bundle and the fornix. Experimental Brain Research 113 (1997) 509-519
20. Fader A.J., Hendricson A.W., and Dohanich G.P. Estrogen improves performance of reinforced T-maze alternation and prevents the amnestic effects of scopolamine administered systemically or intrahippocampally. Neurobiology of Learning and Memory. 69 (1998) 225-240
21. Fernandez S.M., and Frick K.M. Chronic oral estrogen affects memory and neurochemistry in middle-aged female mice. Behavioral Neuroscience 118 (2004) 1340-1351
22. Frick K.M., Fernandez S.M., and Bulinski S.C. Estrogen replacement improves spatial reference memory and increases hippocampal synaptophysin in aged female mice. Neuroscience 115 (2002) 547-558
23. Frye C.A. Estrus-associated decrements in a water maze task are limited to acquisition. Physiology and Behavior 57 (1995) 5-14
24. Frye C.A. The role of neurosteroids and non-genomic effects of progestins and androgens in mediating sexual receptivity of rodents. Brain research. Brain research reviews 37 (2001) 201-222
25. Frye C.A., and Bayon L.E. Mating stimuli influence endogenous variations in the neurosteroids 3α, 5α-THP and 3α-Diol. Journal of Neuroendocrinology 11 (1999) 839-847
26. Frye C.A., and Duncan J.E. Estradiol benzoate potentiates neuroactive steroids' effects on pain sensitivity. Pharmacology, Biochemistry and Behavior 53 (1996) 27-32
27. Frye C.A., and Lacey E.H. Progestins influence performance on cognitive tasks independent of changes in affective behavior. Psychobiology 28 (2001) 550-563
28. Frye C.A., and Rhodes M.E. Enhancing effects of estrogen on inhibitory avoidance performance may be in part independent of intracellular estrogen receptors in the hippocampus. Brain Research 956 (2002) 285-293
29. Frye C.A., and Rhodes M.E. Estrogen-priming can enhance progesterone's anti-seizure effects in part by increasing hippocampal levels of allopregnanolone. Pharmacology, Biochemistry, and Behavior 81 (2005) 907-916
30. Frye, C. A., & Rhodes, M. E. (2006). Exploratory, anti-anxiety, and pro-social behaviors of female rats are mediated, in part, by progestins in the ventral tegmental area. Behavioral Neuroscience (submitted).
31. Frye C.A., Rhodes M.E., and Dudek B. Estradiol to aged female or male mice improves learning in inhibitory avoidance and water maze tasks. Brain Research 1036 (2005) 101-108
32. Frye, C. A., Rhodes, M. E., Petralia, S. M., Walf, A. A., Sumida, K., & Edinger, K. L. (2006). 3α, 5α-THP in the midbrain ventral tegmental area mediates social, sexual, and affective behaviors. Neuroscience (in press).
33. Frye C.A., and Scalise T.J. Anti-seizure effects of progesterone and 3α, 5α-THP in kainic acid and perforant pathway models of epilepsy. Psychoneuroendocrinology 25 (2000) 407-420
34. Frye C.A., and Sturgis J.D. Neurosteroids affect spatial/reference, working, and long-term memory of female rats. Neurobiology of Learning and Memory 64 (1995) 83-96
35. Fugger H.N., Foster T.C., Gustafsson J., and Rissman E.F. Novel effects of estradiol and estrogen receptor α and β on cognitive function. Brain Research 883 (2000) 258-264
36. Galea L.A., 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. Hormones and Behavior 29 (1995) 106-125
37. Galea L.A., Wide J.K., Paine T.A., Holmes M.M., Ormerod B.K., and Floresco S.B. High levels of estradiol disrupt conditioned place preference learning, stimulus response learning and reference memory but have limited effects on working memory. Behavioural Brain Research 126 (2001) 115-126
38. Galea L.A., Lee T.T., Kostaras X., Sidhu J.A., and Barr A.M. High levels of estradiol impair spatial performance in the Morris water maze and increase 'depressive-like' behaviors in the female meadow vole. Physiology and Behavior 77 (2002) 217-225
39. Garcia-Estrada J., Del Rio J.A., Luquin S., Soriano E., and Garcia-Segura L.M. Gonadal hormones down-regulate reactive gliosis and astrocyte proliferation after a penetrating brain injury. Brain Research 628 (1993) 271-278
40. Garey J., Morgan M.A., Frohlich J., McEwen B.S., and Pfaff D.W. Effects of the phytoestrogen coumestrol on locomotor and fear-related behaviors in female mice. Hormones and Behavior 40 (2001) 65-76
41. Gibbs R.B. Effects of estrogen on basal forebrain cholinergic neurons vary as a function of dose and duration of treatment. Brain Research 757 (1997) 10-16
42. Gibbs R.B. Estrogen replacement enhances acquisition of a spatial memory task and reduces deficits associated with hippocampal muscarinic receptor inhibition. Hormones and Behavior 36 (1999) 222-233
43. Gibbs R.B. Long-term treatment with estrogen and progesterone enhances acquisition of a spatial memory task by ovariectomized aged rats. Neurobiology of Aging 21 (2000) 107-116
44. Gibbs R.B., Burke A.M., and Johnson D.A. Estrogen replacement attenuates effects of scopolamine and lorazepam on memory acquisition and retention. Hormones and Behavior 34 (1998) 112-125
45. Gibbs R.B., Gabor R., Cox T., and Johnson D.A. Effects of raloxifene and estradiol on hippocampal acetylcholine release and spatial learning in the rat. Psychoneuroendocrinology 29 (2004) 741-748
46. Granon S., Vidal C., Thinus-Blanc C., Changeux J.P., and Poucet B. Working memory, response selection, and effortful processing in rats with medial prefrontal lesions. Behavioral Neuroscience 108 (1994) 883-891
47. Gresack J.E., and Frick K.M. Environmental enrichment reduces the mnemonic and neural benefits of estrogen. Neuroscience 128 (2004) 459-471
48. Gureviciene I., Puolivali J., Pussinen R., Wang J., Tanila H., and Ylinen A. Estrogen treatment alleviates NMDA-antagonist induced hippocampal LTP blockade and cognitive deficits in ovariectomized mice. Neurobiology of Learning and Memory 79 (2003) 72-80
49. He J., Hoffman S.W., and Stein D.G. Allopregnanolone, a progesterone metabolite, enhances behavioral recovery and decreases neuronal loss after traumatic brain injury. Restorative neurology and neuroscience 22 (2004) 19-31
50. He J., Evans C.O., Hoffman S.W., Oyesiku N.M., and Stein D.G. Progesterone and allopregnanolone reduce inflammatory cytokines after traumatic brain injury. Experimental Neurology 189 (2004) 404-412
51. Heikkinen T., Puolivali J., and Tanila H. Effects of long-term ovariectomy and estrogen treatment on maze learning in aged mice. Experimental Gerontology 39 (2004) 1277-1283
52. 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. Behavioral Neuroscience 116 (2002) 928-934
53. Izquierdo I., and Medina J.H. Memory formation: The sequence of biochemical events in the hippocampus and its connection to activity in other brain structures. Neurobiology of Learning and Memory 68 (1997) 285-316
54. Joyce J.N., and Van Hartesveldt C. Estradiol application to one striatum produces postural deviation to systemic apomorphine. Pharmacology, Biochemistry, and Behavior 20 (1984) 575-581
55. Kiray M., Uysal N., Sonmez A., Acikgoz O., and Gonenc S. Positive effects of deprenyl and estradiol on spatial memory and oxidant stress in aged female rat brains. Neuroscience Letters 354 (2004) 225-228
56. Korol D.L. Role of estrogen in balancing contributions from multiple memory systems. Neurobiology of Learning and Memory 82 (2004) 309-323
57. Korol D.L., and Kolo L.L. Estrogen-induced changes in place and response learning in young adult female rats. Behavioral Neuroscience 116 (2002) 411-420
58. Long J.A., and Evans H.M. Oestrus cycle in the rat and its associated phenomena. Memoirs of the University of California 6 (1922) 1-22
59. Luine V.N., Jacome L.F., and Maclusky N.J. Rapid enhancement of visual and place memory by estrogens in rats. Endocrinology 144 (2003) 2836-2844
60. Luine V.N., Richards S.T., Wu V.Y., and Beck K.D. Estradiol enhances learning and memory in a spatial memory task and effects levels of monoaminergic neurotransmitters. Hormones and Behavior 34 (1998) 149-162
61. Lund T.D., and Lephart E.D. Manipulation of prenatal hormones and dietary phytoestrogens during adulthood alter the sexually dimorphic expression of visual spatial memory. BMC Neuroscience 2 (2001) 21
62. Malendowicz L.K. Sex differences in adrenocortical structure and function. III. The effects of postpubertal gonadectomy and gonadal hormone replacement on adrenal cholesterol sidechain cleavage activity and on steroids biosynthesis by rat adrenal homogenates. Endokrinologie 67 (1976) 26-35
63. Marriott L.K., and Korol D.L. Short-term estrogen treatment in ovariectomized rats augments hippocampal acetylcholine release during place learning. Neurobiology of Learning and Memory 80 (2003) 315-322
64. Martini L., Celotti F., and Melcangi R.C. Testosterone and progesterone metabolism in the central nervous system: cellular localization and mechanism of control of the enzymes involved. Cellular Molecular Neurobiology 16 (1996) 271-282
65. McEchron M.D., Cheng A.Y., and Gilmartin M.R. Trace fear conditioning is reduced in the aging rat. Neurobiology of Learning and Memory 82 (2004) 71-76
66. Meyers M.J., Sun J., Carlson K.E., Marriner G.A., Katzenellenbogen B.S., and Katzenellenbogen J.A. Estrogen receptor-β potency-selective ligands: Structure-activity relationship studies of diarylpropionitriles and their acetylene and polar analogues. Journal of medicinal chemistry 44 (2001) 4230-4235
67. Miller M.M., Hyder S.M., Assayag R., Panarella S.R., Tousignant P., and Franklin K.B. Estrogen modulates spontaneous alternation and the cholinergic phenotype in the basal forebrain. Neuroscience 91 (1999) 1143-1153
68. Mora S., Dussaubat N., and Diaz-Veliz G. Effects of the estrous cycle and ovarian hormones on behavioral indices of anxiety in female rats. Psychoneuroendocrinology 21 (1996) 609-620
69. Morgan M.A., and Pfaff D.W. Effects of estrogen on activity and fear-related behaviors in mice. Hormones and Behavior 40 (2001) 472-482
70. Morgan M.A., and Pfaff D.W. Estrogen's effects on activity, anxiety, and fear in two mouse strains. Behavioural Brain Research 132 (2002) 85-93
71. Morgan M.A., Schulkin J., and Pfaff D.W. Estrogens and non-reproductive behaviors related to activity and fear. Neuroscience and Biobehavioral Reviews 28 (2004) 55-63
72. O'Neal M.F., Means L.W., Poole M.C., and Hamm R.J. Estrogen affects performance of ovariectomized rats in a two-choice water-escape working memory task. Psychoneuroendocrinology 21 (1996) 51-65
73. Packard M.G. Posttraining estrogen and memory modulation. Hormones and Behavior 34 (1998) 126-139
74. Purdy R.H., Moore Jr. P.H., Rao P.N., Hagino N., Yamaguchi T., Schmidt P., et al. Radioimmunoassay of 3α-hydroxy-5α-pregnan-20-one in rat and human plasma. Steroids 55 (1990) 290-296
75. Resko J.A., Stadelman H.L., and Handa R.J. Control of 5α-reduction of testosterone in neuroendocrine tissues of female rats. Biology of Reproduction 34 (1986) 870-877
76. Rhodes M.E., and Frye C.A. Hormones influence cognitive performance. In: Flint R. (Ed). Forget it? -Sources, Theories, and Mechanisms of Alterations in Mnemonic Function (2002), Erudition Books, North Chelmsford, MA 175-196
77. Rhodes M.E., and Frye C.A. Estrogen has mnemonic enhancing effects in the inhibitory avoidance task. Pharmacology, Biochemistry, and Behavior 78 (2004) 551-558
78. Rhodes M.E., and Frye C.A. Progestins in the hippocampus of female rats have antiseizure effects in a pentylenetetrazole seizure model. Epilepsia 45 (2004) 1531-1538
79. Rhodes, M. E., & Frye, C. A. (in press). ERβ-selective SERMs produce mnemonic enhancing effects in the inhibitory avoidance and water maze tasks. Neurobiology of Learning and Memory.
80. Rhodes M.E., McCormick C.M., and Frye C.A. 3α, 5α-THP mediates progestins' effects to protect against adrenalectomy-induced cell death in the dentate gyrus of female and male rats. Pharmacology, Biochemistry, and Behavior 78 (2004) 505-512
81. Rissman E.F., Heck A.L., Leonard J.E., Shupnik M.A., and Gustafsson J.A. Disruption of estrogen receptor β gene impairs spatial learning in female mice. Proceedings of the National Academy of Sciences 99 (2002) 3996-4001
82. Sandstrom N.J., and Williams C.L. Memory retention is modulated by acute estradiol and progesterone replacement. Behavioral Neuroscience 115 (2001) 384-393
83. Sandstrom N.J., and Williams C.L. Spatial memory retention is enhanced by acute and continuous estradiol replacement. Hormones and Behavior 45 (2004) 128-135
84. Sato T., Tanaka K., Ohnishi Y., Teramoto T., Irifune M., and Nishikawa T. Effects of estradiol and progesterone on radial maze performance in middle-aged female rats fed a low-calcium diet. Behavioral Brain Research 150 (2004) 33-42
85. Shors T.J., Lewczyk C., Pacynski M., Mathew P.R., and Pickett J. Stages of estrous mediate the stress-induced impairment of associative learning in the female rat. Neuroreport 9 (1998) 419-423
86. Shughrue P.J., Lane M.V., and Merchenthaler I. Comparative distribution of estrogen receptor-α and -β mRNA in the rat central nervous system. Journal of Comparative Neurology 388 (1997) 507-525
87. Shughrue P.J., Scrimo P.J., and Merchenthaler I. Evidence for the colocalization of estrogen receptor-β mRNA and estrogen receptor-α immunoreactivity in neurons of the rat forebrain. Endocrinology 139 (1998) 5267-5270
88. Stackman R.W., Blasberg M.E., Langan C.J., and Clark A.S. Stability of spatial working memory across the estrous cycle of Long-Evans rats. Neurobiology of Learning and Memory 67 (1997) 167-171
89. Stauffer S.R., Coletta C.J., Tedesco R., Nishiguchi G., Carlson K., Sun J., et al. Pyrazole ligands: Structure-affinity/activity relationships and estrogen receptor-alpha-selective agonists. Journal of medicinal chemistry 43 (2000) 4934-4947
90. Vaucher E., Reymond I., Najaffe R., Kar S., Quirion R., Miller M.M., et al. Estrogen effects on object memory and cholinergic receptors in young and old female mice. Neurobiology of Aging 23 (2002) 87-95
91. Vazquez-Pereyra F., Rivas-Arancibia S., Loaeza-Del Castillo A., and Schneider-Rivas S. Modulation of short term and long term memory by steroid sexual hormones. Life Science 56 (1995) PL255-PL260
92. Vongher J.M., and Frye C.A. Progesterone in conjunction with estradiol has neuroprotective effects in an animal model of neurodegeneration. Pharmacology, Biochemistry, and Behavior 64 (1999) 777-785
93. Warren S.G., and Juraska J.M. Sex differences and estropausal phase effects on water maze performance in aged rats. Neurobiology of learning and Memory 74 (2000) 229-240
94. Warren S.G., and Juraska J.M. Spatial and nonspatial learning across the rat estrous cycle. Behavioral Neuroscience 111 (1997) 259-266
95. Wood G.E., Beylin A.V., and Shors T.J. The contribution of adrenal and reproductive hormones to the opposing effects of stress on trace conditioning in males versus females. Behavioral Neuroscience 115 (2001) 175-187
96. Wide J.K., Hanratty K., Ting J., and Galea L.A. High level estradiol impairs and low level estradiol facilitates non-spatial working memory. Behavioral Brain Research 155 (2004) 45-53