Acute stress impairs spatial memory in male but not female rats: Influence of estrous cycle

Pharmacology Biochemistry and Behavior

Volumn 78, Issue 3, 2004, Pages 569-579

  Conrad, Cheryl D ^a   Jackson, Jamie L ^a   Wieczorek, Lindsay ^a   Baran, Sarah E ^a   Harman, James S ^a   Wright, Ryan L ^a   Korol, Donna L ^b  

^a ARIZONA STATE UNIVERSITY   (United States)

^b UNIVERSITY OF ILLINOIS AT URBANA CHAMPAIGN   (United States)

Author keywords

Acute stress; Estrus; Female; Proestrus; Sex difference; Spatial memory

Indexed keywords

CORTICOSTERONE;

ANIMAL CELL; ANIMAL EXPERIMENT; CONFERENCE PAPER; CONTROLLED STUDY; ESTRUS CYCLE; FEMALE; HIPPOCAMPUS; HORMONE RESPONSE; IMMOBILIZATION STRESS; MALE; MAZE TEST; MEMORY DISORDER; NONHUMAN; PRIORITY JOURNAL; PROESTRUS; RAT; SEX DIFFERENCE; SPATIAL MEMORY;

ACUTE DISEASE; ANIMALS; CORTICOSTERONE; ESTRUS; FEMALE; MALE; MAZE LEARNING; MEMORY DISORDERS; RATS; RATS, SPRAGUE-DAWLEY; SEX CHARACTERISTICS; STRESS, PSYCHOLOGICAL;

EID: 3142572476     PISSN: 00913057     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.pbb.2004.04.025     Document Type: Conference Paper

References (75)

1. Adamec R.E., Shallow T. Lasting effects on rodent anxiety of a single exposure to a cat. Physiol. Behav. 54:1993;101-109
2. Baker K.B., Kim J.J. Effects of stress and hippocampal NMDA receptor antagonism on recognition memory in rats. Learn. Mem. 9:2002;58-65
3. Beatty W.W. Gonadal hormones and sex differences in nonreproductive behaviors. Gerall A.A., Moltz H., Ward I.L. Sexual differentiation. 1992;85-128 Plenum, New York (NY)
4. Beck K.D., Luine V.N. Sex differences in behavioral and neurochemical profiles after chronic stress: role of housing conditions. Physiol. Behav. 75:2002;661-673
5. Berry B., McMahan R., 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
6. Blank T., Nijholt I., Eckart K., Spiess J. Priming of long-term potentiation in mouse hippocampus by corticotropin-releasing factor and acute stress: implications for hippocampus-dependent learning. J. Neurosci. 22:2002;3788-3794
7. Bowman R.E., Zrull M.C., Luine V.N. Chronic restraint stress enhances radial arm maze performance in female rats. Brain Res. 904:2001;279-289
8. Bowman R.E., Ferguson D., Luine V.N. Effects of chronic restraint stress and estradiol on open field activity, spatial memory, and monoaminergic neurotransmitters in ovariectomized rats. Neuroscience. 113:2002;401-410
9. Bowman R.E., Beck K.D., Luine V.N. Chronic stress effects on memory: sex differences in performance and monoaminergic activity. Horm. Behav. 43:2003;48-59
10. Cabib S., Castellano C., Patacchioli F.R., Cigliana G., Angelucci L., Puglisi-Allegra S. Opposite strain-dependent effects of post-training corticosterone in a passive avoidance task in mice: role of dopamine. Brain Res. 729(1):1996;110-118
11. Cahill L., McGaugh J.L. Mechanisms of emotional arousal and lasting declarative memory. TINS. 21:1998;273-313
12. Conrad CD. The relationship between acute glucocorticoid levels and hippocampal function depends upon task aversiveness and memory processing stage. Nonlinear Biol Toxicol Med [in press].
13. Conrad C.D., Galea L.A.M., Kuroda Y., McEwen B.S. Chronic stress impairs rat spatial memory on the Y-maze, and this effect is blocked by tianeptine pretreatment. Behav. Neurosci. 110(6):1996;1321-1334
14. Conrad C.D., Lupien S.J., Thanasoulis L.C., McEwen B.S. The effects of Type I and Type II corticosteroid receptor agonists on exploratory behavior and spatial memory in the Y-maze. Brain Res. 759:1997;76-83
15. Conrad C.D., Lupien S.J., McEwen B.S. Support for a bimodal role for Type II adrenal steroid receptors in spatial memory. Neurobiol. Learn. Mem. 72(1):1999;39-46
16. Conrad C.D., Magariños A.M., LeDoux J.E., McEwen B.S. Repeated restraint stress facilitates fear conditioning independently of causing hippocampal CA3 dendritic atrophy. Behav. Neurosci. 113(5):1999;902-913
17. Conrad C.D., Grote K.A., Hobbs R.J., Ferayorni A. Sex differences in spatial and non-spatial Y-maze performance after chronic stress. Neurobiol. Learn. Mem. 79:2003;32-40
18. Critchlow V., Liebelt R.A., Bar-Sela M., Mountcastle W., Lipscomb H.S. Sex difference in resting pituitary-adrenal function in the rat. Am. J. Physiol. 205(5):1963;807-815
19. Dellu F., Mayo W., Cherkaoui J., Moal M.L., Simon H. A two-trial memory task with automated recording: study in young and aged rats. Brain Res. 588:1992;132-139
20. Diamond D.M., Fleshner M., Ingersoll N., Rose G.M. Psychological stress impairs spatial working memory: relevance to electrophysiological studies of hippocampal function. Behav. Neurosci. 110(4):1996;661-672
21. Diamond D.M., Park C.R., Heman K.L., Rose G.M. Exposing rats to a predator impairs spatial working memory in the radial arm water maze. Hippocampus. 9:1999;542-552
22. Dohanich G.P. Gonadal steroids, learning and memory. Pfaff D.W., Arnold A.P., Etgen A.M., Fahrback S.E., Rubin R.T. Hormones, brain and behavior. 2002;265-327 Academic Press, San Diego (CA)
23. Ennaceur A., Delacour J. A new one-trial test for neurobiological studies of memory in rats: 1. behavioral data. Behav. Brain Res. 31:1988;47-59
24. Figueiredo H.F., Dolgas C.M., Herman J.P. Stress activation of cortex and hippocampus is modulated by sex and stage of estrus. Endocrinology. 143:2002;2534-2540
25. Frye C.A. Estrus-associated decrements in a water maze task are limited to acquisition. Physiol. Behav. 57:1995;5-14
26. Galea L.A.M., McEwen B.S., Tanapat P., Deak T., Spencer R.L., Dhabhar F.S. Sex differences in dendritic atrophy of CA3 pyramidal neurons in response to chronic restraint stress. Neuroscience. 81(3):1997;689-697
27. Haleem D.J., Kennett G., Curzon G. Adaptation of female rats to stress: shift to male pattern by inhibition of corticosterone synthesis. Brain Res. 458:1988;339-347
28. Handa R.J., Burgess L.H., Kerr J.E., O'Keefe J.A. Gonadal steroid hormone receptors and sex differences in the hypothalamo-pituitary-adrenal axis. Horm. Behav. 28:1994;464-479
29. Heinrichs S.C., Menzaghi F., Pich E.M., Baldwin H.A., Rassnick S., Britton K.T., et al. Anti-stress action of a corticotropin-releasing factor antagonist on behavioral reactivity to stressors of varying type and intensity. Neuropsychopharmacology. 11:1994;179-186
30. Johnston A.N.B., Rose S.P.R. Isolation-stress-induced facilitation of passive avoidance memory in the day-old chick. Behav. Neurosci. 112(4):1998;929-936
31. Kant G.J., Lenox R.H., Bunnell B.N., Mougey E.H., Pennington L.L., 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
32. Karandrea D., Kittas C., Kitraki E. Contribution of sex and cellular context in the regulation of brain corticosteroid receptors following restraint stress. Neuroendocrinology. 71:2000;343-353
33. Kim J.J., Baxter M.G. Multiple brain-memory systems: the whole does not equal the sum of its parts. TINS. 24:2001;324-330
34. Kim J.J., Diamond D.M. The stressed hippocampus, synaptic plasticity and lost memories. Nat. Neurosci. 3:2002;453-462
35. Kim J.J., Lee H.J., Han J.-S., Packard M.G. Amygdala is critical for stress-induced modulation of hippocampal long-term potentiation and learning. J. Neurosci. 21:2001;5222-5228
36. Kirschbaum C., Wüst S., Hellhammer D. Consistent sex differences in cortisol responses to psychological stress. Psychosom. Med. 54:1992;648-657
37. Kitay J.I. Sex differences in adrenal cortical secretion in the rat. Endocrinology. 68:1961;818-824
38. Korol D.L., Kolo L.L. Estrogen-induced changes in place and response learning in young adult female rats. Behav. Neurosci. 116:2002;411-420
39. LeDoux J.E. Emotion circuits in the brain. Annu. Rev. Neurosci. 23:2000;155-184
40. Le Mevel J.C., Abitbol S., Beraud G., Maniey J. Temporal changes in plasma adrenocorticotrophin concentration after repeated neurotropic stress in male and female rats. Endocrinology. 105:1979;812-817
41. Livezey G.T., Miller J.M., Vogel W.H. Plasma norepinephrine, epinephrine and corticosterone stress responses to restraint in individual male and female rats, and their correlations. Neurosci. Lett. 62:1985;51-56
42. Long J.A., Evans H.M. The oestrous cycle in the rat and its associated phenomena. Mem. Univ. Calif. 6:1922;1-148
43. Luine V., Villegas M., Martinez C., McEwen B.S. Repeated stress causes reversible impairments of spatial memory performance. Brain Res. 639:1994;167-170
44. MacLusky N.J., Yuan H., Elliot J., Brown T.J. Sex differences in corticosteroid binding in the rat brain: an in vitro autoradiographic study. Brain Res. 708(1-2):1996;71-81
45. Magariños A.M., McEwen B.S. Stress-induced atrophy of apical dendrites of hippocampal CA3c neurons: comparison of stressors. Neuroscience. 69(1):1995;83-88
46. Markus E.J., Zecevic M. Sex differences and estrous cycle changes in hippocampus-dependent fear conditioning. Psychobiology. 25(3):1997;246-252
47. Maroun M., Richter-Levin G. Exposure to acute stress blocks the induction of long-term potentiation of the amygdala-prefrontal cortex pathway in vivo. J. Neurosci. 23:2003;4406-4409
48. McEwen B.S., Sapolsky R.M. Stress and cognitive function. Curr. Opin. Neurobiol. 5:1995;205-216
49. Padovan C.M., Guimarães F.S. Restraint-induced hypoactivity in an elevated plus-maze. Braz. J. Med. Biol. Res. 33:2000;79-83
50. Paré W.P. Enhanced retrieval of unpleasant memories influenced by shock controllability, shock sequence, and rat strain. Biol. Psychiatry. 39:1996;808-813
51. Park C.R., Campbell A.M., Diamond D.M. Chronic psychosocial stress impairs learning and memory and increases sensitivity to yohimbine in rats. Biol. Psychiatry. 50:2001;994-1004
52. Perrot-Sinal T.S., Kostenuik M.A., Ossenkopp K.-P., Kavaliers M. Sex differences in performance in the Morris water maze and the effects of initial nonstationary hidden platform training. Behav. Neurosci. 110:1996;1309-1320
53. Rhodes M.E., Frye C.A. Estrogen has mnemonic-enhancing effects in the inhibitory avoidance task. Pharm. Biochem. Behav. 78:2004;551-558. in this issue
54. Sananbenesi F., Fischer A., Schrick C., Spiess J., Radulovic J. Mitogen-activated protein kinase signaling in the hippocampus and its modulation by corticotropin-releasing factor receptor 2: a possible link between stress and fear memory. J. Neurosci. 23:2003;11436-11443
55. Sandi C. The role and mechanisms of action of glucocorticoid involvement in memory storage. Neural Plast. 6:1998;41-52
56. Shors T.J. Acute stress rapidly and persistently enhances memory formation in the male rat. Neurobiol. Learn Mem. 75:2001;19-29
57. Shors T.J., Dryver E. Stress impedes exploration and the acquisition of spatial information in the eight-arm radial maze. Psychobiology. 20(4):1992;247-253
58. Shors T.J., Weiss C., Thompson R.F. Stress-induced facilitation of classical conditioning. Science. 257:1992;537-539
59. Shors T.J., Lewczyk C., Pacynski M., Matthew P.R., Pickett J. Stages of estrous mediate the stress-induced impairment of associative learning in the female rat. NeuroReport. 9:1998;419-423
60. Shors T.J., Pickett J., Wood G., Paczynski M. Acute stress persistently enhances estrogen levels in the female rat. Stress. 3(2):1999;163-171
61. Shors T.J., Beylin A.V., Wood G.E., Gould E. The modulation of Pavlovian memory. Behav. Brain Res. 110:2000;39-52
62. Shors T.J., Chua C., Falduto J. Sex differences and opposite effects of stress on dendritic spine density in the male versus female hippocampus. J. Neurosci. 21:2001;6292-6297
63. Sousa N., Lukoyanov N.V., Madeira M.D., Almeida O.F.X., Paula-Barbosa M.M. Reorganization of the morphology of hippocampal neurites and synapses after stress-induced damage correlates with behavioral improvement. Neuroscience. 97:2000;253-266
64. Stackman R.W., Blasberg M.E., Langan C.J., Clark A.S. Stability of spatial working memory across the estrous cycle of Long-Evans rats. Neurobiol. Learn Mem. 67:1997;167-171
65. Turner B.B. Sex differences in the binding of Type I and Type II corticosteroid receptors in rat hippocampus. Brain Res. 581:1992;229-236
66. Turner B.B., Weaver D.A. Sexual dimorphism of glucocorticoid binding in rat brain. Brain Res. 343:1985;16-23
67. Viau V., 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
68. Warren S.G., Juraska J.M. Spatial and nonspatial learning across the rat estrous cycle. Behav. Neurosci. 111(2):1997;259-266
69. Warren D.A., Castro C.A., Rudy J.W., Maier S.F. No spatial learning impairment following exposure to inescapable shock. Psychobiology. 19:1991;127-134
70. Watanabe Y., Gould E., McEwen B.S. Stress induces atrophy of apical dendrites of hippocampal CA3 pyramidal neurons. Brain Res. 588:1992;341-345
71. Wilson M.A., Biscardi R. Sex differences in GABA/benzodiazepine receptor changes and corticosterone release after acute stress in rats. Exp. Brain Res. 101:1994;297-306
72. Wolf O.T., Schommer N.C., Hellhammer D.H., McEwen B.S., Kirschbaum C. The relationship between stress induced cortisol levels and memory differs between men and women. Psychoneuroendocrinology. 26:2001;711-720
73. Wood G.E., Shors T.J. Stress facilitates classical conditioning in males, but impairs classical conditioning in females through activational effects of ovarian hormones. PNAS. 95:1998;4066-4071
74. Wood G.E., Beylin A.V., Shors T.J. The contribution of adrenal and reproductive hormones to the opposing effects of stress on trace conditioning in males versus females. Behav. Neurosci. 115:2001;175-187
75. Youngblood B.D., Ryan D.H., Harris R.B.S. Appetitive operant behavior and free-feeding in rats exposed to acute stress. Physiol. Behav. 62:1997;827-830