Differential effects of ovarian steroids on anxiety versus fear as measured by open field test and fear-potentiated startle

Behavioural Brain Research

Volumn 166, Issue 1, 2006, Pages 93-100

  Hiroi, Ryoko ^a   Neumaier, John F ^b  

^a UNIVERSITY OF WASHINGTON   (United States)

^b UNIVERSITY OF WASHINGTON SCHOOL OF MEDICINE   (United States)

Author keywords

Estrogen; Estrous cycle; Fear conditioning; Fear learning; Ovariectomy; Pain sensitivity; Progesterone; Rats

Indexed keywords

ESTROGEN; PROGESTERONE;

ANIMAL BEHAVIOR; ANIMAL EXPERIMENT; ANXIETY; ARTICLE; CONTROLLED STUDY; DIESTRUS; FEAR; FEMALE; HORMONE ACTION; LEARNING; MENSTRUAL CYCLE; NONHUMAN; OPEN FIELD TEST; OVARIECTOMY; OVARY; PRIORITY JOURNAL; PROESTRUS; RAT; STARTLE REFLEX; TASK PERFORMANCE;

ANALYSIS OF VARIANCE; ANIMALS; ANXIETY; BEHAVIOR, ANIMAL; CONDITIONING (PSYCHOLOGY); DRUG DELIVERY SYSTEMS; ESTROGENS; ESTROUS CYCLE; EXPLORATORY BEHAVIOR; FEAR; FEMALE; OVARIECTOMY; PAIN MEASUREMENT; PROGESTERONE; RADIOIMMUNOASSAY; RATS; RATS, SPRAGUE-DAWLEY; STARTLE REACTION; VAGINAL SMEARS;

EID: 27944475942     PISSN: 01664328     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.bbr.2005.07.021     Document Type: Article

References (76)

1. A. Adell, J.M. Casanovas, and F. Artigas Comparative study in the rat of the actions of different types of stress on the release of 5-HT in raphe nuclei and forebrain areas Neuropharmacology 36 1997 735 741
2. Y. Akwa, R.H. Purdy, G.F. Koob, and K.T. Britton The amygdala mediates the anxiolytic-like effect of the neurosteroid allopregnanolone in rat Behav Brain Res 106 1999 119 125
3. J.C. Arpels The female brain hypoestrogenic continuum from the premenstrual syndrome to menopause. A hypothesis and review of supporting data J Reprod Med 41 1996 633 639
4. N.R. Best, M.P. Rees, D.H. Barlow, and P.J. Cowen Effect of estradiol implant on noradrenergic function and mood in menopausal subjects Psychoneuroendocrinology 17 1992 87 93
5. C.L. Bethea, N.Z. Lu, C. Gundlah, and J.M. Streicher Diverse actions of ovarian steroids in the serotonin neural system Front Neuroendocrinol 23 2002 41 100
6. D. Bitran, and J.A. Dowd Ovarian steroids modify the behavioral and neurochemical responses of the central benzodiazepine receptor Psychopharmacology (Berl) 125 1996 65 73
7. D. Bitran, R.J. Hilvers, and C.K. Kellogg Ovarian endocrine status modulates the anxiolytic potency of diazepam and the efficacy of δ-aminobutyric acid-benzodiazepine receptor-mediated chloride ion transport Behav Neurosci 105 1991 653 662
8. D. Bitran, M. Shiekh, and M. McLeod Anxiolytic effect of progesterone is mediated by the neurosteroid allopregnanolone at brain GABAA receptors J Neuroendocrinol 7 1995 171 177
9. L. Bogic, J.L. Gerlach, and B.S. McEwen The ontogeny of sex differences in estrogen-induced progesterone receptors in rat brain Endocrinology 122 1988 2735 2741
10. 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
11. J.S. Brown, H.I. Kalish, and I.E. Farber Conditioned fear as revealed by magnitude of startle response to an auditory stimulus J Exp Psychol 41 1951 317 328
12. I. Camacho-Arroyo, C. Guerra-Araiza, and M.A. Cerbon Progesterone receptor isoforms are differentially regulated by sex steroids in the rat forebrain Neuroreport 9 1998 3993 3996
13. M.S. Clark, E.S. Vincow, T.J. Sexton, and J.F. Neumaier Increased expression of 5-HT1B receptor in dorsal raphe nucleus decreases fear-potentiated startle in a stress dependent manner Brain Res 1007 2004 86 97
14. M.S. Clark, T.J. Sexton, M. McClain, D. Root, R. Kohen, and J.F. Neumaier Overexpression of 5-HT1B receptor in dorsal raphe nucleus using Herpes Simplex Virus gene transfer increases anxiety behavior after inescapable stress J Neurosci 22 2002 4550 4562
15. E. Costa Benzodiazepines and neurotransmitters Arzneimittelforschung 30 1980 858 861
16. J.M. Daniel, A.J. Fader, A.L. Spencer, and G.P. Dohanich Estrogen enhances performance of female rats during acquisition of a radial arm maze Horm Behav 32 1997 217 225
17. M. Davis Neural systems involved in fear-potentiated startle Ann NY Acad Sci 563 1989 165 183
18. M. Davis Are different parts of the extended amygdala involved in fear versus anxiety? Biol Psychiatr 44 1998 1239 1247
19. M. Davis, and C. Shi The extended amygdala: are the central nucleus of the amygdala and the bed nucleus of the stria terminalis differentially involved in fear versus anxiety? Ann NY Acad Sci 877 1999 281 291
20. G. Diaz-Veliz, V. Soto, N. Dussaubat, and S. Mora Influence of the estrous cycle, ovariectomy and estradiol replacement upon the acquisition of conditioned avoidance responses in rats Physiol Behav 46 1989 397 401
21. G. Diaz-Veliz, F. Urresta, N. Dussaubat, and S. Mora Effects of estradiol replacement in ovariectomized rats on conditioned avoidance responses and other behaviors Physiol Behav 50 1991 61 65
22. G. Diaz-Veliz, F. Urresta, N. Dussaubat, and S. Mora Progesterone effects on the acquisition of conditioned avoidance responses an other motoric behaviors in intact and ovariectomized rats Psychoneuroendocrinology 19 1994 387 394
23. G. Diaz-Veliz, M.S. Benavides, S. Butron, N. Dussaubat, and S. Mora Behavioral effects of dopamine agonists and antagonists: influence of estrous cycle, ovariectomy, and estrogen replacement in rats Pharmacol Biochem Behav 62 1999 21 29
24. G. Diaz-Veliz, S. Butron, M.S. Benavides, N. Dussaubat, and S. Mora Gender estrous cycle, ovariectomy, and ovarian hormones influence the effects of diazepam on avoidance conditioning in rats Pharmacol Biochem Behav 66 2000 887 892
25. M. Durand, O. Berton, S. Aguerre, L. Edno, I. Combourieu, and P. Mormede Effects of repeated fluoxetine on anxiety-related behaviours, central serotonergic systems, and the corticotropic axis in SHR and WKY rats Neuropharmacology 38 1999 893 907
26. E. Estrada-Camarena, A. Fernandez-Guasti, and C. Lopez-Rubalcava Antidepressant-like effect of different estrogenic compounds in the forced swimming test Neuropsychopharmacology 28 2003 830 838
27. M. Fendt, and M.S. Fanselow The neuroanatomical and neurochemical basis of conditioned fear Neurosci Biobehav Rev 23 1999 743 760
28. M.E. Freeman The neuroendocrine control of the ovarian cycle of the rat E. Knobil J.D. Neill The physiology of reproduction 2nd ed. 1994 Raven Press Ltd. New York 613 648
29. K.M. Frick, S.M. Fernandez, and S.C. Bulinski Estrogen replacement improves spatial reference memory and increases hippocampal synaptophysin in aged female mice Neuroscience 115 2002 547 558
30. C.A. Frye, S.M. Petralia, and M.E. Rhodes Estrous cycle and sex differences in performance on anxiety tasks coincide with increases in hippocampal progesterone and 3α,5α-THP Pharmacol Biochem Behav 67 2000 587 596
31. F.G. Graeff Minor tranquilizers and brain defense systems Braz J Med Biol Res 14 1981 239 265
32. A.J. Gregoire, R. Kumar, B. Everitt, A.F. Henderson, and J.W. Studd Transdermal oestrogen for treatment of severe postnatal depression Lancet 347 1996 930 933
33. R.R. Gupta, S. Sen, L.L. Diepenhorst, C.N. Rudick, and S. Maren Estrogen modulates sexually dimorphic contextual fear conditioning and hippocampal long-term potentiation (LTP) in rats(1) Brain Res 888 2001 356 365
34. D.A. Haas, B. Borgundvaag, W.C. Sturtridge, and S.R. George Hypothalamic corticotropin-releasing factor immunoreactivity is reduced during induction of pituitary tumors by chronic estrogen treatment Life Sci 41 1987 2101 2106
35. M. Hamon, C. Goetz, C. Euvrard, C. Pasqualini, M. Le Dafniet, and B. Kerdelhue Biochemical and functional alterations of central GABA receptors during chronic estradiol treatment Brain Res 279 1983 141 152
36. V.W. Henderson Estrogen, cognition, and a woman's risk of Alzheimer's disease Am J Med 103 1997 11S 18S
37. A.G. Herzog Psychoneuroendocrine aspects of temporolimbic epilepsy. Part I. Brain, reproductive steroids, and emotions Psychosomatics 40 1999 95 101
38. W.G. Hope, M.E. Bruns, and M.L. Thomas Regulation of duodenal insulin-like growth factor I and active calcium transport by ovariectomy in female rats Proc Soc Exp Biol Med 200 1992 528 535
39. J. Izumi, M. Washizuka, Y. Hayashi-Kuwabara, K. Yoshinaga, Y. Tanaka, and Y. Ikeda Evidence for a depressive-like state induced by repeated saline injections in Fischer 344 rats Pharmacol Biochem Behav 57 1997 883 888
40. G.F. Koob, and S.C. Heinrichs A role for corticotropin releasing factor and urocortin in behavioral responses to stressors Brain Res 848 1999 141 152
41. M.K. Lindberg, S. Moverare, S. Skrtic, H. Gao, K. Dahlman-Wright, and J.A. Gustafsson Estrogen receptor (ER)-β reduces ER-α-regulated gene transcription, supporting a "ying yang" relationship between ER-α and ER-β in mice Mol Endocrinol 17 2003 203 208
42. M.M. Liu, C. Albanese, C.M. Anderson, K. Hilty, P. Webb, and R.M. Uht Opposing action of estrogen receptors α and β on cyclin D1 gene expression J Biol Chem 277 2002 24353 24360
43. C.A. Lowry, J.E. Rodda, S.L. Lightman, and C.D. Ingram Corticotropin-releasing factor increases in vitro firing rates of serotonergic neurons in the rat dorsal raphe nucleus: evidence for activation of a topographically organized mesolimbocortical serotonergic system J Neurosci 20 2000 7728 7736
44. T.D. Lund, T. Rovis, W.C. Chung, and R.J. Handa Novel actions of estrogen receptor-β on anxiety-related behaviors Endocrinology 146 2005 797 807
45. A. Maggi, and J. Perez Progesterone and estrogens in rat brain: modulation of GABA (δ-aminobutyric acid) receptor activity Eur J Pharmacol 103 1984 165 168
46. L. Martinez-Mota, E. Estrada-Camarena, C. Lopez-Rubalcava, C.M. Contreras, and A. Fernandez-Guasti Interaction of desipramine with steroid hormones on experimental anxiety Psychoneuroendocrinology 25 2000 109 120
47. S. Maswood, J.E. Barter, L.R. Watkins, and S.F. Maier Exposure to inescapable but not escapable shock increases extracellular levels of 5-HT in the dorsal raphe nucleus of the rat Brain Res 783 1998 115 120
48. J. Matthews, and J.A. Gustafsson Estrogen signaling: a subtle balance between ER-α and ER-β Mol Interv 3 2003 281 292
49. S. Mora, N. Dussaubat, and G. Diaz-Veliz Effects of the estrous cycle and ovarian hormones on behavioral indices of anxiety in female rats Psychoneuroendocrinology 21 1996 609 620
50. M.A. Morgan, J. Schulkin, and D.W. Pfaff Estrogens and non-reproductive behaviors related to activity and fear Neurosci Biobehav Rev 28 2004 55 63
51. M. Osterlund, G.G. Kuiper, J.A. Gustafsson, and Y.L. Hurd Differential distribution and regulation of estrogen receptor-α and -β mRNA within the female rat brain Brain Res Mol Brain Res 54 1998 175 180
52. W.P. Pare Open field, learned helplessness, conditioned defensive burying, and forced-swim tests in WKY rats Physiol Behav 55 1994 433 439
53. T.A. Pigott Anxiety disorders in women Psychiatr Clin N Am 26 2003 621 672 (vi-vii)
54. A. Ramos, O. Berton, P. Mormede, and F. Chaouloff A multiple-test study of anxiety-related behaviours in six inbred rat strains Behav Brain Res 85 1997 57 69
55. A. Ramos, A.L. Kangerski, P.F. Basso, J.E. Da Silva Santos, J. Assreuy, and L.F. Vendruscolo Evaluation of Lewis and SHR rat strains as a genetic model for the study of anxiety and pain Behav Brain Res 129 2002 113 123
56. S. Rivas-Arancibia, and F. Vazquez-Pereyra Hormonal modulation of extinction responses induced by sexual steroid hormones in rats Life Sci 54 1994 PL363 PL367
57. R.J. Rodgers, and N.J. Johnson Behaviorally selective effects of neuroactive steroids on plus-maze anxiety in mice Pharmacol Biochem Behav 59 1998 221 232
58. B.N. Roy, R.L. Reid, and D.A. Van Vugt The effects of estrogen and progesterone on corticotropin-releasing hormone and arginine vasopressin messenger ribonucleic acid levels in the paraventricular nucleus and supraoptic nucleus of the rhesus monkey Endocrinology 140 1999 2191 2198
59. D.R. Rubinow, P.J. Schmidt, and C.A. Roca Estrogen-serotonin interactions: implications for affective regulation Biol Psychiatr 44 1998 839 850
60. P.J. Schmidt, L.K. Nieman, M.A. Danaceau, L.F. Adams, and D.R. Rubinow Differential behavioral effects of gonadal steroids in women with and in those without premenstrual syndrome N Engl J Med 338 1998 209 216
61. S.L. Sell, J.M. Scalzitti, M.L. Thomas, and K.A. Cunningham Influence of ovarian hormones and estrous cycle on the behavioral response to cocaine in female rats J Pharmacol Exp Ther 293 2000 879 886
62. B.B. Sherwin Estrogen and cognitive functioning in women Proc Soc Exp Biol Med 217 1998 17 22
63. P.J. Shughrue, M.V. Lane, and I. Merchenthaler Comparative distribution of estrogen receptor-α and -β mRNA in the rat central nervous system J Comp Neurol 388 1997 507 525
64. P.J. Shughrue, M.V. Lane, and I. Merchenthaler Regulation of progesterone receptor messenger ribonucleic acid in the rat medial preoptic nucleus by estrogenic and antiestrogenic compounds: an in situ hybridization study Endocrinology 138 1997 5476 5484
65. D.A. Sichel, L.S. Cohen, L.M. Robertson, A. Ruttenberg, and J.F. Rosenbaum Prophylactic estrogen in recurrent postpartum affective disorder Biol Psychiatr 38 1995 814 818
66. R.B. Simerly, C. Chang, M. Muramatsu, and L.W. Swanson Distribution of androgen and estrogen receptor mRNA-containing cells in the rat brain: an in situ hybridization study J Comp Neurol 294 1990 76 95
67. 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
68. E.R. Smith, D.A. Damassa, and J.M. Davidson Hormone administration: peripheral and intracranial implants R.D. Meyer Methods of psychobiology 1978 Academy New York 259 279
69. M.S. Smith, M.E. Freeman, and J.D. Neill The control of progesterone secretion during the estrous cycle and early pseudopregnancy in the rat: prolactin, gonadotropin and steroid levels associated with rescue of the corpus luteum of pseudopregnancy Endocrinology 96 1975 219 226
70. L.K. Takahashi Role of CRF(1) and CRF(2) receptors in fear and anxiety Neurosci Biobehav Rev 25 2001 627 636
71. D.J. Toufexis, C. Davis, A. Hammond, and M. Davis Progesterone attenuates corticotropin-releasing factor-enhanced but not fear-potentiated startle via the activity of its neuroactive metabolite, allopregnanolone J Neurosci 24 2004 10280 10287
72. D.L. Walker, and M. Davis Double dissociation between the involvement of the bed nucleus of the stria terminalis and the central nucleus of the amygdala in startle increases produced by conditioned versus unconditioned fear J Neurosci 17 1997 9375 9383
73. C.R. Winston, B.J. Leavell, P.A. Ardayfio, C. Beard, and R.L. Commissaris A nonextinction procedure for long-term studies of classically conditioned enhancement of acoustic startle in the rat Physiol Behav 73 2001 9 17
74. D.L. Yuan, and K.C. Chambers Estradiol accelerates extinction of lithium chloride-induced conditioned taste aversions through its illness-associated properties Horm Behav 36 1999 287 298
75. W. Zhou, K.A. Cunningham, and M.L. Thomas Estrogen regulation of gene expression in the brain: a possible mechanism altering the response to psychostimulants in female rats Brain Res Mol Brain Res 100 2002 75 83
76. M.J. Zuluaga, D. Agrati, M. Pereira, N. Uriarte, A. Fernandez-Guasti, and A. Ferreira Experimental anxiety in the black and white model in cycling, pregnant and lactating rats Physiol Behav 84 2005 279 286