17β Estradiol increases resilience and improves hippocampal synaptic function in helpless ovariectomized rats

Psychoneuroendocrinology

Volumn 42, Issue , 2014, Pages 77-88

  Bredemann, Teruko M ^a   McMahon, Lori L ^a  

^a UNIVERSITY OF ALABAMA AT BIRMINGHAM   (United States)

Author keywords

Dendritic spines; Estrogen; Hippocampus; Learned helplessness; LTP; Stress

Indexed keywords

ESTRADIOL;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BRAIN FUNCTION; CELL DENSITY; COGNITIVE DEFECT; CONTROLLED STUDY; COPING BEHAVIOR; DENDRITIC SPINE; DEPRESSION; FEMALE; FUNCTIONAL ANATOMY; HIPPOCAMPAL CA1 REGION; HIPPOCAMPAL CA3 REGION; HORMONE SUBSTITUTION; LEARNED HELPLESSNESS; LONG TERM POTENTIATION; MALE; MEMORY DISORDER; NONHUMAN; PRIORITY JOURNAL; RAT;

DENDRITIC SPINES; ESTROGEN; HIPPOCAMPUS; LEARNED HELPLESSNESS; LTP; STRESS;

ANIMALS; DENDRITIC SPINES; DEPRESSION; DISEASE MODELS, ANIMAL; ESTRADIOL; FEMALE; HELPLESSNESS, LEARNED; HIPPOCAMPUS; RATS; RATS, SPRAGUE-DAWLEY; RESILIENCE, PSYCHOLOGICAL; SYNAPSES;

EID: 84895857059     PISSN: 03064530     EISSN: 18733360     Source Type: Journal    
DOI: 10.1016/j.psyneuen.2014.01.004     Document Type: Article

References (74)

1. Baker K.B., Kim J.J. Effects of stress and hippocampal NMDA receptor antagonism on recognition memory in rats. Learn. Mem. 2002, 9:58-65.
2. Baller E.B., Wei S.M., Kohn P.D., Rubinow D.R., Alarcon G., Schmidt P.J., Berman K.F. Abnormalities of dorsolateral prefrontal function in women with premenstrual dysphoric disorder: a multimodal neuroimaging study. Am. J. Psychiatry 2013, 170:305-314.
3. Bath K.G., Chuang J., Spencer-Segal J.L., Amso D., Altemus M., McEwen B.S., Lee F.S. Variant brain-derived neurotrophic factor (Valine66Methionine) polymorphism contributes to developmental and estrous stage-specific expression of anxiety-like behavior in female mice. Biol. Psychiatry 2012, 72:499-504.
4. Campbell S., Marriott M., Nahmias C., MacQueen G.M. Lower hippocampal volume in patients suffering from depression: a meta-analysis. Am. J. Psychiatry 2004, 161:598-607.
5. Chen X., Guo T., Li B. Influence of prophylactic oophorectomy on mood and sexual function in women of menopausal transition or postmenopausal period. Arch. Gynecol. Obstet. 2013, 288:1101-1106.
6. Cohen L.S., Soares C.N., Joffe H. Diagnosis and management of mood disorders during the menopausal transition. Am. J. Med. 2005, 118(Suppl. 12B):93-97.
7. Craig M.C. Should psychiatrists be prescribing oestrogen therapy to their female patients?. Br. J. Psychiatry 2013, 202:9-13.
8. Dalla C., Edgecomb C., Whetstone A.S., Shors T.J. Females do not express learned helplessness like males do. Neuropsychopharmacology 2008, 33:1559-1569.
9. Dobrunz L.E., Stevens C.F. Heterogeneity of release probability, facilitation, and depletion at central synapses. Neuron 1997, 18:995-1008.
10. Duman R.S., Malberg J., Nakagawa S., D'Sa C. Neuronal plasticity and survival in mood disorders. Biol. Psychiatry 2000, 48:732-739.
11. Duman R.S., Monteggia L.M. A neurotrophic model for stress-related mood disorders. Biol. Psychiatry 2006, 59:1116-1127.
12. Estrada-Camarena E., Fernandez-Guasti A., Lopez-Rubalcava C. Antidepressant-like effect of different estrogenic compounds in the forced swimming test. Neuropsychopharmacology 2003, 28:830-838.
13. Foy M.R., Stanton M.E., Levine S., Thompson R.F. Behavioral stress impairs long-term potentiation in rodent hippocampus. Behav. Neural Biol. 1987, 48:138-149.
14. Frye C.A., Duffy C.K., Walf A.A. Estrogens and progestins enhance spatial learning of intact and ovariectomized rats in the object placement task. Neurobiol. Learn. Mem. 2007, 88:208-216.
15. Gass P., Henn F.A. Is there a role for neurogenesis in depression?. Biol. Psychiatry 2009, 66:3-4.
16. Gibbs R.B. Basal forebrain cholinergic neurons are necessary for estrogen to enhance acquisition of a delayed matching-to-position T-maze task. Horm. Behav. 2002, 42:245-257.
17. Gibbs R.B., Chipman A.M., Nelson D. Donepezil plus estradiol treatment enhances learning and delay-dependent memory performance by young ovariectomized rats with partial loss of septal cholinergic neurons. Horm. Behav. 2011, 59:503-511.
18. Gould E., Woolley C.S., Frankfurt M., McEwen B.S. Gonadal steroids regulate dendritic spine density in hippocampal pyramidal cells in adulthood. J. Neurosci. 1990, 10:1286-1291.
19. Hajszan T., Szigeti-Buck K., Sallam N.L., Bober J., Parducz A., Maclusky N.J., Leranth C., Duman R.S. Effects of estradiol on learned helplessness and associated remodeling of hippocampal spine synapses in female rats. Biol. Psychiatry 2010, 67:168-174.
20. Hall J.A., Cantley T.C., Galvin J.M., Day B.N., Anthony R.V. Influence of ovarian steroids on relaxin-induced uterine growth in ovariectomized gilts. Endocrinology 1992, 130:3159-3166.
21. Harburger L.L., Saadi A., Frick K.M. Dose-dependent effects of post-training estradiol plus progesterone treatment on object memory consolidation and hippocampal extracellular signal-regulated kinase activation in young ovariectomized mice. Neuroscience 2009, 160:6-12.
22. Harte-Hargrove L.C., Maclusky N.J., Scharfman H.E. Brain-derived neurotrophic factor-estrogen interactions in the hippocampal mossy fiber pathway: implications for normal brain function and disease. Neuroscience 2013, 239:46-66.
23. Holderbach R., Clark K., Moreau J.L., Bischofberger J., Normann C. Enhanced long-term synaptic depression in an animal model of depression. Biol. Psychiatry 2007, 62:92-100.
24. Jackson R.L., Minor T.R. Effects of signaling inescapable shock on subsequent escape learning: implications for theories of coping and "learned helplessness". J. Exp. Psychol. Anim. Behav. Process. 1988, 14:390-400.
25. Jenkins J.A., Williams P., Kramer G.L., Davis L.L., Petty F. The influence of gender and the estrous cycle on learned helplessness in the rat. Biol. Psychol. 2001, 58:147-158.
26. Joels M., Karst H., Alfarez D., Heine V.M., Qin Y., van Riel E., Verkuyl M., Lucassen P.J., Krugers H.J. Effects of chronic stress on structure and cell function in rat hippocampus and hypothalamus. Stress 2004, 7:221-231.
27. Kessler R.C. Epidemiology of women and depression. J. Affect. Disord. 2003, 74:5-13.
28. Kim J.J., Koo J.W., Lee H.J., Han J.S. Amygdalar inactivation blocks stress-induced impairments in hippocampal long-term potentiation and spatial memory. J. Neurosci. 2005, 25:1532-1539.
29. Kiss A., Delattre A.M., Pereira S.I., Carolino R.G., Szawka R.E., Anselmo-Franci J.A., Zanata S.M., Ferraz A.C. 17beta-estradiol replacement in young, adult and middle-aged female ovariectomized rats promotes improvement of spatial reference memory and an antidepressant effect and alters monoamines and BDNF levels in memory- and depression-related brain areas. Behav. Brain Res. 2012, 227:100-108.
30. Leuner B., Mendolia-Loffredo S., Shors T.J. High levels of estrogen enhance associative memory formation in ovariectomized females. Psychoneuroendocrinology 2004, 29:883-890.
31. Luine V., Frankfurt M. Interactions between estradiol, BDNF and dendritic spines in promoting memory. Neuroscience 2013, 239:34-45.
32. Malberg J.E., Duman R.S. Cell proliferation in adult hippocampus is decreased by inescapable stress: reversal by fluoxetine treatment. Neuropsychopharmacology 2003, 28:1562-1571.
33. McEwen B.S., Magarinos A.M. Stress effects on morphology and function of the hippocampus. Ann. N. Y. Acad. Sci. 1997, 821:271-284.
34. McLaughlin K.J., Bimonte-Nelson H., Neisewander J.L., Conrad C.D. Assessment of estradiol influence on spatial tasks and hippocampal CA1 spines: evidence that the duration of hormone deprivation after ovariectomy compromises 17beta-estradiol effectiveness in altering CA1 spines. Horm. Behav. 2008, 54:386-395.
35. Miller W.R., Seligman M.E. Depression and learned helplessness in man. J. Abnorm. Psychol. 1975, 84:228-238.
36. Mineur Y.S., Obayemi A., Wigestrand M.B., Fote G.M., Calarco C.A., Li A.M., Picciotto M.R. Cholinergic signaling in the hippocampus regulates social stress resilience and anxiety- and depression-like behavior. Proc. Natl. Acad. Sci. U. S. A. 2013, 110:3573-3578.
37. Nestler E.J., Gould E., Manji H., Buncan M., Duman R.S., Greshenfeld H.K., Hen R., Koester S., Lederhendler I., Meaney M., Robbins T., Winsky L., Zalcman S. Preclinical models: status of basic research in depression. Biol. Psychiatry 2002, 52:503-528.
38. Parker W.H. Bilateral oophorectomy versus ovarian conservation: effects on long-term women's health. J. Minim. Invasive Gynecol. 2010, 17:161-166.
39. Pavlides C., Watanabe Y., McEwen B.S. Effects of glucocorticoids on hippocampal long-term potentiation. Hippocampus 1993, 3:183-192.
40. Perez-Lopez F.R., Perez-Roncero G., Fernandez-Inarrea J., Fernandez-Alonso A.M., Chedraui P., Llaneza P., for The M.R.G. Resilience, depressed mood, and menopausal symptoms in postmenopausal women. Menopause 2013, 21. 10.1097/GME.0b013e31829479bb.
41. Pluchino N., Russo M., Santoro A.N., Litta P., Cela V., Genazzani A.R. Steroid hormones and BDNF. Neuroscience 2013, 239:271-279.
42. Rabin D.S., Schmidt P.J., Campbell G., Gold P.W., Jensvold M., Rubinow D.R., Chrousos G.P. Hypothalamic-pituitary-adrenal function in patients with the premenstrual syndrome. J. Clin. Endocrinol. Metab. 1990, 71:1158-1162.
43. Rachman I.M., Unnerstall J.R., Pfaff D.W., Cohen R.S. Estrogen alters behavior and forebrain c-fos expression in ovariectomized rats subjected to the forced swim test. Proc. Natl. Acad. Sci. U. S. A. 1998, 95:13941-13946.
44. Rocca W.A., Grossardt B.R., Geda Y.E., Gostout B.S., Bower J.H., Maraganore D.M., de Andrade M., Melton L.J. Long-term risk of depressive and anxiety symptoms after early bilateral oophorectomy. Menopause 2008, 15:1050-1059.
45. Romano-Torres M., Fernandez-Guasti A. Estradiol valerate elicits antidepressant-like effects in middle-aged female rats under chronic mild stress. Behav. Pharmacol. 2010, 21:104-111.
46. Rubinow D.R., Roy-Byrne P., Hoban M.C., Grover G.N., Stambler N., Post R.M. Premenstrual mood changes. Characteristic patterns in women with and without premenstrual syndrome. J. Affect. Disord. 1986, 10:85-90.
47. Rubinow D.R., Schmidt P.J. Mood disorders and the menstrual cycle. J. Reprod. Med. 1987, 32:389-394.
48. Ryan B.K., Vollmayr B., Klyubin I., Gass P., Rowan M.J. Persistent inhibition of hippocampal long-term potentiation in vivo by learned helplessness stress. Hippocampus 2010, 20:758-767.
49. Ryan S.M., Maier S.F. The estrous cycle and estrogen modulate stress-induced analgesia. Behav. Neurosci. 1988, 102:371-380.
50. Scharfman H.E., MacLusky N.J. Estrogen and brain-derived neurotrophic factor (BDNF) in hippocampus: complexity of steroid hormone-growth factor interactions in the adult CNS. Front. Neuroendocrinol. 2006, 27:415-435.
51. Schmidt P.J., Nieman L., Danaceau M.A., Tobin M.B., Roca C.A., Murphy J.H., Rubinow D.R. Estrogen replacement in perimenopause-related depression: a preliminary report. Am. J. Obstet. Gynecol. 2000, 183:414-420.
52. Schmidt P.J., Rubinow D.R. Sex hormones and mood in the perimenopause. Ann. N. Y. Acad. Sci. 2009, 1179:70-85.
53. Seligman M.E., Beagley G. Learned helplessness in the rat. J. Comp. Physiol. Psychol. 1975, 88:534-541.
54. Sell S.L., Craft R.M., Seitz P.K., Stutz S.J., Cunningham K.A., Thomas M.L. Estradiol-sertraline synergy in ovariectomized rats. Psychoneuroendocrinology 2008, 33:1051-1060.
55. Sherman J.J., LeResche L. Does experimental pain response vary across the menstrual cycle? A methodological review. Am. J. Physiol. Regul. Integr. Comp. Physiol. 2006, 291:R245-R256.
56. 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. 2001, 21:6292-6297.
57. Shors T.J., Leuner B. Estrogen-mediated effects on depression and memory formation in females. J. Affect. Disord. 2003, 74:85-96.
58. Shors T.J., Seib T.B., Levine S., Thompson R.F. Inescapable versus escapable shock modulates long-term potentiation in the rat hippocampus. Science 1989, 244:224-226.
59. Smith C.C., McMahon L.L. Estrogen-induced increase in the magnitude of long-term potentiation occurs only when the ratio of NMDA transmission to AMPA transmission is increased. J. Neurosci. 2005, 25:7780-7791.
60. Smith C.C., McMahon L.L. Estradiol-induced increase in the magnitude of long-term potentiation is prevented by blocking NR2B-containing receptors. J. Neurosci. 2006, 26:8517-8522.
61. Smith C.C., Vedder L.C., Nelson A.R., Bredemann T.M., McMahon L.L. Duration of estrogen deprivation, not chronological age, prevents estrogen's ability to enhance hippocampal synaptic physiology. Proc. Natl. Acad. Sci. U. S. A. 2010, 107:19543-19548.
62. Soares C.N., Almeida O.P., Joffe H., Cohen L.S. Efficacy of estradiol for the treatment of depressive disorders in perimenopausal women: a double-blind, randomized, placebo-controlled trial. Arch. Gen. Psychiatry 2001, 58:529-534.
63. Steenbergen H.L., Heinsbroek R.P., Van Haaren F., Van de Poll N.E. Sex-dependent effects of inescapable shock administration on behavior and subsequent escape performance in rats. Physiol. Behav. 1989, 45:781-787.
64. Vedder L.C., Smith C.C., Flannigan A.E., McMahon L.L. Estradiol-induced increase in novel object recognition requires hippocampal NR2B-containing NMDA receptors. Hippocampus 2013, 23:108-115.
65. Vollmayr B., Henn F.A. Learned helplessness in the rat: improvements in validity and reliability. Brain Res. Brain Res. Protoc. 2001, 8:1-7.
66. Vollmayr B., Mahlstedt M.M., Henn F.A. Neurogenesis and depression: what animal models tell us about the link. Eur. Arch. Psychiatry Clin. Neurosci. 2007, 257:300-303.
67. Vythilingam M., Heim C., Newport J., Miller A.H., Anderson E., Bronen R., Brummer M., Staib L., Vermetten E., Charney D.S., Nemeroff C.B., Bremner J.D. Childhood trauma associated with smaller hippocampal volume in women with major depression. Am. J. Psychiatry 2002, 159:2072-2080.
68. Vythilingam M., Vermetten E., Anderson G.M., Luckenbaugh D., Anderson E.R., Snow J., Staib L.H., Charney D.S., Bremner J.D. Hippocampal volume, memory, and cortisol status in major depressive disorder: effects of treatment. Biol. Psychiatry 2004, 56:101-112.
69. Walf A.A., Frye C.A. Antianxiety and antidepressive behavior produced by physiological estradiol regimen may be modulated by hypothalamic-pituitary-adrenal axis activity. Neuropsychopharmacology 2005, 30:1288-1301.
70. Walf A.A., Frye C.A. Administration of estrogen receptor beta-specific selective estrogen receptor modulators to the hippocampus decrease anxiety and depressive behavior of ovariectomized rats. Pharmacol. Biochem. Behav. 2007, 86:407-414.
71. Walf A.A., Rhodes M.E., Frye C.A. Antidepressant effects of ERbeta-selective estrogen receptor modulators in the forced swim test. Pharmacol. Biochem. Behav. 2004, 78:523-529.
72. Weber M.T., Maki P.M., McDermott M.P. Cognition and mood in perimenopause: a systematic review and meta-analysis. J. Steroid Biochem. Mol. Biol. 2013, 10.1016/j.jsbmb.2013.06.001.
73. Wharton W., Gleason C.E., Olson S.R., Carlsson C.M., Asthana S. Neurobiological underpinnings of the estrogen-mood relationship. Curr. Psychiatry Rev. 2012, 8:247-256.
74. Woolley C.S., McEwen B.S. Roles of estradiol and progesterone in regulation of hippocampal dendritic spine density during the estrous cycle in the rat. J. Comp. Neurol. 1993, 336:293-306.