Social status modifies estradiol activation of sociosexual behavior in female rhesus monkeys

Hormones and Behavior

Volumn 62, Issue 5, 2012, Pages 612-620

  Reding, Katherine ^a   Michopoulos, Vasiliki ^a   Wallen, Kim ^a   Sanchez, Mar ^a,b   Wilson, Mark E ^a   Toufexis, Donna ^a,c  

^a EMORY UNIVERSITY   (United States)

^b EMORY UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c UNIVERSITY OF VERMONT   (United States)

Author keywords

Affiliation; Estradiol; Rhesus monkeys; Sexual behavior; Social subordination

Indexed keywords

ESTRADIOL;

AGGRESSION; ANIMAL EXPERIMENT; ANXIETY; ARTICLE; CONTROLLED STUDY; EMOTION; FEMALE; HORMONE DETERMINATION; MENTAL STRESS; MOTIVATION; NONHUMAN; OVARIECTOMY; PRIORITY JOURNAL; REPRODUCTION; RHESUS MONKEY; SEXUAL BEHAVIOR; SOCIAL BEHAVIOR; SOCIAL STATUS;

AGGRESSION; AGONISTIC BEHAVIOR; ANIMALS; DOSE-RESPONSE RELATIONSHIP, DRUG; ESTRADIOL; FEMALE; HIERARCHY, SOCIAL; MACACA MULATTA; MALE; OSMOLAR CONCENTRATION; OVARIECTOMY; SEX FACTORS; SEXUAL BEHAVIOR, ANIMAL; SOCIAL BEHAVIOR; STRESS, PSYCHOLOGICAL;

EID: 84868195525     PISSN: 0018506X     EISSN: 10956867     Source Type: Journal    
DOI: 10.1016/j.yhbeh.2012.09.010     Document Type: Article

References (74)

1. Adams M.R., Kaplan J.R., Koritnik D.R. Psychosocial influences on ovarian endocrine and ovulatory function in Macaca fascicularis. Physiol. Behav. 1985, 35:935-940.
2. Beach F.A. Sexual attractivity, proceptivity, and receptivity in female mammals. Horm. Behav. 1976, 7:105-138.
3. Berga S.L., Loucks T.L. Stress induced anovulation. Encyclopedia of Stress 2007, 615-631. Academic Press, New York. G. Fink, M. Bruce, E. Kloet, R. Robert, C. George, S. Andrew, R. Noel, C. Ian, F. Giora (Eds.).
4. Bernstein I.S. Primate status hierarchies. Primate Behavior: Developments in Field and Laboratory Research 1970, 71-109. Academic Press, New York. L.A. Rosenblum (Ed.).
5. Bernstein I.S., Gordon T.P. Function of aggression in primate societies. Am. Sci. 1974, 62:304-311.
6. Bernstein I.S., Gordon T.P., Rose R.M. Aggression and social controls in rhesus-monkey (Macaca mulatta) groups revealed in group formation studies. Folia Primatol. 1974, 21:81-107.
7. Bos P.A., Panksepp J., Bluthé R.-M., Honk J.v. Acute effects of steroid hormones and neuropeptides on human social-emotional behavior: a review of single administration studies. Front. Neuroendocrinol. 2012, 33:17-35.
8. Cagnacci A., Volpe A., Arangino S., Malmusi S., Draetta F.P., Matteo M.L., Maschio E., Vacca A.M.B., Melis G.B. Depression and anxiety in climacteric women: role of hormone replacement therapy. Menopause 1997, 4:206-211.
9. Carpenter C.R. Sexual behavior of free ranging rhesus monkeys (Macaca mulatta). I. Specimens, procedures and behavioral characteristics of estrus. J. Comp. Psychol. 1942, 33:113-142.
10. Chrousos G.P. Stress and disorders of the stress system. Nat. Rev. Endocrinol. 2009, 5:374-381.
11. Chrousos G.P., Gold P.W. The concepts of stress and stress system disorders. JAMA 1992, 267:1244-1252.
12. Chrousos G.P., Torpy D.J., Gold P.W. Interactions between the hypothalamic-pituitary-adrenal axis and the female reproductive system: clinical implications. Ann. Intern. Med. 1998, 129:229-240.
13. Cohen S., Line S., Manuck S.B., Rabin B.S., Heise E.R., Kaplan J.R. Chronic social stress, social status, and susceptibility to upper respiratory infections in nonhuman primates. Psychosom. Med. 1997, 59:213-221.
14. Coleman K., Robertson N.D., Bethea C.L. Long-term ovariectomy alters social and anxious behaviors in semi-free ranging Japanese macaques. Behav. Brain Res. 2011, 225:317-327.
15. Collura L.A., Hoffman J.B., Wilson M.E. Administration of human leptin differentially affects parameters of cortisol secretion in socially housed female rhesus monkeys. Endocrine 2009.
16. de Waal F.B.M., Luttrell L.M. The formal hierarchy of rhesus macaques: an investigation of the bared-teeth display. Am. J. Primatol. 1985, 9:73-85.
17. Dubey A.K., Plant T.M. A suppression of gonadotropin secretion by cortisol in castrated male rhesus monkeys (Macaca mulatta) mediated by the interruption of hypothalamic gonadotropin-releasing hormone release. Biol. Reprod. 1985, 33:423-431.
18. Graves F.C., Wallen K. Androgen-induced yawning in rhesus monkey females is reversed with a nonsteroidal anti-androgen. Horm. Behav. 2006, 49:233-236.
19. Halbreich U., Kahn L.S. Role of estrogen in the aetiology and treatment of mood disorders. CNS Drugs 2001, 15:797-817.
20. Isgor C., Cecchi M., Kabbaj M., Akil H., Watson S.J. Estrogen receptor β in the paraventricular nucleus of hypothalamus regulates the neuroendocrine response to stress and is regulated by corticosterone. Neuroscience 2003, 121:837-845.
21. Jarrell H., Hoffman J.B., Kaplan J.R., Berga S., Kinkead B., Wilson M.E. Polymorphisms in the serotonin reuptake transporter gene modify the consequences of social status on metabolic health in female rhesus monkeys. Physiol. Behav. 2008, 93:807-819.
22. Kaplan J.R., Adams M.R., Clarkson T.B., Koritnik D.R. Psychosocial influences on female protection among cynomolgus macaques. Atherosclerosis 1984, 53:283-295.
23. Kaplan J.R., Adams M.R., Clarkson T.B., Manuck S.B., Shively C.A., Williams J.K. Psychosocial factors, sex differences, and atherosclerosis: lessons from animal models. Psychosom. Med. 1996, 58:598-611.
24. Kaplan J.R., Chen H., Appt S.E., Lees C.J., Franke A.A., Berga S.L., Wilson M.E., Manuck S.B., Clarkson T.B. Impairment of ovarian function and associated health-related abnormalities are attributable to low social status in premenopausal monkeys and not mitigated by a high-isoflavone soy diet. Hum. Reprod. 2010, 25:3083-3094.
25. Keen-Rhinehart E., Michopoulos V., Toufexis D.J., Martin E.I., Nair H., Ressler K.J., Davis M., Owens M.J., Nemeroff C.B., Wilson M.E. Continuous expression of corticotropin-releasing factor in the central nucleus of the amygdala emulates the dysregulation of the stress and reproductive axes. Mol. Psychiatry 2009, 14:37-50.
26. Kikusui T., Winslow J.T., Mori Y. Social buffering: relief from stress and anxiety. Philos. Trans. R. Soc. Lond. B Biol. Sci. 2006, 361:2215-2228.
27. Kowalski W., Chatterton R.T. Effects of subchronic infusion of dehydroepiandrosterone sulfate on serum gonadotropin-levels and ovarian-function in the cynomolgus monkey. Fertil. Steril. 1992, 57:912-920.
28. Kowalski W., Chatterton R.T. Peripheral and not central suppression of ovarian-function during osmotic pump infusion of adrenocorticotropin-(1-24) for one menstrual-cycle in the cynomolgus monkey and its partial compensation by a transitory elevation of sex hormone-binding globulin levels. Endocrinology 1992, 130:3582-3592.
29. Lovejoy J., Wallen K. Adrenal suppression and sexual initiation in group-living female rhesus-monkeys. Horm. Behav. 1990, 24:256-269.
30. Lund T.D., Rovis T., Chung W.C.J., Handa R.J. Novel actions of estrogen receptor-beta on anxiety-related behaviors. Endocrinology 2005, 146:797-807.
31. Marcondes F.K., Miguel K.J., Melo L.L., Spadari-Bratfisch R.C.l Estrous cycle influences the response of female rats in the elevated plus-maze test. Physiol. Behav. 2001, 74:435-440.
32. Michael R.P., Zumpe D. A review of hormonal factors influencing the sexual and aggressive-behavior of macaques. Am. J. Primatol. 1993, 30:213-241.
33. Michopoulos V., Wilson M.E. Body weight decreases induced by estradiol in female rhesus monkeys are dependent upon social status. Physiol. Behav. 2011, 102:382-388.
34. Michopoulos V., Berga S.L., Kaplan J.R., Wilson M.E. Social subordination and polymorphisms in the gene encoding the serotonin transporter enhance estradiol inhibition of luteinizing hormone secretion in female rhesus monkeys. Biol. Reprod. 2009, 81:1154-1163.
35. Michopoulos V., Checchi M., Sharpe D., Wilson M.E. Estradiol effects on behavior and serum oxytocin are modified by social status and polymorphisms in the serotonin transporter gene in female rhesus monkeys. Horm. Behav. 2011, 59:528-535.
36. Michopoulos V., Reding K., Wilson M.E., Toufexis D. Social subordination impairs hypothalamic-pituitary-adrenal function in female rhesus monkeys. Horm. Behav. 2012, Epub August 24.
37. Michopoulos V., Higgins M., Toufexis D., Wilson M.E. Social subordination produces distinct stress-related phenotypes in female rhesus monkeys. Psychoneuroendocrinology 2012, 37:1071-1085.
38. Mook D., Felger J., Graves F., Wallen K., Wilson M.E. Tamoxifen fails to affect central serotonergic tone but increases indices of anxiety in female rhesus macaques. Psychoneuroendocrinology 2005, 30:273-283.
39. Morgan M.A., Pfaff D.W. Effects of estrogen on activity and fear-related behaviors in mice. Horm. Behav. 2001, 40:472-482.
40. Moses-Kolko E.L., Berga S.L., Kalro B., Sit D.K.Y., Wisner K.L. Transdermal estradiol for postpartum depression: a promising treatment option. Clin. Obstet. Gynecol. 2009, 52:516-529.
41. Naoki T., Ikuya S., Toshihiro A., Osamu T., Keishi M. Dexamethasone suppresses estrogen action at the pituitary level without modulating estrogen receptor dynamics. J. Steroid Biochem. 1985, 23:385-388.
42. Oakley A.E., Breen K.M., Clarke I.J., Karsch F.J., Wagenmaker E.R., Tilbrook A.J. Cortisol reduces gonadotropin-releasing hormone pulse frequency in follicular phase ewes: influence of ovarian steroids. Endocrinology 2009, 150:341-349.
43. Paiardini M., Hoffman J., Cervasi B., Ortiz A.M., Stroud F., Silvestri G., Wilson M.E. T-cell phenotypic and functional changes associated with social subordination and gene polymorphisms in the serotonin reuptake transporter in female rhesus monkeys. Brain Behav. Immun. 2009, 23:286-293.
44. Pazol K., Kaplan J.R., Abbott D., Appt S.E., Wilson M.E. Practical measurement of total and bioavailable estradiol in female macaques. Clin. Chim. Acta 2004, 340:117-126.
45. Pierce B.N., Hemsworth P.H., Rivalland E.T.A., Wagenmaker E.R., Morrissey A.D., Papargiris M.M., Clarke I.J., Karsch F.J., Turner A.I., Tilbrook A.J. Psychosocial stress suppresses attractivity, proceptivity and pulsatile LH secretion in the ewe. Horm. Behav. 2008, 54:424-434.
46. Pope N.S., Wilson M.E., Gordon T.P. The effect of season on the induction of sexual behavior by estradiol in female rhesus monkeys. Biol. Reprod. 1987, 36:1047-1054.
47. Rivier C., Rivest S. Effect of stress on the activity of the hypothalamic-pituitary-gonadal axis - peripheral and central mechanisms. Biol. Reprod. 1991, 45:523-532.
48. Ronnekleiv O.K., Bosch M.A., Zhang C. Regulation of endogenous conductances in GnRH neurons by estrogens. Brain Res. 2010, 1364:25-34.
49. Saketos M., Sharma N., Santoro N.F. Suppression of the hypothalamic-pituitary-ovarian axis in normal women by glucocorticoids. Biol. Reprod. 1993, 49:1270-1276.
50. Samuels M.H., Luther M., Henry P., Ridgway E.C. Effects of hydrocortisone on pulsatile pituitary glycoprotein-secretion. J. Clin. Endocrinol. Metab. 1994, 78:211-215.
51. Sapolsky R.M. Social subordinance as a marker of hypercortisolism. Ann. N. Y. Acad. Sci. 1995, 771:626-639.
52. 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.
53. Shively C.A. Social subordination stress, behavior, and central monoaminergic function in female cynomolgus monkeys. Biol. Psychiatry 1998, 44:882-891.
54. Shively C., Kaplan J. Effects of social-factors on adrenal weight and related physiology of Macaca fascicularis. Physiol. Behav. 1984, 33:777-782.
55. Shively C.A., Laber-Laird K., Anton R.F. Behavior and physiology of social stress and depression in female cynomolgus monkeys. Biol. Psychiatry 1997, 41:871-882.
56. Shively C.A., Williams J.K., Laber-Laird K., Anton R.F. Depression and coronary artery atherosclerosis and reactivity in female cynomolgus monkeys. Psychosom. Med. 2002, 64:699-706.
57. Tilbrook A., Turner A., Clarke I. Effects of stress on reproduction in non-rodent mammals: the role of glucocorticoids and sex differences. Rev. Reprod. 2000, 5:105-113.
58. Toufexis D.J., Myers K.M., Davis M. The effect of gonadal hormones and gender on anxiety and emotional learning. Horm. Behav. 2006, 50:539-549.
59. Uphouse L., Selvamani A., Lincoln C., Morales L., Comeaux D. Mild restraint reduces the time hormonally primed rats spend with sexually active males. Behav. Brain Res. 2005, 157:343-350.
60. Van Vugt D.A., Piercy J., Farley A.E., Reid R.L., Rivest S. Luteinizing hormone secretion and corticotropin-releasing factor gene expression in the paraventricular nucleus of rhesus monkeys following cortisol synthesis inhibition. Endocrinology 1997, 138:2249-2258.
61. Walf A.A., Frye C.A. Er[beta]-selective estrogen receptor modulators produce antianxiety behavior when administered systemically to ovariectomized rats. Neuropsychopharmacology 2005, 30:1598-1609.
62. Walker M.L., Wilson M.E., Gordon T.P. Female rhesus-monkey aggression during the menstrual-cycle. Anim. Behav. 1983, 31:1047-1054.
63. Walker M.L., Wilson M.E., Gordon T.P. Endocrine control of the seasonal occurrence of ovulation in rhesus monkeys housed outdoors. Endocrinology 1984, 114:1074-1081.
64. Wallen K. Influence of female hormonal state on rhesus sexual-behavior varies with space for social-interaction. Science 1982, 217:375-377.
65. Wallen K. Desire and ability: hormones and the regulation of female sexual behavior. Neurosci. Biobehav. Rev. 1990, 14:233-241.
66. Wallen K., Goy R.W. Effects of estradiol benzoate, estrone, and propionates of testosterone or dihydrotestosterone on sexual and related behaviors of ovariectomized rhesus-monkeys. Horm. Behav. 1977, 9:228-248.
67. Wallen K., Tannenbaum P.L. Hormonal modulation of sexual behavior and affiliation in rhesus monkeys. Ann. N. Y. Acad. Sci. 1997, 807:185-202.
68. Wallen K., Winston L.A. Social complexity and hormonal influences on sexual-behavior in rhesus-monkeys (Macaca mulatta). Physiol. Behav. 1984, 32:629-637.
69. Wallen K., Winston L.A., Gaventa S., Davisdasilva M., Collins D.C. Periovulatory changes in female sexual-behavior and patterns of ovarian-steroid secretion in group-living rhesus-monkeys. Horm. Behav. 1984, 18:431-450.
70. White S., Uphouse L. Estrogen and progesterone dose-dependently reduce disruptive effects of restraint on lordosis behavior. Horm. Behav. 2004, 45:201-208.
71. Wilson M.E., Gordon T.P., Collins D.C. Variation in ovarian steroids associated with the annual mating period in female rhesus monkeys (Macaca mulatta). Biol. Reprod. 1982, 27:530-539.
72. Wilson M.E., Fisher J., Fischer A., Lee V., Harris R.B., Bartness T.J. Quantifying food intake in socially housed monkeys: social status effects on caloric consumption. Physiol. Behav. 2008, 94:586-594.
73. Zehr J.L., Maestripieri D., Wallen K. Estradiol increases female sexual initiation independent of male responsiveness in rhesus monkeys. Horm. Behav. 1998, 33:95-103.
74. Zumpe D., Michael R.P. Redirected aggression and gonadal hormones in captive rhesus monkeys (Macaca mulatta). Anim. Behav. 1970, 18(Part 1):11-19.