Perinatal Testosterone Exposure and Maternal Care Effects on the Female Rat's Development and Sexual Behaviour

Journal of Neuroendocrinology

Volumn 25, Issue 6, 2013, Pages 528-536

  Borrow, A P ^a   Levy, M J ^a   Soehngen, E P ^a   Cameron, N M ^a  

^a BINGHAMTON UNIVERSITY   (United States)

Author keywords

Androgen; Parental care; Puberty; Reproduction

Indexed keywords

TESTOSTERONE;

ANIMAL EXPERIMENT; ANOGENITAL DISTANCE; ARTICLE; BODY WEIGHT; CONTROLLED STUDY; ESTRUS CYCLE; FEMALE; FETUS; GROOMING; HORMONE SUBSTITUTION; HORMONE SYNTHESIS; MATERNAL BEHAVIOR; MATERNAL CARE; MOUSE; NONHUMAN; OVARIECTOMY; PHENOTYPE; PLACENTA WEIGHT; PRIORITY JOURNAL; SEXUAL BEHAVIOR;

ANIMALS; FEMALE; MALE; MATERNAL EXPOSURE; PLACEBOS; PREGNANCY; PRENATAL EXPOSURE DELAYED EFFECTS; RATS; RATS, LONG-EVANS; SEXUAL BEHAVIOR, ANIMAL; SEXUAL MATURATION; TESTOSTERONE;

EID: 84878345578     PISSN: 09538194     EISSN: 13652826     Source Type: Journal    
DOI: 10.1111/jne.12035     Document Type: Article

References (56)

1. Kraemer GW. Psychobiology of early social attachment in rhesus monkey. Clinical implications. Ann NY Acad Sci 1997; 807: 401-418.
2. Suomi SJ. Early determinants of behaviour: evidence from primate studies. Br Med Bull 1997; 53: 170-184.
3. Chugani HT, Behen ME, Muzik O, Juhász C, Nagy F, Chugani DC. Local brain functional activity following early deprivation: a study of post-institutionalized Romanian orphans. NeuroImage 2001; 14: 1290-1301.
4. Ellis BH, Fisher PA, Zaharie S. Predictors of disruptive behavior, developmental delays, anxiety, and affective symptomatology among institutionally reared Romanian children. J Am Acad Child Adolesc Psychiatry 2004; 43: 1283-1292.
5. Lévy F, Melo AI, Galef BG, Madden M, Fleming AS. Complete maternal deprivation affects social, but not spatial, learning in adult rats. Dev Psychobiol 2003; 43: 177-191.
6. Zhang LX, Levine S, Dent G, Zhan Y, Xing G, Okimoto D, Gordon MK, Post RM, Smith MA. Maternal deprivation increases cell death in the infant rat brain. Brain Res Dev Brain Res 2002; 133: 1-11.
7. Cameron NM. Maternal programming of reproductive function and behavior in the female rat. Front Evol Neurosci 2011; 3: 10.
8. Numan M, Rosenblatt JS, Komisaruk BR. Medial preoptic area and onset of maternal behavior in the rat. J Comp Physiol Psychol 1977; 91: 146-164.
9. Champagne FA, Weaver ICG, Diorio J, Sharma S, Meaney MJ. Natural variations in maternal care are associated with estrogen receptor α expression and estrogen sensitivity in the medial preoptic area. Endocrinology 2003; 144: 4720-4724.
10. Champagne FA, Weaver IC, Diorio J, Dymov S, Szyf M, Meaney MJ. Maternal care associated with methylation of the estrogen receptor-alpha1b promoter and estrogen receptor-alpha expression in the medial preoptic area of female offspring. Endocrinology 2006; 147: 2909-2915.
11. Champagne FA, Francis DD, Mar A, Meaney MJ. Variations in maternal care in the rat as a mediating influence for the effects of environment on development. Physiol Behav 2003; 79: 359-371.
12. Cameron N, Del Corpo A, Diorio J, McAllister K, Sharma S, Meaney MJ. Maternal programming of sexual behavior and hypothalamic-pituitary-gonadal function in the female rat. PLoS ONE 2008; 3: e2210.
13. Cameron NM, Fish EW, Meaney MJ. Maternal influences on the sexual behavior and reproductive success of the female rat. Horm Behav 2008; 54: 178-184.
14. Sakhai SA, Kriegsfeld JJ, Francis DD. Maternal programming of sexual attractivity in female Long Evans rats. Psychoneuroendocrinology 2011; 36: 1217-1225.
15. Uriarte N, Breigeiron MK, Benetti F, Rosa XF, Lucion AB. Effects of maternal care on the development, emotionality, and reproductive functions in male and female rats. Dev Psychobiol 2007; 49: 451-462.
16. Cameron NM, Soehngen E, Meaney MJ. Variation in maternal care influences ventromedial hypothalamus activation in the rat. J Neuroendocrinol 2011; 23: 393-400.
17. Prior KM, Meaney MJ, Cameron NM. Variations in maternal care associated with differences in female rat reproductive behavior in a group-mating environment. Dev Psychobiol 2012; doi:10.1002/dev.21075. [Epub ahead of print].
18. Gerall AA, Ward IL. Effects of prenatal exogenous androgen on the sexual behavior of the female albino rat. J Comp Physiol Psychol 1966; 62: 370-375.
19. Cameron NM, Shahrokh D, Del Corpo A, Dhir SK, Szyf M, Champagne FA, Meaney MJ. Epigenetic programming of phenotypic variations in reproductive strategies in the rat through maternal care. J Neuroendocrinol 2008; 20: 795-801.
20. Welsh M, Saunders PTK, Fisken M, Scott HM, Hutchison GR, Smith LB, Sharpe RM. Identification in rats of a programming window for reproductive tract masculinization, disruption of which leads to hypospadias and cryptorchidism. J Clin Invest 2008; 118: 1479-1490.
21. Arnold AP, Gorski RA. Gonadal steroid induction of structural sex differences in the central nervous system. Annu Rev Neurosci 1984; 7: 413-442.
22. Zuloaga DG, Puts DA, Jordan CL, Breedlove SM. The role of androgen receptors in the masculinization of brain and behavior: what we've learned from the testicular feminization mutation. Horm Behav 2008; 52: 613-626.
23. Arnold AP. The organizational-activational hypothesis as the foundation for a unified theory of sexual differentiation of all mammalian tissues. Horm Behav 2009; 55: 570-578.
24. Phoenix CH, Goy RW, Gerall AA, Young WC. Organizing action of prenatally administered testosterone propionate on the tissues mediating mating behavior in the female guinea pig. Endocrinology 1959; 655: 369-382.
25. Schulz KM, Molenda-Figueira HA, Sisk CL. Back to the future: the organizational-activational hypothesis adapted to puberty and adolescence. Horm Behav 2009; 55: 597-604.
26. Gans S, Erskine MS. Effects of neonatal testosterone treatment on pacing behaviors and development of a conditioned place preference. Horm Behav 2003; 44: 354-364.
27. Hoepfner BA, Ward IL. Prenatal and neonatal androgen exposure interact to affect sexual differentiation in female rats. Behav Neurosci 1988; 102: 61-65.
28. Roselli CE, Chambers K. Sex differences in male-typical copulatory behaviors in response to androgen and estrogen treatment in rats. Neuroendocrinology 1999; 69: 290-298.
29. Hotchkiss AK, Lambright CS, Ostby JS, Parks-Saldutti L, Vandenbergh JG, Gray LE Jr. Prenatal testosterone exposure permanently masculinizes anogenital distance, nipple development, and reproductive tract morphology in female Sprague-Dawley rats. Toxicol Sci 2007; 96: 335-345.
30. McCoy SJ, Shirley BA. Effects of prenatal administration of testosterone and cortisone on the reproductive system of the female rat. Life Sci 1992; 50: 621-628.
31. McDonald PG, Doughty C. Comparison of the effect of neonatal administration of testosterone and dihydrotestosterone in the female rat. J Reprod Fert 1972; 30: 55-62.
32. Kudwa AE, Michopoulos V, Gatewood JD, Rissman EF. Roles of estrogen receptors alpha and beta in differentiation of mouse sexual behavior. Neuroscience 2006; 138: 921-928.
33. Mong JA, Glaser E, McCarthy MM. Gonadal steroids promote glial differentiation and alter neuronal morphology in the developing hypothalamus in a regionally specific manner. J Neurosci 1999; 19: 1464-1472.
34. Quadros PS, Pfau JL, Goldstein AYN, De Vries GJ, Wagner CK. Sex differences in progesterone receptor expression: a potential mechanism for estradiol-mediated sexual differentiation. Neuroendocrinology 2002; 143: 3727.
35. Roselli CE, Klosterman SA. Sexual differentiation of aromatase activity in the rat brain: effects of perinatal steroid exposure. Endocrinology 1998; 139: 3193-3201.
36. Champagne FA, Meaney MJ. Stress during gestation alters postpartum maternal care and the development of the offspring in a rodent model. Biol Psychiatry 2006; 59: 1227-1235.
37. Francis DD, Young LJ, Meaney MJ, Insel TR. Naturally occurring differences in maternal care are associated with the expression of oxytocin and vasopressin (V1a) receptors: gender differences. J Neuroendocrinol 2002; 14: 349-353.
38. Erskine MS. Effects of paced coital stimulation on estrus duration in intact cycling rats and ovariectomized and ovariectomized-adrenalectomized hormone-primed rats. Behav Neurosci 1985; 99: 151-161.
39. Erskine MS. Solicitation behavior in the estrous female rat: a review. Horm Behav 1989; 23: 473-502.
40. Hardy DF, DeBold JF. Effects of coital stimulation upon behavior of the female rat. J Comp Physiol Psychol 1972; 78: 400-408.
41. Edinger KL, Frye CA. Sexual experience of male rats influences anxiety-like behavior and androgen levels. Physiol Behav 2007; 92: 443-453.
42. Rhees RW, Kirk BA, Sephton S, Lephart ED. Effects of prenatal testosterone on sexual behavior, reproductive morphology and LH secretion in the female rat. Dev Neurosci 1997; 19: 430-437.
43. Amalfi S, Velez LM, Heber MF, Vighi S, Ferreira SR, Orozco AV, Pignataro O, Mota AB. Prenatal hyperandrogenization induces metabolic and endocrine alterations which depend on the levels of testosterone exposure. PLoS ONE 2012; 7: e37658.
44. Carlsen SM, Jacobsen G, Romundstad P. Maternal testosterone levels during pregnancy are associated with offspring size at birth. Eur J Endocrinol 2006; 155: 365-370.
45. Sathishkumar K, Elkins R, Chinnathambi V, Gao H, Hankins GD, Yallampalli C. Prenatal testosterone-induced fetal growth restriction is associated with down-regulation of rat placental amino acid transport. Reprod Biol Endocrinol 2011; 9: 110.
46. Manikkam M, Crespi EJ, Doop DD, Herkimer C, Lee JS, Yu S, Brown MB, Foster DL, Padmanabhan V. Fetal programming: prenatal testosterone excess leads to fetal growth retardation and postnatal catch-up growth in sheep. Endocrinology 2004; 145: 790-798.
47. Christiansen K. Behavioral effects of androgen in men and women. J Endocrinol 2001; 170: 39-48.
48. Traish AM, Kim SW, Stankovic M, Goldstein I, Kim NN. Testosterone increases blood flow and expression of androgen and estrogen receptors in the rat vagina. J Sex Med 2007; 4: 609-619.
49. Foecking EM, Szabo M, Schwartz NB, Levine JE. Neuroendocrine consequences of prenatal androgen exposure in the female rat: absence of luteinizing hormones surges, suppression of progesterone receptor gene expression, and acceleration of the gonadotropin-releasing hormone pulse generator. Biol Reprod 2005; 72: 1475-1483.
50. Bogic L, Gerlach JL, McEwen BS. The ontogeny of sex differences in estrogen-induced progesterone receptors in rat brain. Endocrinology 1988; 122: 2735-2741.
51. Fadem BH, Barfield RJ, Whalen RE. Dose-response and time-response relationships between progesterone and the display of patterns of receptive and proceptive behavior in the female rat. Horm Behav 1976; 13: 40-48.
52. Pleim ET, Barfield RJ. Progesterone versus estrogen facilitation of female sexual behavior by intracranial administration to female rats. Horm Behav 1988; 22: 150-159.
53. Siegel HI, Rosenblatt JS. Progesterone inhibition of estrogen-induced maternal behavior in hysterectomized-ovariectomized virgin rats. Horm Behav 1975; 6: 223-230.
54. 2)-treated, preogesterone receptor knockout (PRKO) mice. Endocrinology 1999; 140: 3653-3658.
55. Ward IL. Prenatal stress feminizes and demasculinizes the behavior of males. Science 1972; 175: 82-84.
56. Parent CI, Del Corpo A, Cameron NM, Meaney MJ. Maternal care associates with play dominance rank among adult female rats. Dev Psychobiol 2012; doi: 10.1002/dev.21070. [Epub ahead of print].