Variation in aromatase activity in the medial preoptic area and plasma progesterone is associated with the onset of paternal behavior

Neuroendocrinology

Volumn 78, Issue 1, 2003, Pages 36-44

  Trainor, Brian C ^a,d   Bird, Ian M ^b   Alday, Noel A ^c   Schlinger, Barney A ^c   Marler, Catherine A ^a  

^a UNIVERSITY OF WISCONSIN MADISON   (United States)

^b UNIVERSITY OF WISCONSIN SCHOOL OF MEDICINE AND PUBLIC HEALTH   (United States)

^c UNIVERSITY OF CALIFORNIA   (United States)

^d HARVARD UNIVERSITY   (United States)

Author keywords

Aromatase; Gonadal steroids; Mice; Paternal behavior; Preoptic area

Indexed keywords

AROMATASE; ESTRADIOL; PROGESTERONE;

ANIMAL BEHAVIOR; ANIMAL EXPERIMENT; ANIMAL TISSUE; AROMATIZATION; ARTICLE; BRAIN; CONTROLLED STUDY; CORRELATION ANALYSIS; ENZYME ACTIVITY; FATHER; MALE; MATING; MEDIAL PREOPTIC AREA; MOUSE; NONHUMAN; PATERNAL BEHAVIOR; PLASTICITY; PRIORITY JOURNAL; PROGESTERONE BLOOD LEVEL; SEXUAL BEHAVIOR; SOCIAL BEHAVIOR;

ANIMALS; AROMATASE; DIHYDROTESTOSTERONE; FEMALE; MALE; MICE; PATERNAL BEHAVIOR; PREOPTIC AREA; PROGESTERONE; SEXUAL BEHAVIOR, ANIMAL; TESTOSTERONE;

EID: 0042164910     PISSN: 00283835     EISSN: None     Source Type: Journal    
DOI: 10.1159/000071704     Document Type: Article

References (67)

1. Adkins-Regan E: Hormonal mechanisms of mate choice. Am Zool 1998;38:166-178.
2. Schlinger BA, Callard GV: Aromatization mediates aggressive behavior in quail. Gen Comp Endocrinol 1990;79:39-53.
3. Simon NG, Lu SF, McKenna SE, Chen X, Clifford AC: Sexual dimorphisms in regulatory systems for aggression; in Haug M, Whalen RE, Aron C, Olsen KL (eds): The Development of Sex Differences and Similarities in Behavior. Boston, Kluwer Academic Press, 1993, pp 389-408.
4. Balthazart J, Surlemont C: Androgen and estrogen action in the preoptic area and activation of copulatory behavior in quail. Physiol Behav 1990;48:599-609.
5. Baum MJ: Neuroendocrinology of sexual behavior in the male; in Becker JB, Breedlove SM, Crews D, McCarthy M (eds): Behavioral Endocrinology, ed 2. Cambridge, MIT Press, 2002, pp 153-204.
6. Fadem BH, Walters MJ, MacLusky N: Neural aromatase activity in a marsupial, the gray short tailed opossum (Monodelphis domestica): Ontogeny during postnatal development and androgen regulation in adulthood. Dev Brain Res 1993;74:199-205.
7. Roselli CE, Stormshak F, Resko JA: Distribution and regulation of aromatase activity in the ram hypothalamus and amygdala. Brain Res 1998;811:105-110.
8. Roselli CE, Resko JA: Testosterone regulates aromatase activity in discrete brain areas of male rhesus macaques. Biol Reprod 1989;40:929-934.
9. Hutchison RE, Hutchison JB, Steimer T, Steel E, Powers JB, Walker AP, Herbert J, Hastings MH: Brain aromatization of testosterone in the male Syrian hamster - Effects of androgen and photoperiod. Neuroendocrinology 1991;53:194-203.
10. Roselli CE, Klosterman SA, Fasasi TA: Sex differences in androgen responsiveness in the rat brain: Regional differences in the induction of aromatase activity. Neuroendocrinology 1996;64:139-145.
11. Balthazart J, Foidart A: Brain aromatase and the control of male sexual behavior. J Steroid Biochem Mol Biol 1993;44:521-540.
12. Baum MJ, Vreeburg JTM: Copulation in castrated male rats following combined treatment with estradiol and dihydrotestosterone. Science 1973;182:283-284.
13. Roselli CE, Horton LE, Resko JA: Distribution and regulation of aromatase activity in the rat hypothalamus and limbic system. Endocrinology 1985;117:2471-2477.
14. Clancy AN, Zumpe D, Michael RP: Intracerebral infusion of an aromatase inhibitor, sexual behavior and brain estrogen receptor-like immunoreactivity in intact male rats. Neuroendocrinology 1995;61:98-111.
15. Newman SW: The medial extended amygdala in male reproductive behavior. Ann NY Acad Sci 1999;877:242-257.
16. Sachs BD, Meisel RL: The physiology of male sexual behavior; in Knobil E, Neil J (eds): The Physiology of Reproduction. New York, Raven Press, 1994, pp 3-105.
17. Compaan JC, Hutchinson JB, Wozniak A, Ruiter AJH, Koolhaas JM: Brain aromatase activity and plasma testosterone levels are elevated in aggressive male mice during early ontogeny. Dev Brain Res 1994;82:185-192.
18. Resko JA, Perkins A, Roselli CE, Fitzgerald JA, Choate JVA, Stormshak F: Endocrine correlates of partner preference behavior in rams. Biol Reprod 1996;55:120-126.
19. Breedlove SM: Sex on the brain. Nature 1998;389:801.
20. Francis RC, Soma K, Fernald RD: Social regulation of the brain-pituitary-gonadal axis. Proc Natl Acad Sci USA 1993;90:7794-7798.
21. Erksine MS, Tobet SA, Baum MJ: Effects of birth on plasma testosterone, brain aromatase activity, and hypothalamic estradiol in male and female ferrets. Endocrinology 1998;122:524-530.
22. Riters LV, Baillien M, Eens M, Pinxten R, Foidart A, Ball GF, Balthazart J: Seasonal variation in androgen-metabolizing enzymes in the diencephalon and telencephalon of the male European starling (Sturnus vulgaris). J Neuroendocrinol 2001;13:985-997.
23. Soma KK, Bindra RK, Gee J, Wingfield JC, Schlinger BA: Androgen-metabolizing enzymes show region-specific changes across the breeding season in the brain of a wild songbird. J Neurobiol 1999;41:176-188.
24. Trainor BC, Marler CA: Testosterone promotes paternal behaviour via conversion to oestrogen in a monogamous mammal. Proc R Soc Lond B 2002;269:823-829.
25. Gubernick DJ, Nelson RJ: Prolactin and paternal behavior in the biparental California mouse, Peromyscus californicus. Horm Behav 1989;23:203-210.
26. Gubernick DJ, Schneider KA, Jeannotte LA: Individual differences in the mechanisms underlying the onset and maintenance of paternal behavior and the inhibition of infanticide in the monogamous biparental California mouse, Peromyscus californicus. Behav Ecol Sociobiol 1994;34:225-231.
27. Brown RE, Murdoch T, Murphy PR, Moger WH: Hormonal responses of male gerbils to stimuli from their mate and pups. Horm Behav 1995;29:474-491.
28. Reburn CJ, Wynne-Edwards KE: Hormonal changes in males of a naturally biparental and a uniparental mammal. Horm Behav 1999;35:163-176.
29. Ziegler TE, Snowdon CT: Preparental hormone levels and parenting experience in male cotton-top tamarins, Saguinus oedipus. Horm Behav 2001;38:59-167.
30. Nunes S, Fite JE, Patera KJ, French JA: Interactions among paternal behavior, steroid hormones, and parental experience in male marmosets (Callithrix kuhlii). Horm Behav 2001;39:70-82.
31. Clark MM, Galef BG Jr: A testosterone-mediated trade-off between parental and sexual effort in male Mongolian gerbils (Meriones unguiculatus). J Comp Psychol 1999;113:388-395.
32. Lonstein JS, De Vries GJ: Sex differences in the parental behaviour of adult virgin prairie voles: Independence from gonadal hormones and vasopressin. J Neuroendocrinol 1999;11:441-449.
33. Wang Z, De Vries GJ: Testosterone effects on paternal behavior and vasopressin immunoreactive projections in prairie voles (Microtus ochrogaster). Brain Res 1993;631:156-160.
34. Lonstein JS, Rood BD, De Vries GJ: Parental responsiveness is feminized after neonatal castration in virgin male prairie voles but is not masculinized by perinatal testosterone in virgin females. Horm Behav 2002;41:80-87.
35. Trainor BC, Marler CA: Paternal behavior, aggression, and testosterone in the California mouse, Peromyscus californicus. Horm Behav 2001;40:32-42.
36. Marler CA, Bester-Meredith JK, Trainor BC: Paternal behavior and aggression: Endocrine mechanisms and nongenomic transmission of behavior. Adv Study Behav 2003;32:263-323.
37. Bridges RS: Biochemical basis of parental behavior in the rat. Adv Stud Behav 1996;25:215-242.
38. Rosenblatt JS, Ceus K: Estrogen implants in the medial preoptic area stimulate maternal behavior in male rats. Horm Behav 1998;33:23-30.
39. Lee AW, Brown RE: Medial preoptic lesions disrupt parental behavior in both male and female California mice. Behav Neurosci 2002;116:968-975.
40. Fleming AS, Vaccarino F, Luebke C: Amygdaloid inhibition of maternal behavior in the nulliparous female rat. Physiol Behav 1980;25:731-743.
41. Sheehan T, Paul M, Amaral E, Numan MJ, Numan M: Evidence that the medial amygdala projects to the anterior/ventromedial hypothalamic nuclei to inhibit maternal behavior in rats. Neuroscience 2001;106:341-356.
42. Berridge CW, Mitton E, Clark W, Roth RH: Engagement in a non-escape (displacement) behavior elicits a selective and lateralized suppression of frontal cortical dopaminergic utilization in stress. Synapse 1999;32:187-197.
43. Lephart ED, Simpson ER: Assay of aromatase activity. Methods Enzymol 1991;206:4413-4420.
44. Schlinger BA, Callard GV: A comparison of aromatase, 5α- and 5β-reductase in brain and pituitary of male and female Japanese quail (Coturnix coturnix japonica). J Exp Zool 1987;242:171-180.
45. Bird IM, Pasquarette MM, Rainey WE, Mason JI: Hydroxysteroid dehydrogenase expression in human adrenocortical H295R cells. J Clin Endocrinol Metab 1996;81:2171-2178.
46. Marsh DA, Brodie HJ, Garrett WM, Tsai-Morris CH, Brodie AMH: Aromatase inhibitors - Synthesis and biological activity of androstenedione derivatives. J Med Chem 1985;28:788-795.
47. Davis ES, Marler CA: The progesterone challenge: steroid changes following an aggressive encounter in female Peromyscus californicus. Horm Behav, in press.
48. Zar JH: Biostatistical Analysis. Prentice-Hall, Englewood Cliffs, 1996.
49. Odum J, Ashby J: Detection of aromatase inhibitors in vitro using rat ovary microsomes. Toxicol Lett 2002;129:119-122.
50. Chabab A, Nicolas JC, Sultan C: Aromatase activity in human skin fibroblasts: Characterization by an enzymatic method. J Steroid Biochem 1986;25:157-163.
51. Dao TL: Estrogen synthesis in human breast tumor and its inhibition by testololactone and bromoandrostenedione. Cancer Res 1982;42(8 suppl):3338S-3341S.
52. Bird IM, Conley AJ: Steroid biosynthesis: Enzymology, integration and control; in Mason JI (ed): Genetics of Steroid Biosynthesis and Function. New York, Routledge, 2002, pp 1-35.
53. Kirkpatrick B, Kim JW, Insel TR: Limbic system fos expression associated with paternal behavior. Brain Res 1994;658:112-118.
54. Ehret G, Jürgens A, Koch M: Oestrogen receptor occurrence in the male mouse brain: modulation by paternal experience. Neuroreport 1993;4:1247-1250.
55. Ogawa S, Eng V, Taylor J, Lubahin DB, Korach KS, Pfaff DW: Roles of estrogen receptor-α gene expression in reproduction-related behaviors in female mice. Endocrinology 1998;139:5070-5081.
56. Krege JH, Hodgin JB, Couse JF, Enmark E, Warner W, Mahler JF, Sar M, Korach KS, Gustafsson J, Smithies O: Generation and reproductive phenotypes of mice lacking estrogen receptor β. Proc Natl Acad Sci USA 1998;95:15677-15682.
57. Winslow JT, Hastings N, Carter CS, Harbaugh CR, Insel TR: A role for central vasopressin in pair bonding in monogamous prairie voles. Nature 1993;365:545-548.
58. Delville Y, De Vries GJ, Ferris CF: Neural connections of the anterior hypothalamus and agonistic behavior in golden hamsters. Brain Behav Evol 2000;55:53-76.
59. Kollack-Walker S, Newman SW: Mating and agonistic behavior produce different patterns of fos immunolabeling in the male Syrian hamster brain. Neuroscience 1995;66:721-736.
60. Piva F, Gagliano P, Motta M, Martini L: Adrenal progesterone: Factors controlling its secretion. Endocrinology 1973;93:1178-1184.
61. Van Lier E, Regueiro M, Pérez-Clariget R, Andersson H, Kindahl H, Forsberg M: Effects of adrenocorticotrophin (ACTH) and progesterone on luteinising hormone (LH) secretion in recently castrated rams. Anim Reprod Sci 1999;55:115-126.
62. Baulieu EE, Robel P, Schumacher M: Neurosteroids: A New Regulatory Function in the Nervous System. Totowa, Humana Press, 1999.
63. Schneider JS, Stone MK, Wynne-Edwards KE, Horton TH, Lydon J O'Malley B, Levine JE: Progesterone receptors mediate male aggression toward infants. Proc Natl Acad Sci USA 2003;100:2951-2956.
64. Erpino MJ: Temporary inhibition by progesterone of sexual behavior in intact male mice. Horm Behav 1973;4:335-339.
65. Zumpe D, Bonsall RW, Michael RP: Effects of the nonsteroidal aromatase inhibitor, fadrozole, on the sexual behaviour of male cynomolgus monkeys (Macaca fascicularis). Horm Behav 1993;27:200-215.
66. Witt DM, Young LJ, Crews D: Progesterone modulation of androgen-dependent sexual behavior in male rats. Physiol Behav 1995;57:307-313.
67. Lephart ED, Butler PC, Mills RH, Jacobson NA, Ladle DR, Bloch GJ: Effects of testosterone and progesterone on brain 5α-reductase and aromatase in Long-Evans males and comparison of aromatase in Long-Evans vs. Sprague-Dawley rats. Brain Res 1998;789:327-330.