Both estrogen receptors and androgen receptors contribute to testosterone-induced changes in the morphology of the medial amygdala and sexual arousal in male rats

Hormones and Behavior

Volumn 43, Issue 2, 2003, Pages 336-346

  Cooke, Bradley M ^a   Breedlove, S Marc ^b   Jordan, Cynthia L ^b  

^a OREGON HEALTH AND SCIENCE UNIVERSITY   (United States)

^b MICHIGAN STATE UNIVERSITY   (United States)

Author keywords

Androgen receptor; Estrogen receptor; Hemispheric laterality; Male copulation; Noncontact penile erection; Ultrasonic vocalization

Indexed keywords

ANDROGEN RECEPTOR; ANDROSTANOLONE; ESTRADIOL; ESTROGEN RECEPTOR; SILASTIC; STEROID; STEROID RECEPTOR;

AMYGDALOID NUCLEUS; ANIMAL BEHAVIOR; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BRAIN NERVE CELL; BRAIN REGION; CASTRATION; CELL SIZE; CELL VOLUME; CONTROLLED STUDY; DRUG CAPSULE; EJACULATION; HEMISPHERIC DOMINANCE; HORMONAL THERAPY; HORMONE ACTION; LEFT HEMISPHERE; MALE; MORPHOLOGY; NERVE CELL PLASTICITY; NONHUMAN; PENIS ERECTION; PRIORITY JOURNAL; RAT; REGULATORY MECHANISM; RIGHT HEMISPHERE; SEXUAL AROUSAL; SEXUAL BEHAVIOR; VOCALIZATION;

EID: 0037304835     PISSN: 0018506X     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0018-506X(02)00047-8     Document Type: Article

References (54)

1. al-Shamma H., De Vries G. Neurogenesis of the sexually dimorphic vasopressin cells of the bed nucleus of the stria terminalis and amygdala in rats. J. Neurobiol. 29:1995;91-98.
2. Arnold A.P., Breedlove S.M. Organizational and activational effects of sex steroids on brain and behavior a reanalysis . Horm. Behav. 19:1985;469-498.
3. Baum M.J., Tobet S.A., Starr M.S., Bradshaw W.G. Implantation of dihydrotestosterone proprionate into the lateral septum or medial amygdala facilitates copulation in castrated male rats given estradiol systemically. Horm. Behav. 16:1982;208-223.
4. Breedlove S.M. Sexual dimorphism in the vertebrate nervous system. J. Neurosci. 12:1992;4133-4142.
5. Breedlove S.M., Arnold A.P. Sexually dimorphic motor nucleus in the rat lumbar spinal cord response to adult hormone manipulation, absence in androgen-insensitive rats . Brain Res. 225:1981;297-307.
6. Butera P.C., Czaja J.A. Activation of sexual behavior in male rats by combined subcutaneous and intracranial treatments of 5 alpha-dihydrotestosterone. Horm. Behav. 23:1989;92-105.
7. Cooke B., Hegstrom C.D., Villeneuve L.S., Breedlove S.M. Sexual differentiation of the vertebrate brain principles and mechanisms . Front. Neuroendocrinol. 19:1998;323-362.
8. Cooke B.M., Tabibnia G., Breedlove S.M. A brain sexual dimorphism controlled by adult circulating androgens. Proc. Nat. Acad. Sci., USA. 96:1999;7538-7540.
9. Cooke B.M., Hegstrom C.D., Keen A., Breedlove S.M. Photoperiod and social cues influence the medial amygdala but not the bed nucleus of the stria terminalis in the Siberian hamster. Neurosci. Lett. 312:2001;9-12.
10. Davidson J.M. Characteristics of sex behaviour in male rats following castration. Anim. Behav. 14:1966;266-272.
11. De Vries G.J., Buijs R.M., Leeuwen F.W., Caffé A.R., Swaab D.F. The vasopressinergic innervation of the brain in normal and castrated rats. J. Comp. Neurol. 233:1985;236-254.
12. Ferreira A., Caceres A. Estrogen-enhanced neurite growth evidence for a selective induction of tau and stable microtubules . J. Neurosci. 11:1991;392-400.
13. Forger N.G., Fishman R.B., Breedlove S.M. Differential effects of testosterone metabolites upon the size of sexually dimorphic motoneurons in adulthood. Horm. Behav. 26:1992;204-213.
14. Geyer, L.A., Barfield, R.J., McIntosh, T.K. 1978. Influence of gonadal hormones and sexual behavior on ultrasonic vocalization in rats: II. Treatment of males. J. Comp. Physiol. Psychol. 92, 447-456.
15. Geyer, L.A., McIntosh, T.K., Barfield, R.J. 1978. Effects of ultrasonic vocalizations and male's urine on female rat readiness to mate. J. Comp. Physiol. Psychol. 92, 438-446.
16. Gladue B. Dihydrotestosterone stimulates mounting behavior but not lordosis in female rats. Physiol. Behav. 33:1984;49-53.
17. Gomez D.M., Newman S.W. Medial nucleus of the amygdala in the adult Syrian hamster a quantitative Golgi analysis of gonadal hormonal regulation of neuronal morphology . Anat. Rec. 231:1991;498-509.
18. Gréco B., Edwards D.A., Zumpe D., Michael R.P., Clancy A.N. Fos induced by mating or noncontact sociosexual interaction is colocalized with androgen receptors in neurons within the forebrain, midbrain, and lumbosacral spinal cord of male rats. Horm. Behav. 33:1998;125-138.
19. Gréco B., Edwards D.A., Michael R.P., Clancy A.N. Androgen receptors and estrogen receptors are colocalized in male rat hypothalamic and limbic neurons that express Fos immunoreactivity induced by mating. Neuroendocrinology. 67:1998;18-28.
20. Hart B.L., Wallach S.J.R., Melese-d'Hospital P.Y. Differences in responsiveness to testosterone of penile reflexes and copulatory behavior of male rats. Horm. Behav. 17:1983;274-283.
21. Jakab R.L., Horvath T.L., Leranth C., Harada N., Naftolin F. Aromatase immunoreactivity in the rat brain gonadectomy sensitive hypothalamic neurons and an unresponsive "limbic ring" of the lateral septum-bed nucleus-amygdala complex . J. Steroid Biochem. Mol. Biol. 44:1993;481-498.
22. Kendrick K.M., Drewett R.F. Testosterone-sensitive neurones respond to oestradiol but not to dihydrotestosterone. Nature. 286:1980;67-68.
23. Kondo Y., Sachs B.D., Sakuma Y. Importance of the medial amygdala in rat penile erection evoked by remote stimuli from estrous females. Behav. Brain. Res. 88:1997;153-160.
24. Leedy M.G., Beattie M.S., Bresnahan J.C. Testosterone-induced plasticity of synaptic inputs to adult mammalian motoneurons. Brain Res. 424:1987;386-390.
25. Lorenzo A., Diaz H., Carrer H., Caceres A. Amygdala neurons in vitro neurite growth and effects of estradiol . J. Neurosci. Res. 33:1992;418-435.
26. Lustig R.H., Sudol M., Pfaff D.W., Federoff H.J. Estrogenic regulation and sex dimorphism of growth-associated protein 43 kDa (GAP-43) messenger RNA in the rat. Mol. Brain Res. 11:1991;125-132.
27. Madeira M.D., Lieberman A.R. Sexual dimorphisms in the mammalian limbic system. Prog. Neurobiol. 45:1995;275-333.
28. Malsbury C.W., McKay K. Neurotrophic effects of testosterone on the medial nucleus of the amygdala in adult male rats. J. Neuroendocrinol. 6:1994;57-69.
29. Manzo J., Cruz M.R., Hernandez M.E., Pacheco P., Sachs B.D. Regulation of noncontact erection in rats by gonadal steroids. Horm. Behav. 35:1999;264-270.
30. Matsumoto A. Hormonally induced neuronal plasticity in the adult motoneurons. Brain Res. Bull. 44:1997;539-547.
31. Matsumoto A., Arai Y., Urano A., Hyodo S. Effect of androgen on the expression of gap junction and b actin mRNAs in adult rat motoneurons. Neurosci. Res. 14:1992;133-144.
32. McEwen B.S. Permanence of brain sex differences and structural plasticity of the adult brain. Proc. Nat. Acad. Sci. USA. 96:1999;7128-7130.
33. Micevych P.E., Abelson L., Fok H., Ulibarri C., Priest C.A. Gonadal steroid control of preprocholecystokinin mRNA expression in the limbic-hypothalamic circuit comparison of adult with neonatal steroid treatments . J. Neurosci. Res. 38:1994;386-398.
34. Micevych P., Akesson T., Elde R. Distribution of cholecystokinin-immunoreactive cell bodies in the male and female rat. II. Bed nucleus of the stria terminalis and amygdala. J. Comp. Neurol. 269:1988;381-391.
35. Monks D., Getsios S., MacCalman C., Watson N. N-Cadherin is regulated by gonadal steroids in the adult hippocampal formation. Proc. Natl. Acad. Sci. USA. 98:2001;1312-1316.
36. Newman S.W. The medial extended amygdala in male reproductive behavior. A node in the mammalian social behavior network. Ann NY Acad. Sci. 877:1999;242-257.
37. Rogers L.C., Boer I., Junier M.-P., Ojeda S.R. Estradiol increases neural specific class II-b-tubulin mRNA levels in the developing female hypothalamus by regulating mRNA stability. Mol. Cell. Neurosci. 4:1993;424-431.
38. Romeo R.D., Sisk C.L. Pubertal and seasonal plasticity in the amygdala. Brain Res. 889:2001;71-77.
39. Roselli C.E., Abdelgadir S.E., Resko J.A. Regulation of aromatase gene expression in the adult rat brain. Brain Res. Bull. 44:1997;351-357.
40. Sandhu S., Cook P., Diamond M.C. Rat cerebral cortical estrogen receptors male-female, right-left . Exp. Neurol. 92:1986;186-196.
41. Shugrue P.J., Dorsa D.M. Estrogen and androgen differentially modulate the growth-associated protein GAP-43 (Neuromodulin) messenger ribonucleic acid in postnatal rat brain. Endocrinology. 134:1994;1321-1328.
42. Shugrue P.J., Lane M.V., Merchenthaler I. Comparative distribution of estrogen receptor-a and b mRNA in the rat central nervous system. J. Comp. Neurol. 388:1997;507-525.
43. Simerly R.B., Chang C., Muramatsu M., Swanson L.W. 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.
44. Simerly R.B., Young B.J., Capozza M.A., Swanson L.W. Estrogen differentially regulates neuropeptide gene expression in a sexually dimorphic olfactory pathway. Proc. Nat. Acad. Sci. USA. 86:1989;4766-4770.
45. Simerly R.B., Zee M.C., Pendleton J.W., Lubahn D.B., Korach K.S. Estrogen receptor-dependent sexual differentiation of dopaminergic neurons in the preoptic region of the mouse. Proc. Nat. Acad. Sci. USA. 94:1997;14077-14082.
46. Södersten P. Mounting behavior and lordosis behavior in castrated male rats treated with testosterone proprionate, or with estradiol benzoate or dihydrotestosterone in combination with testosterone proprionate. Horm. Behav. 6:1975;109-126.
47. Swann J.M., Newman S.W. Testosterone regulates substance P within neurons of the medial nucleus of the amygdala, the bed nucleus of the stria terminalis and the medial preoptic area of the male golden hamster. Brain Res. 590:1992;18-28.
48. Toran-Allerand C.D. Sex steroids and the development of the newborn mouse hypothalamus and preoptic area in vitro: implications for sexual differentiation. Brain Res. 106:1976;407-412.
49. Vagell M.E., McGinnis M.Y. The role of gonadal steroid receptor activation in the restoration of sociosexual behavior in adult male rats. Horm. Behav. 33:1998;163-179.
50. von Ziegler N.I., Lichtensteiger W. Asymmetry of brain aromatase activity regional- and sex-specific developmental patterns . Neuroendocrinology. 55:1992;512-518.
51. Wade G.N. Gonadal hormones and behavioral regulation of body weight. Physiol. Behav. 8:1972;523-534.
52. Wang Z., De Vries G.J. Androgen and estrogen effects on vasopressin messenger RNA expression in the medial amygdaloid nucleus in male and female rats. J. Neuroendocrinol. 7:1995;827-831.
53. Whalen R.E., Luttge W.G. Testosterone, androstenedione, and dihydrotestosterone effects on mating behavior of male rats . Horm. Behav. 2:1971;117-125.
54. White N.R., Gonzales R.N., Barfield R.J. Do vocalizations of the male rat elicit calling from the female? Behav. Neural Biol. 59:1993;76-78.