Androgen and estrogen (α) receptor distribution in the periaqueductal gray of the male rat

Hormones and Behavior

Volumn 36, Issue 2, 1999, Pages 98-108

  Murphy, Anne Z ^a   Shupnik, Margaret A ^b   Hoffman, Gloria E ^a  

^a UNIVERSITY OF MARYLAND SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF VIRGINIA   (United States)

Author keywords

Antinociception; Copulation; Gonadal steroids; Hormones; Lordosis; Pain; Reproduction; Sex behavior

Indexed keywords

ANDROGEN RECEPTOR; ESTROGEN RECEPTOR; RECEPTOR SUBTYPE;

ANTINOCICEPTION; ARTICLE; AUTONOMIC INNERVATION; COPULATION; HUMAN TISSUE; IMMUNOCYTOCHEMISTRY; IMMUNOREACTIVITY; MALE; NONHUMAN; PERIAQUEDUCTAL GRAY MATTER; PRIORITY JOURNAL; PROTEIN LOCALIZATION; RAT; RECEPTOR DENSITY; SEXUAL BEHAVIOR; TISSUE DISTRIBUTION;

EID: 0032837239     PISSN: 0018506X     EISSN: None     Source Type: Journal    
DOI: 10.1006/hbeh.1999.1528     Document Type: Article

References (83)

1. Albert, D. J., Jonik, R. H., and Walsh, M. L. (1991). Hormone-dependent aggression in the female rat: Testosterone plus estradiol implants prevent the decline in aggression following ovariectomy. Physiol. Behav. 49, 673-677.
2. Albert, D. J., Walsh, M. L., Gorzalka, B. B., Siemens, Y., and Louie, H. (1986). Testosterone removal in rats results in a decrease in social aggression and a loss of social dominance. Physiol Behav. 36, 401-407.
3. Bandler, R. (1982). Identification of neuronal cell bodies mediating components of biting attack behaviour in the cat: Induction of jaw opening following microinjection of glutamate into hypothalamus. Brain Res. 245, 192-197.
4. Bandler, R., and Shipley, M. T. (1994). Columnar organization in the midbrain periaqueductal gray: Modules for emotional expression? Trends Neurosci. 19, 379-389.
5. Basbaum, A. I., and Fields, H. L. (1984). Endogenous pain control systems: Brainstem spinal pathways and endorphin circuitry. Annu. Rev. Neurosci. 7, 309-338.
6. Beach, F. (1948). Hormones and Behavior. Hoeber, New York.
7. Behbehani, M. M. (1995). Functional characteristics of the midbrain periaqueductal gray. Prog. Neurobiol. 46, 575-605.
8. Bernard, J. F., and Bandler, R. (1998). Parallel circuits for emotional coping behaviour: New pieces in the puzzle. J. Comp. Neurol. 401, 429-436.
9. Budai, D., and Fields, H. L. (1998). Endogenous opioid peptides acting at mu opioid receptors in the dorsal horn contribute to midbrain modulation of spinal nociceptive neurons. J. Neurophysiol 79, 677-687.
10. Cameron, A., Khan, I., Westlund, K., and Willis, W. (1995). The efferent projections of the periaqueductal gray in the rat: A PHA-L study. H. Descending projections. J. Comp. Neurol. 351, 585-601.
11. Canteras, N. S., Simerly, R. B., and Swanson, L. W. (1994). Organization of projections from the ventromedial nucleus of the hypothalamus: A phaseolus vulgaris-leucoagglutinin study in the rat. J. Comp. Neurol. 348, 41-79.
12. Carrive, P., Bandler, R., and Dampney, R. A. L. (1988). Anatomical evidence that hypertension associated with the defence reaction in the cat is mediated by a direct projection from a restricted portion of the midbrain periaqueductal grey to the subretrofacial nucleus of the medulla. Brain Res. 460, 339-345.
13. Daniels, D., Miselis, R. R., and Flanagan-Cato, L. M. (1999). Central neuronal circuit innervating the lordosis-producing muscles defined by transneuronal transport of pseudorabies virus. J. Neurosci. 19(7), 2823-2833.
14. Davidson, J. M. (1966). Characteristics of sex behaviour in male rats following castration. Anim. Behav. 14, 266-272.
15. Dawson-Basoa, M. E., and Gintzler, A. R. (1996). Estrogen and progesterone activate spinal kappa-opiate receptor analgesic mechanisms. Pain 64, 607-615.
16. Depaulis, A., Bandler, R., and Vergnes, M. (1989). Characterization of pretentorial periaqueductal gray matter neurons mediating intraspecific defensive behaviors in the rat by microinjections of kainic acid. Brain Res. 486, 121-132.
17. Depaulis, A., Pechnick, R. N., and Liebeskind, J. C. (1988). Relationship between analgesia and cardiovascular changes induced by electrical stimulation of the mesencephalic periaqueductal gray matter in the rat. Brain Res. 451, 326-332.
18. Edwards, D. A., and Pfeifle, J. K. (1981). Hypothalamic and midbrain control of sexual receptivity in the female rat. Physiol. Behav. 26, 1061-1067.
19. Forman, L. F., Tingle, V., Estilow, S., and Cater, J. (1989). The response of analgesia testing is affected by gonadal steroids in the rat. Life Sci. 45, 447-454.
20. Frankfurt, M., Siegel, R. A., Sim, I., and Wuttke, W. (1986). Estrous cycle variations in cholecystokinin and substance P concentration in discrete areas of the rat brain. Neuroendocrinology 42, 226-231.
21. Friend, K., Resnick, E., Ang, L., and Shupnik, M. (1997). Specific modulation of estrogen receptor mRNA isoforms in rat pituitary throughout the estrous cycle and in response to steroid hormones. Mol. Cell. Endocrinol. 131, 147-155.
22. Gordon, F. T., and Soliman, M. R. I. (1996). The effects of estradiol and progesterone on pain sensitivity and brain opioid receptors in ovariectomized rats. Horm. Behav. 30, 244-250.
23. Gréco, B., Edwards, D., Michael, R., and Clancy, A. (1998). Androgen receptors and estrogen receptors are colocalized in male rat hypothalamic and limbic neurons that express Fos immunoreactivity induced by mating. Neuroendocrinology 67, 18-28.
24. Hennessey, A. C., Camak, L., Gordon, F., and Edwards, D. A. (1990). Connections between the pontine central gray and the ventromedial hypothalamus are essential for lordosis in female rats. Behav. Neurosci. 104, 477-488.
25. Herbison, A. (1997). Estrogen regulation of GABA transmission in rat preoptic area. Brain Res. Bull. 44, 321-326.
26. Herbison, A. E., Augood, S. J., Simonian, S. X., and Chapman, C. (1995). Regulation of GABA transporter activity and mRNA expression by estrogen in rat preoptic area. J. Neurosci. 15, 8302-8309.
27. 3H estradiol in catecholamine neurons of rat brain stem: Combined localization by autoradiography and formaldehyde-induced fluorescence. J. Comp. Neurol. 176, 607-630.
28. Holtzman, D., Brooks, P., Pfaff, D., and Schwartz-Giblin, S. (1997). Preproenkephalin mRNA is regulated by an interaction between steroid hormones and nociceptive stimulation. J. Neuroendocrinol. 9, 913-922.
29. Hull, E., Du, J., Lorrain, D., and Matuszewich, L. (1997). Testosterone, preoptic dopamine and copulation in male rats. Brain Res. Bull. 44, 327-334.
30. Jonge, F. H. D., and Poll, N. E. V. D. (1984). Relationships between sexual and aggressive behavior in male and female rats: Effects of gonadal hormones. Prog. Brain Res. 61, 283-302.
31. Kalyuzhny, A. E., and Wessendorf, M. W. (1998). Relationship of mu and delta opioid receptors to GABAergic neurons in the central nervous system, including antinociceptive brainstem circuits. J. Comp. Neurol. 392, 528-547.
32. Krieger, M. S., Conrad, L. C. A., and Pfaff, D. W. (1979). An autoradiographic study of the efferent connections of the ventromedial nucleus of the hypothalamus. J. Comp. Neurol. 183, 785-816.
33. Lauber, A. H., Romano, G. J., Mobbs, C. V., Howells, R. D., and Pfaff, D. W. (1990). Estradiol induction of proenkephalin messenger RNA in hypothalamus: Dose-response and relation to reproductive behavior in the female rat. Brain Res. Mol. Brain Res. 8, 47-54.
34. Lonstein, J. S., and Stern, J. M. (1998). Site and behavioral specificity of periaqueductal gray lesions on postpartum sexual, maternal, and aggressive behaviors in rats. Brain Res. 804(1), 21-35.
35. Marson, L., and McKenna, K. E. (1990). The identification of a brainstem site controlling spinal reflexes in male rats. Brain Res. 515, 303-308.
36. Marson, L., and McKenna, K. E. (1996). CNS cell groups involved in the control of the ischiocavernosus and bulbospongiosus muscles: A transneuronal tracing study using pseudorabies virus. J. Comp. Neurol. 374, 161-179.
37. Mathews, D., and Edwards, D. A. (1977). Involvement of the ventromedial and anterior hypothalamic nuclei in the hormonal induction of receptivity in the female rat. Physiol. Behav. 19, 319-326.
38. 3H-muscimol binding in hippocampus, hypothalamus and midbrain in rats. J. Neuroendocrinol. 4, 393-399.
39. McCarthy, M., Kaufman, L., Brooks, P., Pfaff, D., and Swartz-Giblin, S. (1995). Estrogen modulation of mRNA levels for the two forms of glutamic acid decarboxylase (GAD) in female rat brain. J. Comp. Neurol. 360, 685-697.
40. A receptor activation enhances, and blockade reduces, sexual behavior in the female rat. Exp. Brain Res. 86, 108-116.
41. McQueen, J. K., Wilson, H., Sumner, B. E. H., and Fink, G. (1999). Serotonin transporter (SERT) mRNA and binding site densities in male rat brain affected by sex steroids. Brain Res. Mol. Brain Res. 63, 241-247.
42. Miller, F. R., Ozimek, G., Milner, R. J., and Bloom, F. E. (1989). Regulation of neuronal oxytocin mRNA by ovarian steroids in the mature and developing hypothalamus. Proc. Natl. Acad. Sci. USA 86, 2468-2472.
43. Moffatt, C. A., Rissman, E. F., Shupnik, M. A., and Blaustein, J. D. (1998). Induction of progestin receptors by estradiol in the forebrain of estrogen receptor-alpha gene-disrupted mice. J. Neurosci. 18, 9556-9563.
44. Murphy, A. Z., Davis, A. M., Amateau, S., Hoffman, G. E., and McCarthy, M. M. (1999). Modulation of GABA transporters by gonadal steroids in the hypothalamus and midbrain of adult male and female rats. Soc. Neurosci. Abstr. 25.
45. Murphy, A., and Hoffman, G. (1998). Distribution of gonadal steroid receptor containing neurons in the preoptic-periaqueductal gray-brainstem pathway: A unique circuit for male sex behavior. Soc. Neurosci. 23, 81.2.
46. Murphy, A. Z., Ennis, M., Rizvi, T. A., Behbehani, M. M., and Shipley, M. T. (1995). Fos expression induced by changes in arterial pressure is localized in distinct, longitudinally organized columns of neurons in the rat midbrain periaqueductal gray. J. Comp. Neurol. 360, 286-300.
47. Murphy, A. Z., Ennis, M., Shipley, M. T., and Behbehani, M. M. (1994). Directionally specific changes in arterial pressure induce differential patterns of Fos expression in discrete areas of the rat brainstem: A double-labeling study for Fos and catecholamines. J. Comp. Neurol. 349, 36-50.
48. Murphy, A. Z., Shipley, M. T., Vanderhorst, V. G., and Holstege, G. (1996). Descending projections from the caudal ventrolateral medulla of the male rat selectively innervate discrete motoneuronal pools within the lumbosacral cord: Possible role in reproductive behavior. Soc. Neurosci. Abstr. 22.
49. Ogawa, S., Kow, L.-M., McCarthy, M. M., Pfaff, D. W., and Schwartz-Giblin, S. (1991). Midbrain PAG control of female reproductive behavior: In vitro electrophysiological characterization of actions of lordosis-relevant substances. In A. Depaulis and R. Bandler (Eds.), The Midbrain Periaqueductal Gray Matter: Functional, Anatomical and Neurochemical Organization, pp. 211-238. Plenum, New York/London.
50. Osborne, P. B., Vaughan, C. W., Wilson, H. I., and Christie, M. J. (1996). Opioid inhibition of rat periaqueductal grey neurones with identified projections to the rostral ventromedial medulla in vitro. J. Physiol. 490, 383-389.
51. Paxinos, G., and Watson, C. (1997). The Rat Brain in Stereotaxic Coordinates, 3rd ed. Academic Press, New York.
52. Pednekar, J. R., and Mulgaonker, V. K. (1995). Role of testosterone on pain threshold in rats. Indian J. Physiol. Pharmacol. 39, 423-424.
53. Pfaff, D., and Keiner, M. (1973). Atlas of estradiol-concentrating cells in the central nervous system of the female rat. J. Comp. Neurol. 151, 121-158.
54. Pfaff, D. W., and Sakuma, Y. (1979a). Deficit in the lordosis reflex of female rats caused by lesion in the ventromedial nucleus of the hypothalamus. J. Physiol. 288, 203-210.
55. Pfaff, D. W., and Sakuma, Y. (1979b). Facilitation of the lordosis reflex of female rats from the ventromedial nucleus of the hypothalamus. J. Physiol. 288, 189-202.
56. Pfaff, D. W., Schwartz-Giblin, S., McCarthy, M. M., and Kow, L.-M. (1994). Cellular and molecular mechanisms of female reproductive behavior. In E. Knobil and J. D. Neill (Eds.), The Physiology of Reproduction, pp. 107-220. Raven Press, New York.
57. Popper, P., Priest, C. A., and Micevych, P. E. (1995). Effects of sex steroids on the cholecystokinin circuit modulating reproductive behavior. In P. E. Micevych and R. P. Hammer (Eds.), Neurobiological Effects of Sex Steroid Hormones, pp. 160-183. Cambridge Univ. Press, Cambridge.
58. Priest, C. A., Eckersell, C. B., and Micevych, P. E. (1995). Estrogen regulates preproenkephalin-A mRNA levels in the rat ventromedial nucleus: Temporal and cellular aspects. Brain Res. Mol. Brain Res. 28, 251-262.
59. Ratka, A., and Simpkins, J. W. (1991). Effects of estradiol and progesterone on the sensitivity to pain and on morphine-induced antinociception in female rats. Horm. Behav. 25, 217-228.
60. Reichling, D. B., and Basbaum, A. I. (1990). Contribution of brainstem GABAergic circuitry to descending antinociceptive controls. I. GABA-immunoreactive projection neurons in the periaqueductal gray and nucleus raphe magnus. J. Comp. Neurol. 302, 370-377.
61. Renno, W. M., Mullett, M. A., and Beitz, A. J. (1992). Systemic morphine reduces GABA release in the lateral but not medial portion of the midbrain periaqueductal gray of the rat. Brain Res. 594, 221-232.
62. Reynolds, D. V. (1969). Surgery in the rat during electrical analgesia induced by focal brain stimulation. Science 164, 444-445.
63. Riskind, P., and Moss, R. (1979). Midbrain LHRH infusions enhance lordotic behavior in ovariectomized estrogen-primed rats. Brain Res. Bull. 4, 203-205.
64. Rizvi, T. A., Ennis, M., and Shipley, M. T. (1992). Reciprocal connections between the medial preoptic area and the midbrain periaqueductal gray in rat: A WGA-HRP and PHA-L study. J. Comp. Neurol. 315, 1-15.
65. Rizvi, T. A., Murphy, A. Z., Ennis, M., Behbehani, M. M., and Shipley, M. T. (1996). Medial preoptic area afferents to periaqueductal gray medullo-output neurons: A combined Fos and tract tracing study. J. Neurosci. 16, 333-344.
66. Rosenfeld, J. P. (1994). Interacting brain stem components of opiate-activated, descending, pain-inhibitory systems. Neurosci. Biobehav. Rev. 18, 403-409.
67. Sagrillo, C., and Selmanoff, M. (1997). Castration decreases single cell levels of mRNA encoding glutamic acid decarboxylase in the diagonal band of Broca and the sexually dimorphic nucleus of the preoptic area. J. Neuroendocrinol. 9, 699-706.
68. Sakuma, Y., and Pfaff, D. (1979a). Facilitation of female reproductive behavior from mesencephalic central gray in the rat. Am J Physiol. 237, R278-284.
69. Sakuma, Y., and Pfaff, D. (1979b). Mesencephalic mechanisms for integration of female reproductive behavior in the rat. Am J Physiol. 237, R285-290.
70. Saper, C. B., Reis, D. J., and Joh, T. (1983). Medullary catecholamine inputs to the anteroventral third ventricular cardiovascular regulatory region in the rat. Neurosci. Lett. 42, 285-291.
71. Shaikh, M. B., and Siegel, A. (1989). Naloxone-induced modulation of feline aggression elicited from midbrain periaqueductal gray. Pharmacol. Biochem. Behav. 31, 791-796.
72. Shughrue, P. J., Lane, M. V., and Merchenthaler, I. (1997). Comparative distribution of estrogen receptor-alpha and -beta mRNA in the rat central nervous system. J. Comp. Neurol. 388, 507-525.
73. Simerly, R. B., Chang, C., Muramatsu, M., and Swanson, L. W. (1990). Distribution of androgen and estrogen receptor mRNA-containing cells in the rat brain: An in situ hybridization study. J. Comp. Neurol. 294, 76-95.
74. Smith, G. S. T., Savery, D., Marden, C., Costa, J. J. L., Averill, S., Priestley, J. V., and Rattray, M. (1994). Distribution of messenger RNAs encoding enkephalin, substance P, somatostatin, galanin, vasoactive intestinal polypeptide, neuropeptide Y, and calcitonin gene-related peptide in the midbrain periaqueductal grey in the rat. J. Comp. Neurol. 350, 23-40.
75. Turcotte, J. C., and Blaustein, J. D. (1993). Immunocytochemical localization of midbrain estrogen receptor- and progestin receptor-containing cells in female guinea pigs. J. Comp. Neuroll 328, 76-87.
76. van Bockstaele, E. J., Aston-Jones, G., Pieribone, V. A., Ennis, M., and Shipley, M. T. (1991). Subregions of the periaqueductal gray topographically innervate the rostral ventral medulla in the rat. J. Comp. Neurol. 309, 305-327.
77. VanderHorst, V. G. J. M., Schasfoort, F. C., Meijer, E., Van Leeuwen, F. W., and Holstege, G. (1998). Estrogen receptor-alpha-immuno-reactive neurons in the periaqueductal gray of the adult ovariectomized female cat. Neurosci. Lett. 240, 13-16.
78. Van Tol, H. H. M., Bolwerk, E. L. M., Liu, B., and Burbach, J. P. H. (1988). Oxytocin and vasopressin gene expression in the hypothalamo-neurohypophyseal system of the rat during estrous cycle, pregnancy and lactation. Endocrinology 122, 945-951.
79. Vaughan, C. W., Ingram, S. L., Connor, M. A., and Christie, M. J. (1997). How opioids inhibit GABA-mediated neurotransmission. Nature 390, 611-614.
80. Watson, R. E., Wiegand, S. J., Clough, R. W., and Hoffman, G. E. (1986). Use of cryoprotectant to maintain longterm peptide immunoreactivity and tissue morphology. Peptides 7, 155-159.
81. Williams, F. G., Mullet, M. A., and Beitz, A. J. (1995). Basal release of Met-enkephalin and neurotensin in the ventrolateral periaqueductal gray matter of the rat: A microdialysis study of antinociceptive circuits. Brain Res. 690, 207-216.
82. Wood, R., and Newman, S. (1995). Androgen and estrogen receptors coexist within individual neurons in the brain of the Syrian hamster. Neuroendocrinology 62, 487-497.
83. Zhou, L., Blaustein, J. D., and De Vries, G. J. (1994). Distribution of androgen receptor immunoreactivity in vasopressin- and oxytocin-immunoreactive neurons in the male rat brain. Endocrinology 134(6), 2622-2627.