The inhibitory effect of testosterone on hypothalamic-pituitary-adrenal responses to stress is mediated by the medial preoptic area

Journal of Neuroscience

Volumn 16, Issue 5, 1996, Pages 1866-1876

  Viau, Victor ^a   Meaney, Michael J ^a  

^a MCGILL UNIVERSITY   (Canada)

Author keywords

ACTH; arginine vasopressin; glucocorticoid receptors; medial preoptic area; stress; testosterone

Indexed keywords

ARGIPRESSIN; CORTICOTROPIN; CORTICOTROPIN RELEASING FACTOR; GLUCOCORTICOID RECEPTOR; MINERALOCORTICOID RECEPTOR; TESTOSTERONE;

ANIMAL EXPERIMENT; ARTICLE; CONTROLLED STUDY; HYPOTHALAMUS HYPOPHYSIS ADRENAL SYSTEM; MALE; NONHUMAN; PREOPTIC AREA; PRIORITY JOURNAL; RAT; STRESS; TESTOSTERONE BLOOD LEVEL; TESTOSTERONE RELEASE;

EID: 0029960048     PISSN: 02706474     EISSN: None     Source Type: Journal    
DOI: 10.1523/jneurosci.16-05-01866.1996     Document Type: Article

References (74)

1. Acs Z, Stark E (1978) Possible role of γ-aminobutyric acid synthesis in the mechanism of dexamethasone feedback action. J Endocrinol 77:137-141.
2. Aguilera G, Lightman SL, Kiss A (1993) Regulation of the hypothalamic-pituitary-adrenal axis during water deprivation. Endocrinology 132:241-248.
3. Antoni FA (1993) Vasopressinergic control of pituitary adrenocorticotropin secretion comes of age. Front Neuroendocrinol 14:76-122.
4. Bartke A, Steele RE, Musto N, Caldwell BV (1973) Fluctuations in plasma testosterone levels in adult male rats and mice. Endocrinology 92:1223-1228.
5. Bingaman EW, Magnuson DJ, Gray TS, Handa RJ (1994) Androgen inhibits the increases in hypothalamic corticotropin-releasing hormone (CRH) and CRH-immunoreactivity following gonadectomy. Neuroendocrinology 59:228-234.
6. Bohler HCL, Zoeller RT, King JC, Rubin BS, Weber R, Merriam GR (1990) Corticotropin-releasing hormone mRNA is elevated on the afternoon of proestrous in the parvocellular paraventricular nuclei of the female rat. Mol Brain Res 8:259-262.
7. Bradford M (1976) A rapid and sensitive method for quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72:248-254.
8. Buijs RM (1978) Intra- and extrahypothalamic vasopressin and oxytocin pathways in the rat. Cell Tissue Res 192:423-435.
9. Cuello AC, Horn AS, MacKay AVP, Iversen LL (1973) Catecholamines in the median eminence: new evidence for a major noradrenergic input. Nature 243:465.
10. Cullinan WE, Herman JP, Watson SJ (1993) Ventral subicular interaction with the hypothalamic paraventricular nucleus: evidence for a relay in the bed nucleus of the stria terminalis. J Comp Neurol 332:1-20.
11. Dallman MF, Akana SF, Cascio CS, Darlington DN, Jacobson L, Levin N (1987) Regulation of ACTH secretion: variations on a theme of B. Recent Prog Horm Res 43:113-173.
12. Dallman MF, Akana SF, Scribner KA, Bradbury MJ, Walker C-D, Strack AM, Cascio CS (1993) Stress, feedback and facilitation in the hypothalamo-pituitary-adrenal axis. J Neuroendocrinology 4:517-526.
13. Decavel C, van den Pol AN (1990) GABA: a dominant neurotransmitter in the hypothalamus. J Comp Neurol 302:1019-1037.
14. De Vries GJ, Buijs RM, Sluiter AA (1984) Gonadal hormone actions on the morphology of the vasopressinergic innervation of the adult rat brain. Brain Res 298:141-145.
15. De Vries GJ, Buijs RM, Van Leeuwen FW, Caffe AR, Swaab DF (1985) The vasopressinergic innervation of the brain in normal and castrated rats. J Comp Neurol 233:236-254.
16. Diorio D, Viau V, Meaney MJ (1993) The role of the medial prefrontal cortex (cingulate gyrus) in the regulation of hypothalamic-pituitary-adrenal responses to stress. J Neurosci 13:3839-3847.
17. Dohanics J, Hoffman GE, Verbalis JG (1991) Hyponatremia-induced inhibition of magnocellular neurons causes stressor-selective impairment of stimulated adrenocorticotropin secretion in rats. Endocrinology 128:331-340.
18. Dubey AK, Herbert J, Abbott DA, Martenz ND (1984) Serum and CSF concentrations of testosterone and LH related to negative feedback in male rhesus monkeys. Neuroendocrinology 39:176-185.
19. Dubois PM, Morel G, Forest MG, Dubois MP (1978) Localization of luteinizing hormone (LH) and testosterone or dihydrotestosterone (DHT) in the gonadocropic cells of the anterior pituitary by using ultracryomicrotomy and immunocytochemistry. Horm Metab Res 10:250-252.
20. Feldman S, Conforti N, Saphier D (1990) The preoptic area and bed nucleus of the stria terminalis are involved in the effects of the amygdala on adrenocortical secretion. Neuroscience 37:775-779.
21. Grattan DR, Sagrillo CA, Selmanoff M, Ruchkin DS (1992) Effects of castration on GABA turnover in microdissected brain regions in the male rat. Soc Neurosci Abstr 18:456.
22. Handa RJ, Nunley KM, Lorens SA, Louie JP, McGivern RF, Bollnow MR (1994) Androgen regulation of adrenocorticotropin and corticosterone secretion in the male rat following novelty and foot shock stressors. Physiol Behav 55:117-124.
23. Hermes MLHJ, Buijs RM, Renaud LP (1991) Electrical stimulation in the suprachiasmatic nucleus depresses the activity in neurons in the hypothalamic paraventricular nucleus region. Soc Neurosci Abstr 17:542.
24. Hiroshige T, Abe K, Wada S, Kaneko M (1973) Sex difference in circadian periodicity of CRF activity in the rat hypothalamus. Neuroendocrinology 11:306-320.
25. Hoorneman EMD, Buijs RM (1982) Vasopressin fiber pathways in the rat brain following suprachiasmatic nucleus lesioning. Brain Res 243:235-241.
26. Irvine CHG, Alexander SL, Donald RA (1989) Effect of osmotic stimulus on the secretion of arginine vasopressin and adrenocorticotropin in the horse. Endocrinology 124:3102-3108.
27. Jones MT, Gillham B, Altaher ARH, Nicholson SA, Campbell EA, Watts SM, Thody A (1984) Clinical and experimental studies on the role of GABA in the regulation of ACTH secretion: a review. Psychoneuroendocrinology 9:107-123.
28. Kalra PS, Kalra SP (1977) Circadian periodicities of serum androgens, progesterone, gonadotropins and luteinizing hormone-releasing hormone in male rats: the effects of hypothalamic deafferentation, castration and adrenalectomy. Endocrinology 101:1821-1827.
29. Kalsbeek A, Buijs RM, van Heerikhuize JJ, Arts M, van der Woude TP (1992) Vasopressin-containing neurons of the suprachiasmatic nuclei inhibit corticosterone release. Brain Res 580:62-67.
30. Kant GJ, Lenox RH, Bunnell BN, Mougey EH, Pennington LL, Meyerhoff JL (1983) Comparison of stress response in male and female rats: pituitary cyclic AMP and plasma prolactin, growth hormone and corticosterone. Psychoneuroendocrinology 8:421-428.
31. Kitay JI (1968) Effects of estrogen and androgen on the adrenal cortex of the rat. In: Functions of the adrenal cortex (McKerns KW, ed), pp 775-811. New York: Appleton-Century-Crofts.
32. Kovacs KJ, Makara G (1988) Corticosterone and dexamethasone act at different brain sites to inhibit adrenalectomy-induced adrenocorticotropin hypersecretion. Brain Res 474:205-210.
33. Krey LC, Lu K, Butler W, Hotchkiss J, Piva F, Knobil E (1975) Surgical disconnections of the medial basal hypothalamus and pituitary function in the rhesus monkey. II. GH and cortisol secretion. Endocrinology 96:1088-1093.
34. Krieger HP, Krieger DT (1970) Chemical stimulation of the brain: effect on adrenal corticoid release Am J Physiol 218:1632-1641.
35. Le Mevel JC, Abitibol S, Beraud G, Maniey J (1978) Dynamic changes in plasma adrenocorticotrophin after neurotropic stress in male and female rats. J Endocrinol 76:359-360.
36. Le Mevel JC, Abitibol S, Beraud G, Maniey J (1979) Temporal changes in plasma adrenocorticotropin concentration after repeated neurotropic stress in male and female rats. Endocrinology 105:812-817.
37. Lescoat G, Jego P, Beraud B, Maniey J (1970) Influence de sexe sur les modalités de réponse de l'axe hypothalamo-hypophyso-surrénalien aux agressions emotionellcs et somatiques chez le rat. C R Seances Soc Biol Fil 164:2106-2113.
38. Meaney MJ, McEwen BS (1986) Testosterone implants into the amygdala during the neonatal period masculinize the social play of juvenile female rats. Brain Res 398:324-328.
39. McEwen BS (1980) Binding and metabolism of sex steroids by the hypothalamic-pituitary unit: physiological implications. Annu Rev Physiol 42:97-110.
40. Nicoll RA, Barker JL (1971) The pharmacology of recurrent inhibition in the supraoptic neurosecretory system. Brain Res 35:501-511.
41. Nissen R, Cunningham JT, Allen AM, Renaud LP (1991) Ibotenic acid lesions of median preoptic nucleus do not influence baroreceptor-induced inhibition of suproptic vasopressin-secreting neurons in the rat. Soc Neurosci Abstr 17:473.
42. 131I. Proc Soc Exp Biol Med 128:807-811.
43. Palkovits M (1987) Anatomy of neural pathways affecting CRH secretion. Ann NY Acad Sci 512:139-148.
44. Papir-Kricheli D, Feldman S (1982) Steroid sensitive identified and unidentified neurons in the medial preoptic area of the rat. Neuroscience 7:2793-2800.
45. Paxinos G, Watson D (1982) The rat brain in stereotaxic coordinates. New York: Academic.
46. Plymate SR, Tenover JS, Bremner WJ (1989) Circadian variation in testosterone, sex hormone-binding globulin, and calculated non-sex hormone-binding globulin bound testosterone in healthy young and elderly men. J Androl 10:366-371.
47. Raff H, Papanek PE, Cowley AW (1991) ACTH and vasopressin responses to insulin-induced hypoglycemia in intact and neurohypophysectomized conscious dogs. Neuroendocrinology 53:85-90.
48. Redgate ES, Fahringer EE (1973) A comparison of the pituitary adrenal activity elicited by electrical stimulation of preoptic, amygdaloid and hypothalamic sites in the rat brain. Neuroendocrinology 12:334-343.
49. Rittmaster RS, Cutler GB, Gold PW, Brandon DD, Tomai T, Loriaux DL, Chrousos GP (1987) The relationship of saline-induced changes in vasopressin secretion to basal and corticotropin-releasing hormone-stimulated adrenocorticotropin and cortisol secretion in man. J Clin Endocrinol Metab 64:371-376.
50. Rivier C, Rivest W (1991) Effect of stress on the activity of the hypothalamic-pituitary-gonadal axis: peripheral and central mechanisms. Biol Reprod 45:523-532.
51. Roland BL, Sawchenko PE (1993) Local origins of some GABAergic projections to the paraventricular and supraoptic nuclei of the hypothalamus in the rat. J Comp Neurol 332:123-143.
52. Roselli CE, Horton LE, Resko JA (1985) Distribution and regulation of aromatase activity in the rat hypothalamus and limbic system. Endocrinology 117:2471-2477.
53. Saphier D. Feldman S (1985) Effects of neural stimuli on paraventricular nucleus neurones. Brain Res Bull 14:401-407.
54. Saphier D, Feldman S (1986) Effects of stimulation of the preoptic area on hypothalamic paraventricular nucleus unit activity and corticosterone secretion in freely moving rats. Neuroendocrinology 42:167-173.
55. Sapolsky RM, Armanini MP, Packan DR, Sutton SW, Plotsky PM (1990) Glucocorticoid feedback inhibition of adrenocorticotropic hormone secretagogue release. Neuroendocrinology 51:328-336.
56. Simerly RB, Swanson LW (1988) Projections of the medial preoptic nucleus: a Phaseolus vulgaris leucoagglutinin anterograde tract-tracing study in the rat. J Comp Neurol 270:209-242.
57. Simeriy RB, Chang C, Muramatsu M, Swanson LW (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.
58. Skowsky WR, Swan L, Smith P (1979) Effects of sex steroid hormones on arginine vasopressin in intact and castrated male and female rats. Endocrinology 104:105-108.
59. Smith ER, Damassa DA, Davidson JM (1977) Hormone administration: peripheral and intracranial implants. Methods Psychobiol 3:249-279.
60. Swanson LW (1976) An autoradiographic study of the efferent connections of the preoptic region in the rat. J Comp Neurol 167:227-256.
61. Swanson LW (1987) The hypothalamus. In: Handbook of chemical neuroanatomy (Björklund A, Hökfelt T, Swanson LW, eds), pp 1-124. New York: Elsevier.
62. Tallarida RJ, Murray RB (1981) Area under a curve: Simpson's rule and trapezoidal rule. In: Manual of pharmacological calculations with computer programs, pp 47-49. New York: Springer.
63. Telegdy GL, Schreiberg G, Endroczi E (1964) Effects of estrogens implanted into the hypothalamus on the activity of the pituitary-adrenocortical system. Acta Physiol Acad Sci Hung 25:229-234.
64. Thieulant ML, Duvall J (1985) Differential distribution of androgen and estrogen receptors in rat pituitary cell populations separated by centrifugal elutriation. Endocrinology 116:1299-1303.
65. Urban JH, Miller MA, Dorsa DM (1991) Dexamethasone-induced suppression of vasopressin gene expression in the bed nucleus of the stria terminalis and medial amygdala is mediated by changes in testosterone. Endocrinology 128:109-116.
66. Vale W, Vaughan J, Yamamoto G, Bruhn T, Douglas C, Dalton D, Rivier C, Rivier J (1983) Assay for corticotropin releasing factor. In: Methods in enzymology (Conn PM, ed), pp 565-577. New York: Academic.
67. Viau V, Meaney MJ (1991a) Variations in the hypothalamic-pituitary-adrenal response to stress during the estrous cycle in the rat. Endocrinology 129:2503-2511.
68. Viau V, Meaney MJ (1991b) Individual differences in the hypothalamic-pituitary-adrenal response to stress: relationship to testosterone. Soc Neurosci Abstr 17:542.
69. Viau V, Meaney MJ (1992) Regulation of ACTH co-secretagogues during the estrous cycle in the rat. Soc Neurosci Abstr 18:643.
70. Viau V, Plotsky PM, Meaney MJ (1993) Increased plasma ACTH responses to stress in non-handled compared with handled rats require basal levels of corticosterone and are associated with increased levels of ACTH secretagogues in the median eminence. J Neurosci 13:1097-1105.
71. Watts AG, Swanson LW (1989) Diurnal variations in the content of preprocorticotropin-releasing hormone messenger ribonucleic acids in the hypothalamic paraventricular nucleus of rats of both sexes as measured by in situ hybridization. Endocrinology 125:1734-1738.
72. Whitnall MH (1993) Regulation of the hypothalamic corticotropin-releasing hormone neurosecretory system. Prog Neurobiol 40:573-629.
73. Winters SJ, Medhamurthy R, Gay VL, Plant TM (1991) A comparison of moment to moment and diurnal changes in circulating inhibin and testosterone concentrations in male rhesus monkeys. Endocrinology 129:1755-1761.
74. Zhou L, Blaustein JD, De Vries GJ (1994) Distribution of androgen receptor immunoreactivity in vasopressin- and oxytocin-immunoreactive neurons in the male rat brain. Endocrinology 134: 2622-2627.