Central organization of androgen-sensitive pathways to the hypothalamic-pituitary-adrenal axis: Implications for individual differences in responses to homeostatic threat and predisposition to disease

Progress in Neuro-Psychopharmacology and Biological Psychiatry

Volumn 29, Issue 8, 2005, Pages 1239-1248

  Williamson, Martin ^a   Bingham, Brenda ^a   Viau, Victor ^a  

^a UNIVERSITY OF BRITISH COLUMBIA   (Canada)

Author keywords

Amygdala; Androgen receptors; Arginine vasopressin; Bed nuclei of the stria terminalis; Corticotropin releasing hormone; Paraventricular nucleus of the hypothalamus; Stress; Testosterone

Indexed keywords

ANDROGEN; ANDROGEN RECEPTOR; ARGIPRESSIN; CORTICOSTERONE; CORTICOTROPIN; CORTICOTROPIN RELEASING FACTOR; GLUCOCORTICOID; TESTOSTERONE;

ADRENAL GLAND; AMYGDALOID NUCLEUS; BEHAVIOR; BRAIN; BRAIN NUCLEUS; DISEASE PREDISPOSITION; EMOTION; FOREBRAIN; GONAD; HOMEOSTASIS; HORMONE ACTION; HORMONE RESPONSE; HORMONE SENSITIVITY; HYPOTHALAMUS HYPOPHYSIS ADRENAL SYSTEM; INDIVIDUALITY; NEUROENDOCRINE SYSTEM; NONHUMAN; REVIEW; STRESS; STRIA TERMINALIS; THALAMUS MIDLINE NUCLEUS; THREAT;

ANDROGENS; ANIMALS; ARGININE VASOPRESSIN; CORTICOSTERONE; DISEASE; HOMEOSTASIS; HUMANS; HYPOTHALAMO-HYPOPHYSEAL SYSTEM; NEURAL PATHWAYS; PITUITARY-ADRENAL SYSTEM; TESTOSTERONE;

EID: 27944503487     PISSN: 02785846     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.pnpbp.2005.08.009     Document Type: Review

References (117)

1. G. Aguilera Regulation of pituitary ACTH secretion during chronic stress Front. Neuroendocrinol. 15 1994 321 350
2. F.A. Antoni Hypothalamic control of adrenocorticotropin secretion: advances since the discovery of 41-residue corticotropin-releasing factor Endocr. Rev. 7 1986 351 378
3. F.A. Antoni Vasopressinergic control of pituitary adrenocorticotropin secretion comes of age Front. Neuroendocrinol. 14 1993 76 122
4. J.M. Aubry, V. Bartanusz, P. Driscol, P. Schulz, T. Steimer, and J.Z. Kiss Corticotropin-releasing factor and vasopressin mRNA levels in roman high- and low-avoidance rats: response to open-field exposure Neuroendocrinology 61 1995 89 97
5. T.L. Bale, and W.W. Vale CRF and CRF receptors: role in stress responsivity and other behaviors Annu. Rev. Pharmacol. Toxicol. 44 2004 525 557
6. A. Bartke, R.E. Steele, N. Musto, and B.V. Caldwell Fluctuations in plasma testosterone levels in adult male rats and mice Endocrinology 92 1973 1223 1228
7. B. Bingham, P. Lee, and V. Viau Androgen and estrogen receptor-β distribution within spinal and pituitary-communicating neurons in the paraventricular nucleus of the rat Proc. 34th Annual Meeting of the Society for Neuroscience, San Diego, CA 2004 Abstract 997.8
8. D.C. Blanchard, R.R. Sakai, B.S. McEwen, S.M. Weiss, and R.J. Blanchard Subordination stress: behavioral, brain, and neuroendocrine correlates Behav. Brain Res. 58 1993 113 121
9. B. Bohus, J.M. Koolhaas, P.G. Luiten, S.M. Korte, lB. Roozendaa, and A. Wiersma The neurobiology of the central nucleus of the amygdala in relation to neuroendocrine and autonomic outflow Prog. Brain Res. 107 1996 447 460
10. J.L. Cameron Interrelationships between hormones, behavior, and affect during adolescence: complex relationships exist between reproductive hormones, stress-related hormones, and the activity of neural systems that regulate behavioral affect. Comments on part III Ann. N. Y. Acad. Sci. 1021 2004 134 142
11. D. Champagne, J. Beaulieu, and G. Drolet CRFergic innervation of the paraventricular nucleus of the rat hypothalamus: a tract-tracing study J. Neuroendocrinol. 10 1998 119 131
12. X. Chen, and J. Herbert The effect of long-term castration on the neuronal and physiological responses to acute or repeated restraint stress: interactions with opioids and prostaglandins J. Neuroendocrinol. 7 1995 137 144
13. R.L. Cole, and P.E. Sawchenko Neurotransmitter regulation of cellular activation and neuropeptide gene expression in the paraventricular nucleus of the hypothalamus J. Neurosci. 22 2002 959 969
14. M.F. Dallman, V. Viau, S. Bhatnagar, F. Gomez, K. Laugero, and M.E. Bell Corticotropin-releasing factor, corticosteroids, stress, and sugar: energy balance, the brain and behavior D.W. Pfaff A.P. Arnold A.M. Etgen S.E. Fahrbach R.T. Rubin Hormones, Brain, and Behavior 2002 Academic Press New York, NY 571 632
15. R. Dantzer, and R.M. Bluthe Vasopressin and behavior: from memory to olfaction Regul. Pept. 45 1993 121 125
16. C.V. Dayas, K.M. Buller, and T.A. Day Neuroendocrine responses to an emotional stressor: evidence for involvement of the medial but not the central amygdala Eur. J. Neurosci. 11 1999 2312 2322
17. C.V. Dayas, K.M. Buller, J.W. Crane, Y. Xu, and T.A. Day Stressor categorization: acute physical and psychological stressors elicit distinctive recruitment patterns in the amygdala and in medullary noradrenergic cell groups Eur. J. Neurosci. 14 2001 1143 1152
18. D.C. De Goeij, H. Dijkstra, and F.J. Tilders Chronic psychosocial stress enhances vasopressin, but not corticotropin-releasing factor, in the external zone of the median eminence of male rats: relationship to subordinate status Endocrinology 131 1992 847 853
19. G.J. De Vries, and M.A. Miller Anatomy and function of extrahypothalamic vasopressin systems in the brain Prog. Brain Res. 119 1998 3 20
20. G.J. DeVries, R.M. Buijs, F.W. Van Leeuwen, A.R. Caffe, and D.F. Swaab The vasopressinergic innervation of the brain in normal and castrated rats J. Comp. Neurol. 233 1985 236 254
21. L.L. DonCarlos, D. Garcia-Ovejero, S. Sarkey, L.M. Garcia-Segura, and I. Azcoitia Androgen receptor immunoreactivity in forebrain axons and dendrites in the rat Endocrinology 144 2003 3632 3638
22. H.W. Dong, and L.W. Swanson Organization of axonal projections from the anterolateral area of the bed nuclei of the stria terminalis J. Comp. Neurol. 468 2004 277 298
23. H.W. Dong, and L.W. Swanson Projections from bed nuclei of the stria terminalis, posterior division: implications for cerebral hemisphere regulation of defensive and reproductive behaviors J. Comp. Neurol. 471 2004 396 433 (Erratum in: J. Comp. Neurol. 474, 603-604.)
24. H.W. Dong, G.D. Petrovich, and L.W. Swanson Topography of projections from amygdala to bed nuclei of the stria terminalis Brain Res. Brain Res. Rev. 38 2001 192 246
25. H.W. Dong, G.D. Petrovich, A.G. Watts, and L.W. Swanson Basic organization of projections from the oval and fusiform nuclei of the bed nuclei of the stria terminalis in adult rat brain J. Comp. Neurol. 436 2001 430 455
26. M. Engelmann, C.T. Wotjak, K. Ebner, and R. Landgraf Behavioural impact of intraseptally released vasopressin and oxytocin in rats Exp. Physiol. 85 2000 125S 130S
27. H.G. Everts, A.J. De Ruiter, and J.M. Koolhaas Differential lateral septal vasopressin in wild-type rats: correlation with aggression Horm Behav. 31 1997 136 144
28. F. Gomez, and M.F. Dallman Manipulation of androgens causes different energetic responses to cold in 60- and 40-day-old male rats J. Physiol. Regul. Integr. Comp. Physiol. 280 2001 R262 R273
29. F. Gomez, S. Manalo, and M.F. Dallman Androgen-sensitive changes in regulation of restraint-induced adrenocorticotropin secretion between early and late puberty in male rats Endocrinology 145 2004 59 70
30. D.K. Grammatopoulos, and G.P. Chrousos Functional characteristics of CRH receptors and potential clinical applications of CRH-receptor antagonists Trends Endocrinol. Metab. 13 2002 436 444
31. D.R. Grattan, and M. Selmanoff Regional variation in gamma-aminobutyric acid turnover: effect of castration on gamma-aminobutyric acid turnover in microdissected brain regions of the male rat J. Neurochem. 60 1993 2254 2264
32. D.R. Grattan, and M. Selmanoff Castration-induced decrease in the activity of medial preoptic and tuberoinfundibular GABAergic neurons is prevented by testosterone Neuroendocrinology 60 1994 141 149
33. M. Hallbeck, O. Hermanson, and A. Blomqvist Distribution of preprovasopressin mRNA in the rat central nervous system J. Comp. Neurol. 411 1999 181 200
34. R.J. Handa, L.H. Burgess, J.E. Kerr, and J.A. O'Keefe Gonadal steroid hormone receptors and sex differences in the hypothalamo-pituitary-adrenal axis Horm. Behav. 28 1994 464 476
35. R.J. Handa, J.E. Kerr, L.L. DonCarlos, R.F. McGivern, and G. Hejna Hormonal regulation of androgen receptor messenger RNA in the medial preoptic area of the male rat Brain Res. Mol. Brain Res. 39 1996 57 67
36. M. Hatzinger, C.T. Wotjak, T. Naruo, R. Simchen, M.E. Keck, R. Landgraf, F. Holsboer, and I.D. Neumann Endogenous vasopressin contributes to hypothalamic-pituitary-adrenocortical alterations in aged rats J. Endocrinol. 164 2000 197 205
37. J.P. Henry Biological basis of the stress response Integr. Physiol. Behav. Sci. 27 1992 66 83
38. J.P. Herman, and W.E. Cullinan Neurocircuitry of stress: central control of the hypothalamo-pituitary-adrenocortical axis Trends Neurosci. 20 1997 78 84
39. J.P. Herman, M.K. Schafer, S.J. Watson, and T.G. Sherman In situ hybridization analysis of arginine vasopressin gene transcription using intron-specific probes Mol. Endocrinol. 5 1991 1447 1456
40. J.P. Herman, M.K. Schafer, R.C. Thompson, and S.J. Watson Rapid regulation of corticotropin-releasing hormone gene transcription in vivo Mol. Endocrinol. 6 1992 1061 1069
41. J.P. Herman, W.E. Cullinan, and S.J. Watson Involvement of the bed nucleus of the stria terminalis in tonic regulation of paraventricular hypothalamic CRH and AVP mRNA expression J. Neuroendocrinol. 6 1994 433 442
42. J.P. Herman, J.G. Tasker, D.R. Ziegler, and W.E. Cullinan Local circuit regulation of paraventricular nucleus stress integration: glutamate-GABA connections Pharmacol. Biochem. Behav. 71 2002 457 468
43. J.P. Herman, W.E. Cullinan, D.R. Ziegler, and J.G. Tasker Role of the paraventricular nucleus microenvironment in stress integration Eur. J. Neurosci. 16 2002 381 385
44. J.P. Herman, H. Figueiredo, N.K. Mueller, Y. Ulrich-Lai, M.M. Ostrander, D.C. Choi, and W.E. Cullinan Central mechanisms of stress integration: hierarchical circuitry controlling hypothalamo-pituitary-adrenocortical responsiveness Front. Neuroendocrinol. 24 2003 151 180
45. J.P. Herman, N.K. Mueller, and H. Figueiredo Role of GABA and glutamate circuitry in hypothalamo-pituitary-adrenocortical stress integration Ann. N. Y. Acad. Sci. 1018 2004 35 45
46. F. Hernando, O. Schoots, S.J. Lolait, and J.P. Burbach Immunohistochemical localization of the vasopressin V1b receptor in the rat brain and pituitary gland: anatomical support for its involvement in the central effects of vasopressin Endocrinology 142 2001 1659 1668
47. C. Isgor, M. Cecchi, M. Kabbaj, H. Akil, and S.J. Watson Estrogen receptor beta in the paraventricular nucleus of hypothalamus regulates the neuroendocrine response to stress and is regulated by corticosterone Neuroscience 121 2003 837 845
48. D.S. Jessop Review: central non-glucocorticoid inhibitors of the hypothalamo-pituitary-adrenal axis J. Endocrinol. 160 1999 169 180
49. P.S. Kalra, and S.P. Kalra Circadian periodicities of serum androgens, progesterone, gonadotropins and luteinizing hormone-releasing hormone in male rats: the effects of hypothalamic differentation Endocrinology 101 1977 1821 1827
50. A. Kalsbeek, R.M. Buijs, J.J. van Heerikhuize, M. Arts, and T.P. van der Woude Vasopressin-containing neurons of the suprachiasmatic nuclei inhibit corticosterone release Brain Res. 580 1992 62 67
51. J.M. Koolhaas, H. Everts, A.J. de Ruiter, S.F. de Boer, and B. Bohus Coping with stress in rats and mice: differential peptidergic modulation of the amygdala-lateral septum complex Prog. Brain Res. 119 1998 437 448
52. K.J. Kovacs, A. Foldes, and P.E. Sawchenko Glucocorticoid negative feedback selectively targets vasopressin transcription in parvocellular neurosecretory neurons J. Neurosci. 20 2000 3843 3852
53. R. Landgraf, C.T. Wotjak, I.D. Neumann, and M. Engelmann Release of vasopressin within the brain contributes to neuroendocrine and behavioral regulation Prog. Brain Res. 119 1998 201 220
54. B. Lesniewska, B. Miskowiak, M. Nowak, and L.K. Malendowicz Sex differences in adrenocortical structure and function: XXVII. The effect of ether stress on ACTH and corticosterone in intact, gonadectomized, and testosterone- or estradiol-replaced rats Res. Exp. Med. (Berl.) 190 1990 95 103
55. V.N. Luine, D.R. Grattan, and M. Selmanoff Gonadal hormones alter hypothalamic GABA and glutamate levels Brain Res. 747 1997 165 168
56. T.D. Lund, D.J. Munson, M.E. Haldy, and R.J. Handa Androgen inhibits, while oestrogen enhances, restraint-induced activation of neuropeptide neurones in the paraventricular nucleus of the hypothalamus J. Neuroendocrinol. 16 2004 272 278
57. T.D. Lund, D.J. Munson, M.E. Haldy, and R.J. Handa Dihydrotestosterone may inhibit hypothalamo-pituitary-adrenal activity by acting through estrogen receptor in the male mouse Neurosci. Lett. 365 2004 43 47
58. X.M. Ma, S.L. Lightman, and G. Aguilera Vasopressin and corticotropin-releasing hormone gene responses to novel stress in rats adapted to repeated restraint Endocrinology 140 1999 3623 3632
59. G.B. Makara The relative importance of hypothalamic neurons containing corticotropin- releasing factor or vasopressin in the regulation of adrenocorticotropic hormone secretion Ciba Found. Symp. 168 1992 43 51
60. G.B. Makara, Z. Mergl, and D. Zelena The role of vasopressin in hypothalamo-pituitary-adrenal axis activation during stress: an assessment of the evidence Ann. N. Y. Acad. Sci. 1018 2004 151 161
61. M. Mauri, A. Calderone, and V. Camilleri Gender differences in anxiety disorders: the role of female hormones A.R. Genazzani Hormone Replacement Therapy and The Brain. The Current Status of Research and Practice 2003 Parthenon Publishing New York, NY 161 167
62. B.S. McEwen Sex, stress and the hippocampus: allostasis, allostatic load and the aging process Neurobiol. Aging 23 2002 921 939
63. B.S. McEwen, and J.C. Wingfield The concept of allostasis in biology and biomedicine Horm. Behav. 43 2003 2 15
64. L.R. Meek, R.D. Romeo, C.M. Novak, and C.L. Sisk Actions of testosterone in prepubertal and postpubertal male hamsters: dissociation of effects on reproductive behavior and brain androgen receptor immunoreactivity Horm Behav. 31 1997 75 88
65. M.B. Muller, R. Landgraf, J. Preil, I. Sillaber, A.E. Kresse, M.E. Keck, S. Zimmermann, F. Holsboer, and W. Wurst Selective activation of the hypothalamic vasopressinergic system in mice deficient for the corticotropin-releasing hormone receptor 1 is dependent on glucocorticoids Endocrinology 141 2000 4262 4269
66. N.L. Ostrowski, S.J. Lolait, and W.S. Young III Cellular localization of vasopressin V1a receptor messenger ribonucleic acid in adult male rat brain, pineal, and brain vasculature Endocrinology 135 1994 1511 1528
67. G.D. Petrovich, N.S. Canteras, and L.W. Swanson Combinatorial amygdalar inputs to hippocampal domains and hypothalamic behavior systems Brain. Res. Brain Res. Rev. 38 2001 247 289
68. P.M. Plotsky, T.O. Bruhn, and W. Vale Central modulation of immunoreactive corticotropin-releasing factor secretion by arginine vasopressin Endocrinology 115 1984 1639 1641
69. S.R. Plymate, J.S. Tenover, and W.J. Bremner 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 1989 366 371
70. C.M. Prewitt, and J.P. Herman Hypothalamo-pituitary-adrenocortical regulation following lesions of the central nucleus of the amygdala Stress 1 1997 263 280
71. C.M. Prewitt, and J.P. Herman Anatomical interactions between the central amygdaloid nucleus and the hyptohalamic paraventricular nucleus of the rat: a dual tract-tracing analysis J. Chem. Neuroanat. 15 1998 173 185
72. P.Y. Risold, R.H. Thompson, and L.W. Swanson The structural organization of connections between hypothalamus and cerebral cortex Brain Res. Brain Res. Rev. 24 1997 197 254
73. C. Rivier, and S. Rivest Effect of stress on the activity of the hypothalamic-pituitary-gonadal axis: peripheral and central mechanisms Biol. Reprod. 45 1991 523 532
74. R.D. Romeo, S.L. Diedrich, and C.L. Sisk Effects of gonadal steroids during pubertal development on androgen and estrogen receptor-alpha immunoreactivity in the hypothalamus and amygdala J. Neurobiol. 44 2000 361 368
75. R.D. Romeo, S.J. Lee, N. Chhua, C.R. McPherson, and B.S. McEwen Testosterone cannot activate an adult-like stress response in prepubertal male rats Neuroendocrinology 79 2004 125 132
76. L.M. Romero, S. Levine, and R.M. Sapolsky Patterns of adrenocorticotropin secretagog release in response to social interactions and various degrees of novelty Psychoneuroendocrinology 20 1995 183 191
77. D.R. Rubinow, and P.J. Schmidt Gonadal steroids, brain, and behavior: role of context Dialogues Clin. Neurosci. 4 2002 123 137
78. P.E. Sawchenko, and L.W. Swanson Immunohistochemical identification of neurons in the paraventricular nucleus of the hypothalamus that project to the medulla or to the spinal cord in the rat J. Comp. Neurol. 205 1982 260 272
79. P.E. Sawchenko, E.R. Brown, R.K. Chan, A. Ericsson, H.Y. Li, B.L. Roland, and K.J. Kovacs The paraventricular nucleus of the hypothalamus and the functional neuroanatomy of visceromotor responses to stress Prog. Brain Res. 107 1996 201 222
80. P.E. Sawchenko, H.Y. Li, and A. Ericsson Circuits and mechanisms governing hypothalamic responses to stress: a tale of two paradigms Prog. Brain Res. 122 2000 61 78
81. P.J. Schmidt, K.L. Berlin, M.A. Danaceau, A. Neeren, N.A. Haq, C.A. Roca, and D.R. Rubinow The effects of pharmacologically induced hypogonadism on mood in healthy men Arch. Gen. Psychiatry. 61 2004 997 1004
82. T.E. Seeman, B. Singer, C.W. Wilkinson, and B. McEwen Gender differences in age-related changes in HPA axis reactivity Psychoneuroendocrinology 26 2001 225 240
83. I. Sencar-Cupovic, and S. Milkovic The development of sex differences in the adrenal morphology and responsiveness in stress of rats from birth to the end of life Mech. Ageing Dev. 5 1976 1 9
84. M.M. Shores, V.M. Moceri, K.L. Sloan, A.M. Matsumoto, and D.R. Kivlahan Low testosterone levels predict incident depressive illness in older men: effects of age and medical morbidity J. Clin. Psychiatry 66 2005 7 14
85. T.J. Shors Opposite effects of stressful experience on memory formation in male versus females Dialogues Clin. Neurosci. 4 2002 139 147
86. R.B. Simerly, C. Chang, M. Muramatsu, and L.W. Swanson 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
87. J.W. Simpkins, P.S. Kalra, and S.P. Kalra Alterations in daily rhythms of testosterone and progesterone in old male rats Exp. Aging Res. 7 1981 25 32
88. J.E. Stern, and W. Zhang Preautonomic neurons in the paraventricular nucleus of the hypothalamus contain estrogen receptor beta Brain Res. 975 2003 99 109
89. L.W. Swanson, and P.E. Sawchenko Hypothalamic integration: organization of the paraventricular and supraoptic nuclei Annu. Rev. Neurosci. 6 1983 269 324
90. L.K. Takahashi Role of CRF(1) and CRF(2) receptors in fear and anxiety Neurosci. Biobehav. Rev. 25 2001 627 636
91. K.L. Tamashiro, M.M. Nguyen, T. Fujikawa, T. Xu, Ma.L. Yun, S.C. Woods, and R.R. Sakai Metabolic and endocrine consequences of social stress in a visible burrow system Physiol. Behav. 80 2004 683 693
92. G. Van den Berghe Dynamic neuroendocrine responses to critical illness Front. Neuroendocrinol. 23 2002 370 391
93. K. Van Pett, V. Viau, J.C. Bittencourt, R.K. Chan, H.Y. Li, C. Arias, G.S. Prins, M. Perrin, W. Vale, and P.E. Sawchenko Distribution of mRNAs encoding CRF receptors in brain and pituitary of rat and mouse J. Comp. Neurol. 428 2000 191 212
94. V. Viau Functional cross-talk between the hypothalamic-pituitary-gonadal and -adrenal axes J. Neuroendocrinol. 14 2002 506 513
95. V. Viau, and M.J. Meaney The inhibitory effect of testosterone on hypothalamic-pituitary-adrenal responses to stress is mediated by the medial preoptic area J. Neurosci. 16 1996 1866 1876
96. V. Viau, and M.J. Meaney Alpha1 adrenoreceptors mediate the stimulatory effects of oestrogen on stress-related hypothalamic-pituitary-adrenal activity in the female rat J. Neuroendocrinol. 16 2004 72 78
97. V. Viau, and M.J. Meaney Testosterone-dependent variations in plasma and intrapituitary corticosteroid binding globulin and stress hypothalamic- pituitary-adrenal activity in the male rat J. Endocrinol. 181 2004 223 231
98. V. Viau, and P.E. Sawchenko Hypophysiotropic neurons of the paraventricular nucleus respond in spatially, temporally, and phenotypically differentiated manners to acute vs. repeated restraint stress J. Comp. Neurol. 445 2002 293 307
99. V. Viau, A. Chu, L. Soriano, and M.F. Dallman Independent and overlapping effects of corticosterone and testosterone on corticotropin-releasing hormone and arginine vasopressin mRNA expression in the paraventricular nucleus of the hypothalamus and stress-induced adrenocorticotropic hormone release J. Neurosci. 19 1999 6684 6693
100. V. Viau, L. Soriano, and M.F. Dallman Androgens alter corticotropin releasing hormone and arginine vasopressin mRNA within forebrain sites known to regulate activity in the hypothalamic-pituitary-adrenal axis J. Neuroendocrinol. 13 2001 442 452
101. V. Viau, P. Lee, J. Sampson, and J. Wu A testicular influence on restraint-induced activation of medial parvocellular neurons in the paraventricular nucleus in the male rat Endocrinology 144 2003 3067 3075
102. V. Viau, B. Bingham, J. Davis, P. Lee, and M. Wong Gender and puberty interact on the stress-induced activation of parvocellular neurosecretory neurons and corticotropin-releasing hormone messenger ribonucleic acid expression in the rat Endocrinology 146 2005 137 146
103. S. Volpi, C. Rabadan-Diehl, and G. Aguilera Vasopressinergic regulation of the hypothalamic pituitary adrenal axis and stress adaptation Stress 7 2004 75 83
104. D.L. Walker, D.J. Toufexis, and M. Davis Role of the bed nucleus of the stria terminalis versus the amygdala in fear, stress, and anxiety Eur. J. Pharmacol. 463 2003 199 216
105. A.G. Watts, and L.W. Swanson 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 1989 1734 1738
106. A. Weindl, and M. Sofroniew Neuroanatomical pathways related to vasopressin Curr. Top. Neuroendocrinol. 4 1985 137 195
107. M.H. Whitnall Distributions of pro-vasopressin expressing and pro-vasopressin deficient CRH neurons in the paraventricular hypothalamic nucleus of colchicine-treated normal and adrenalectomized rats J. Comp. Neurol. 275 1988 13 28
108. M.H. Whitnall Regulation of the hypothalamic corticotropin-releasing hormone neurosecretory system Prog. Neurobiol. 40 1993 573 629
109. M. Williamson, B. Bingham, and V. Viau Immunohistochemical detection of androgen receptor-expressing neurons that project to the paraventricular nucleus of the hypothalamus Proc. 34th Annual Meeting of the Society for Neuroscience, San Diego, CA 2004 Abstract 425.12
110. J.C. Wingfield, and R.M. Sapolsky Reproduction and resistance to stress: when and how J. Neuroendocrinol. 15 2003 711 724
111. S.J. Winters, R. Medhamurthy, V.L. Gay, and T.M. Plant A comparison of moment to moment and diurnal changes in circulating inhibin and testosterone concentrations in male rhesus monkeys (Macaca mulatta) Endocrinology 129 1991 1755 1761
112. C.T. Wotjak, M. Kubota, G. Liebsch, A. Montkowski, F. Holsboer, I. Neumann, and R. Landgraf Release of vasopressin within the rat paraventricular nucleus in response to emotional stress: a novel mechanism of regulating adrenocorticotropic hormone secretion? J. Neurosci. 16 1996 7725 7732
113. M.J. Yoo, R.V. Searles, J.R. He, W.B. Shen, D.R. Grattan, and M. Selmanoff Castration rapidly decreases hypothalamic gamma-aminobutyric acidergic neuronal activity in both male and female rats Brain Res. 878 2000 1 10
114. E.A. Young The role of gonadal steroids in hypothalamic-pituitary-adrenal axis regulation Crit. Rev. Neurobiol. 9 1995 371 381
115. E.A. Young, and M. Altemus Puberty, ovarian steroids, and stress. Puberty, ovarian steroids, and stress Ann. N. Y. Acad. Sci. 1021 2004 124 133
116. D. Zelena, A. Foldes, Z. Mergl, I. Barna, K.J. Kovacs, and G.B. Makara Effects of repeated restraint stress on hypothalamo-pituitary-adrenocortical function in vasopressin deficient Brattleboro rats Brain Res. Bull. 63 2004 521 530
117. L. Zhou, J.D. Blaustein, and G.J. De Vries Distribution of androgen receptor immunoreactivity in vasopressin- and oxytocin-immunoreactive neurons in the male rat brain Endocrinology 134 1994 2622 2627