Androgen receptor expressing neurons that project to the paraventricular nucleus of the hypothalamus in the male rat

Journal of Comparative Neurology

Volumn 503, Issue 6, 2007, Pages 717-740

  Williamson, Martin ^a   Viau, Victor ^a  

^a UNIVERSITY OF BRITISH COLUMBIA   (Canada)

Author keywords

Androgen receptor; Catecholamine neurons; FluoroGold; Hypothalamic pituitary adrenal axis; Paraventricular nucleus of the hypothalamus

Indexed keywords

ANDROGEN RECEPTOR; CORTICOTROPIN RELEASING FACTOR; FLUOROGOLD;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CAUDATE NUCLEUS; CONTROLLED STUDY; FOREBRAIN; HYPOTHALAMUS; MALE; MEDULLA OBLONGATA; NERVE CELL; NONHUMAN; PARABRACHIAL NUCLEUS; PERIAQUEDUCTAL GRAY MATTER; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; RHOMBENCEPHALON; STAINING; STRIA TERMINALIS; THALAMUS MIDLINE NUCLEUS;

ANIMALS; HYPOTHALAMO-HYPOPHYSEAL SYSTEM; MALE; NEURAL PATHWAYS; NEURONS; PARAVENTRICULAR HYPOTHALAMIC NUCLEUS; PITUITARY-ADRENAL SYSTEM; RATS; RATS, SPRAGUE-DAWLEY; RECEPTORS, ANDROGEN;

EID: 34548060062     PISSN: 00219967     EISSN: 10969861     Source Type: Journal    
DOI: 10.1002/cne.21411     Document Type: Article

References (240)

1. Abercrombie M. 1946. Estimation of nuclear population from microtome sections. Anat Rec 94:239-247.
2. Argente J, Chowen-Breed JA, Steiner RA, Clifton DK. 1990. Somatostatin messenger RNA in hypothalamic neurons is increased by testosterone through activation of androgen receptors and not by aromatization to estradiol. Neuroendocrinology 52:342-349.
3. Auger CJ, De Vries GJ. 2002. Progestin receptor immunoreactivity within steroid-responsive vasopressin-immunoreactive cells in the male and female rat brain. J Neuroendocrinol 14:561-567.
4. Baker RA, Herkenham M. 1995. Arcuate nucleus neurons that project to the hypothalamic paraventricular nucleus: neuropeptidergic identity and consequences of adrenalectomy on mRNA levels in the rat. J Comp Neurol 358:518-530.
5. Baldino F Jr, Fitzpatrick-McElligott S, O'Kane TM, Gozes I. 1988. Hormonal regulation of somatostatin messenger RNA. Synapse 2:317-325.
6. Bandler R, Keay KA. 1996. Columnar organization in the midbrain periaqueductal gray and the integration of emotional expression. Prog Brain Res 107:285-300.
7. Bandler R, Keay KA, Floyd N, Price J. 2000. Central circuits mediating patterned autonomic activity during active vs. passive emotional coping. Brain Res Bull 53:95-104.
8. Bao AM, Fischer DF, Wu YH, Hol EM, Balesar R, Unmehopa UA, Zhou JN, Swaab DF. 2006. A direct androgenic involvement in the expression of human corticotropin-releasing hormone. Mol Psychiatry 11:567-576.
9. Bartke A, Steele RE, Musto N, Caldwell BV. 1973. Fluctuations in plasma testosterone levels in adult male rats and mice. Endocrinology 92: 1223-1228.
10. Berk ML, Finkelstein JA. 1981. Afferent projections to the preoptic area and hypothalamic regions in the rat brain. Neuroscience 6:1601-1624.
11. Bester H, Besson JM, Bernard JF. 1997. Organization of efferent projections from the parabrachial area to the hypothalamus: a Phaseolus vulgaris-leucoagglutinin study in the rat. J Comp Neurol 383:245-281.
12. Bingaman EW, Baeckman LM, Yracheta JM, Handa RJ, Gray TS. 1994. Localization of androgen receptor within peptidergic neurons of the rat forebrain. Brain Res Bull 35:379-382.
13. Bingham B, Lee P, Viau V. 2005. Adrenal adaptation to repeated restraint is met by an increased drive to the gonadal axis in the male rat. Soc Neurosci Abstr 31. 637.612.
14. Bingham B, Williamson M, Viau V. 2006. Androgen and estrogen receptor-beta distribution within spinal-projecting and neurosecretory neurons in the paraventricular nucleus of the male rat. J Comp Neurol 499: 911-923.
15. Bittencourt JC, Benoit R, Sawchenko PE. 1991. Distribution and origins of substance P-immunoreactive projections to the paraventricular and supraoptic nuclei: partial overlap with ascending catecholaminergic projections. J Chem Neuroanat 4:63-78.
16. Blanchard DC, Sakai RR, McEwen B, Weiss SM, Blanchard RJ. 1993. Subordination stress: behavioral, brain, and neuroendocrine correlates. Behav Brain Res 58:113-121.
17. Bloch GJ, Butler PC, Eckersell CB, Mills RH. 1998. Gonadal steroid-dependent GAL-IR cells within the medial preoptic nucleus (MPN) and the stimulatory effects of GAL within the MPN on sexual behaviors. Ann N Y Acad Sci 863:188-205.
18. Boudaba C, Szabo K, Tasker JG. 1996. Physiological mapping of local inhibitory inputs to the hypothalamic paraventricular nucleus. J Neurosci 16:7151-7160.
19. Bowers G, Cullinan WE, Herman JP. 1998. Region-specific regulation of glutamic acid decarboxylase (GAD) mRNA expression in central stress circuits. J Neurosci 18:5938-5947.
20. Brann DW. 1995. Glutamate: a major excitatory transmitter in neuroendocrine regulation. Neuroendocrinology 61:213-225.
21. Buller K, Xu Y, Dayas C, Day T. 2001. Dorsal and ventral medullary catecholamine cell groups contribute differentially to systemic interleukin-1beta-induced hypothalamic pituitary adrenal axis responses. Neuroendocrinology 73:129-138.
22. Cameron AA, Khan IA, Westlund KN, Cliffer KD, Willis WD. 1995. The efferent projections of the periaqueductal gray in the rat: a Phaseolus vulgaris-leucoagglutinin study. I. Ascending projections. J Comp Neurol 351:568-584.
23. Campeau S, Watson SJ Jr. 2000. Connections of some auditory-responsive posterior thalamic nuclei putatively involved in activation of the hypothalamo-pituitary-adrenocortical axis in response to audiogenic stress in rats: an anterograde and retrograde tract tracing study combined with Fos expression. J Comp Neurol 423:474-491.
24. Canteras NS, Swanson LW. 1992. Projections of the ventral subiculum to the amygdala, septum, and hypothalamus: a PHAL anterograde tract-tracing study in the rat. J Comp Neurol 324:180-194.
25. Canteras NS, Simerly RB, Swanson LW. 1992. Connections of the posterior nucleus of the amygdala. J Comp Neurol 324:143-179.
26. Canteras NS, Simerly RB, Swanson LW. 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.
27. Canteras NS, Simerly RB, Swanson LW. 1995. Organization of projections from the medial nucleus of the amygdala: a PHAL study in the rat. J Comp Neurol 360:213-245.
28. Card JP, Sved JC, Craig B, Raizada M, Vazquez J, Sved AF. 2006. Efferent projections of rat rostroventrolateral medulla C1 catecholamine neurons: Implications for the central control of cardiovascular regulation. J Comp Neurol 499:840-859.
29. Carstens E, Leah J, Lechner J, Zimmermann M. 1990. Demonstration of extensive brainstem projections to medial and lateral thalamus and hypothalamus in the rat. Neuroscience 35:609-626.
30. Ceccarelli I, Scaramuzzino A, Massafra C, Aloisi AM. 2003. The behavioral and neuronal effects induced by repetitive nociceptive stimulation are affected by gonadal hormones in male rats. Pain 104:35-47.
31. Ceccarelli I, Fiorenzani P, Massafra C, Aloisi AM. 2006. Repeated nociceptive stimulation induces different behavioral and neuronal responses in intact and gonadectomized female rats. Brain Res 1106:142-149.
32. Champagne D, Beaulieu J, Drolet G. 1998. CRFergic innervation of the paraventricular nucleus of the rat hypothalamus: a tract-tracing study. J Neuroendocrinol 10:119-131.
33. Chan RK, Sawchenko PE. 1994. Spatially and temporally differentiated patterns of c-fos expression in brainstem catecholaminergic cell groups induced by cardiovascular challenges in the rat. J Comp Neurol 348: 433-460.
34. Chang C, Saltzman A, Yeh S, Young W, Keller E, Lee HJ, Wang C, Mizokami A. 1995. Androgen receptor: an overview. Crit Rev Eukaryot Gene Expr 5:97-125.
35. Chen S, Wang J, Yu G, Liu W, Pearce D. 1997. Androgen and glucocorticoid receptor heterodimer formation. A possible mechanism for mutual inhibition of transcriptional activity. J Biol Chem 272:14087-14092.
36. Cheung S, Will YM, Hentschel K, Moore KE, Lookingland KJ. 1997. Role of gonadal steroids in determining sexual differences in expression of Fos-related antigens in tyrosine hydroxylase-immunoreactive neurons in subdivisions of the hypothalamic arcuate nucleus. Endocrinology 138:3804-3810.
37. Chibbar R, Toma JG, Mitchell BF, Miller FD. 1990. Regulation of neural oxytocin gene expression by gonadal steroids in pubertal rats. Mol Endocrinol 4:2030-2038.
38. Clancy AN, Bonsall RW, Michael RP. 1992. Immunohistochemical labeling of androgen receptors in the brain of rat and monkey. Life Sci 50:409-417.
39. Cole RL, Sawchenko PE. 2002. Neurotransmitter regulation of cellular activation and neuropeptide gene expression in the paraventricular nucleus of the hypothalamus. J Neurosci 22:959-969.
40. Coolen LM, Peters HJ, Veening JG. 1998. Anatomical interrelationships of the medial preoptic area and other brain regions activated following male sexual behavior: a combined fos and tract-tracing study. J Comp Neurol 397:421-435.
41. 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.
42. Cullinan WE, Herman JP, Battaglia DF, Akil H, Watson SJ. 1995. Pattern and time course of immediate early gene expression in rat brain following acute stress. Neuroscience 64:477-505.
43. Cullinan WE, Helmreich DL, Watson SJ. 1996. Fos expression in forebrain afferents to the hypothalamic paraventricular nucleus following swim stress. J Comp Neurol 368:88-99.
44. Cunningham ET Jr, Sawchenko PE. 1988. Anatomical specificity of noradrenergic inputs to the paraventricular and supraoptic nuclei of the rat hypothalamus. J Comp Neurol 274:60-76.
45. Cunningham ET Jr, Bohn MC, Sawchenko PE. 1990. Organization of adrenergic inputs to the paraventricular and supraoptic nuclei of the hypothalamus in the rat. J Comp Neurol 292:651-667.
46. Da Costa AP, Wood S, Ingram CD, Lightman SL. 1996. Region-specific reduction in stress-induced c-fos mRNA expression during pregnancy and lactation. Brain Res 742:177-184.
47. Dalkin AC, Gilrain JT, Marshall JC. 1994. Ovarian regulation of pituitary inhibin subunit and activin receptor type II gene expression: evidence for a nonsteroidal inhibitory substance. Endocrinology 135:944-949.
48. Dallman MF. 2003. Stress by any other name ...? Horm Behav 43:18-20.
49. Dallman MF, Viau V, Bhatnagar S, Gomez F, Laugero K, Bell ME. 2002. Corticotropin-releasing factor, corticosteroids, stress, and sugar: energy balance, the brain and behavior. In: Pfaff DW, Arnold AP, Etgen AM, Fahrbach SE, Rubin RT, editors. Hormones, brain, and behavior. New York: Academic Press. p 571-632.
50. Day TA. 2005. Defining stress as a prelude to mapping its neurocircuitry: no help from allostasis. Prog Neuropsychopharmacol Biol Psychiatry 29:1195-1200.
51. Dayas CV, Buller KM, Crane JW, Xu Y, Day TA. 2001a. Stressor categorization: acute physical and psychological stressors elicit distinctive recruitment patterns in the amygdala and in medullary noradrenergic cell groups. Eur J Neurosci 14:1143-1152.
52. Dayas CV, Buller KM, Day TA. 2001b. Medullary neurones regulate hypothalamic corticotropin-releasing factor cell responses to an emotional stressor. Neuroscience 105:707-719.
53. De Goeij DC, Dijkstra H, Tilders FJ. 1992. 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 131:847-853.
54. De Vries GJ, Miller MA. 1998. Anatomy and function of extrahypothalamic vasopressin systems in the brain. Prog Brain Res 119:3-20.
55. De Vries GJ, Duetz W, Buijs RM, van Heerikhuize J, Vreeburg JT. 1986. Effects of androgens and estrogens on the vasopressin and oxytocin innervation of the adult rat brain. Brain Res 399:296-302.
56. Diano S, Naftolin F, Horvath TL. 1997. Gonadal steroids target AMPA glutamate receptor-containing neurons in the rat hypothalamus, septurn and amygdala: a morphological and biochemical study. Endocrinology 138:778-789.
57. Dong HW, Swanson LW. 2004. Projections from bed nuclei of the stria terminalis, posterior division: implications for cerebral hemisphere regulation of defensive and reproductive behaviors. J Comp Neurol 471:396-433.
58. Dong HW, Swanson LW. 2006a. Projections from bed nuclei of the stria terminalis, magnocellular nucleus: implications for cerebral hemisphere regulation of micturition, defecation, and penile erection. J Comp Neurol 494:108-141.
59. Dong HW, Swanson LW. 2006b. Projections from bed nuclei of the stria terminalis, dorsomedial nucleus: implications for cerebral hemisphere integration of neuroendocrine, autonomic, and drinking responses. J Comp Neurol 494:75-107.
60. Dong HW, Swanson LW. 2006c. Projections from bed nuclei of the stria terminalis, anteromedial area: cerebral hemisphere integration of neuroendocrine, autonomic, and behavioral aspects of energy balance. J Comp Neurol 494:142-178.
61. Dong HW, Petrovich GD, Watts AG, Swanson LW. 2001. 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 436:430-455.
62. Engel J, Ahlenius S, Almgren O, Carlsson A, Larsson K, Sodersten P. 1979. Effects of gonadectomy and hormone replacement on brain monoamine synthesis in male rats. Pharmacol Biochem Behav 10:149-154.
63. Figueiredo HF, Dolgas CM, Herman JP. 2002. Stress activation of cortex and hippocampus is modulated by sex and stage of estrus. Endocrinology 143:2534-2540.
64. Floyd NS, Keay KA, Arias CM, Sawchenko PE, Bandler R. 1996. Projections from the ventrolateral periaqueductal gray to endocrine regulatory subdivisions of the paraventricular nucleus of the hypothalamus in the rat. Neurosci Lett 220:105-108.
65. Fodor M, Csaba Z, Kordon C, Epelbaum J. 1994. Growth hormone-releasing hormone, somatostatin, galanin and beta-endorphin afferents to the hypothalamic periventricular nucleus. J Chem Neuroanat 8:61-73.
66. Fulwiler CE, Saper CB. 1984. Subnuclear organization of the efferent connections of the parabrachial nucleus in the rat. Brain Res Rev 7:229-259.
67. Gandelman R. 1983. Gonadal hormones and sensory function. Neurosci Biobehav Rev 7:1-17.
68. Giesler GJ Jr, Katter JT, Dado RJ. 1994. Direct spinal pathways to the limbic system for nociceptive information. Trends Neurosci 17:244-250.
69. Gomez F, Dallman MF. 2001. Manipulation of androgens causes different energetic responses to cold in 60- and 40-day-old male rats. Am J Physiol Regul Integr Comp Physiol 280:R262-273.
70. Gomez F, Manalo S, Dallman MF. 2004. Androgen-sensitive changes in regulation of restraint-induced adrenocorticotropin secretion between early and late puberty in male rats. Endocrinology 145:59-70.
71. Goto M, Canteras NS, Burns G, Swanson LW. 2005. Projections from the subfornical region of the lateral hypothalamic area. J Comp Neurol 493:412-438.
72. Grattan DR, Selmanoff M. 1993. 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 60:2254-2264.
73. Grattan DR, Selmanoff M. 1994. Castration-induced decrease in the activity of medial preoptic and tuberoinfundibular GABAergic neurons is prevented by testosterone. Neuroendocrinology 60:141-149.
74. Grattan DR, Rocca MS, Sagrillo CA, McCarthy MM, Selmanoff M. 1996. Antiandrogen microimplants into the rostral medial preoptic area decrease gamma-aminobutyric acidergic neuronal activity and increase luteinizing hormone secretion in the intact male rat. Endocrinology 137:4167-4173.
75. Greco B, Edwards DA, Michael RP, Clancy AN. 1998a. 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.
76. Greco B, Edwards DA, Zumpe D, Michael RP, Clancy AN. 1998b. 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 33:125-138.
77. Greco B, Allegretto EA, Tetel MJ, Blaustein JD. 2001. Coexpression of ER beta with ER alpha and progestin receptor proteins in the female rat forebrain: effects of estradiol treatment. Endocrinology 142:5172-5181.
78. Groenewegen HJ, Van Dijk CA. 1984. Efferent connections of the dorsal tegmental region in the rat, studied by means of anterograde transport of the lectin Phaseolus vulgaris-leucoagglutinin (PHA-L). Brain Res 304:367-371.
79. Gu G, Cornea A, Simerly RB. 2003. Sexual differentiation of projections from the principal nucleus of the bed nuclei of the stria terminalis. J Comp Neurol 460:542-562.
80. Guillery RW. 2002. On counting and counting errors. J Comp Neurol 447:1-7.
81. Halvorson LM, Weiss J, Bauer-Dantoin AC, Jameson LJ. 1994. Dynamic regulation of pituitary follistatin, but not inhibin subunit, messenger ribonucleic acids during the rat estrous cycle. Endocrinology 134:1247-1253.
82. Hamson DK, Jones BA, Watson NV. 2004. Distribution of androgen receptor immunoreactivity in the brainstem of male rats. Neuroscience 127:797-803.
83. 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.
84. Heinlein CA, Chang C. 2002. The roles of androgen receptors and androgen-binding proteins in nongenomic androgen actions. Mol Endocrinol 16:2181-2187.
85. Henry JP. 1992. Biological basis of the stress response. Integr Physiol Behav Sci 27:66-83.
86. Herbison AE. 1997. Estrogen regulation of GABA transmission in rat preoptic area. Brain Res Bull 44:321-326.
87. Herbison AE. 2006. Physiology of the gonadotropin-releasing hormone neuronal network. In: Neill JD, editor. Knobil and Neill's physiology of reproduction, 3rd ed. Amsterdam: Elsevier. p 1415-1482.
88. Herman JP, Cullinan WE, Ziegler DR, Tasker JG. 2002a. Role of the paraventricular nucleus microenvironment in stress integration. Eur J Neurosci 16:381-385.
89. Herman JP, Tasker JG, Ziegler DR, Cullinan WE. 2002b. Local circuit regulation of paraventricular nucleus stress integration: glutamate-GABA connections. Pharmacol Biochem Behav 71:457-468.
90. Herman JP, Figueiredo H, Mueller NK, Ulrich-Lai Y, Ostrander MM, Choi DC, Cullinan WE. 2003. Central mechanisms of stress integration: hierarchical circuitry controlling hypothalamo-pituitary-adrenocortical responsiveness. Front Neuroendocrinol 24:151-180.
91. Herman JP, Mueller NK, Figueiredo H. 2004. Role of GABA and glutamate circuitry in hypothalamo-pituitary-adrenocortical stress integration. Ann N Y Acad Sci 1018:35-45.
92. Herman JP, Ostrander MM, Mueller NK, Figueiredo H. 2005. Limbic system mechanisms of stress regulation: hypothalamo-pituitary-adrenocortical axis. Prog Neuropsychopharmacol Biol Psychiatry 29: 1201-1213.
93. Hull EM, Du J, Lorrain DS, Matuszewich L. 1997. Testosterone, preoptic dopamine, and copulation in male rats. Brain Res Bull 44:327-333.
94. Hurley KM, Herbert H, Moga MM, Saper CB. 1991. Efferent projections of the infralimbic cortex of the rat. J Comp Neurol 308:249-276.
95. Isgor C, Cecchi M, Kabbaj M, Akil H, Watson SJ. 2003. Estrogen receptor beta in the paraventricular nucleus of hypothalamus regulates the neuroendocrine response to stress and is regulated by corticosterone. Neuroscience 121:837-845.
96. Jhamandas JH, Harris KH, Petrov T, Krukoff TL. 1992. Characterization of the parabrachial nucleus input to the hypothalamic paraventricular nucleus in the rat. J Neuroendocrinol 4:461-471.
97. Ju G, Swanson LW. 1989. Studies on the cellular architecture of the bed nuclei of the stria terminalis in the rat. I. Cytoarchitecture. J Comp Neurol 280:587-602.
98. Kalra SP, Kalra PS. 1983. Neural regulation of luteinizing hormone secretion in the rat. Endocr Rev 4:311-351.
99. Kalsbeek A, Palm IF, Buijs RM. 2002. Central vasopressin systems and steroid hormones. Prog Brain Res 139:57-73.
100. Kerr JE, Allore RJ, Beck SG, Handa RJ. 1995. Distribution and hormonal regulation of androgen receptor (AR) and AR messenger ribonucleic acid in the rat hippocampus. Endocrinology 136:3213-3221.
101. Kerr JE, Beck SG, Handa RJ. 1996. Androgens selectively modulate C-fos messenger RNA induction in the rat hippocampus following novelty. Neuroscience 74:757-766.
102. Koolhaas JM, Everts H, de Ruiter AJ, de Boer SF, Bohus B. 1998. Coping with stress in rats and mice: differential peptidergic modulation of the amygdala-lateral septum complex. Prog Brain Res 119:437-448.
103. Kritzer MF. 1997. Selective colocalization of immunoreactivity for intracellular gonadal hormone receptors and tyrosine hydroxylase in the ventral tegmental area, substantia nigra, and retrorubral fields in the rat. J Comp Neurol 379:247-260.
104. Kritzer MF. 2003. Long-term gonadectomy affects the density of tyrosine hydroxylase- but not dopamine-beta-hydroxylase-, choline acetyltransferase- or serotonin-immunoreactive axons in the medial prefrontal cortices of adult male rats. Cereb Cortex 13:282-296.
105. Kritzer MF. 2004. The distribution of immunoreactivity for intracellular androgen receptors in the cerebral cortex of hormonally intact adult male and female rats: localization in pyramidal neurons making corticocortical connections. Cereb Cortex 14:268-280.
106. Krukoff TL, Harris KH, Jhamandas JH. 1993. Efferent projections from the parabrachial nucleus demonstrated with the anterograde tracer Phaseolus vulgaris leucoagglutinin. Brain Res Bull 30:163-172.
107. Laflamme N, Nappi RE, Drolet G, Labrie C, Rivest S. 1998. Expression and neuropeptidergic characterization of estrogen receptors (ERalpha and ERbeta) throughout the rat brain: anatomical evidence of distinct roles of each subtype. J Neurobiol 36:357-378.
108. Larsen PJ, Mikkelsen JD. 1995. Functional identification of central afferent projections conveying information of acute "stress" to the hypothalamic paraventricular nucleus. J Neurosci 15:2609-2627.
109. Larsen PJ, Hay-Schmidt A, Mikkelsen JD. 1994. Efferent connections from the lateral hypothalamic region and the lateral preoptic area to the hypothalamic paraventricular nucleus of the rat. J Comp Neurol 342: 299-319.
110. Larsen PJ, Hay-Schmidt A, Vrang N, Mikkelsen JD. 1996. Origin of projections from the midbrain raphe nuclei to the hypothalamic paraventricular nucleus in the rat: a combined retrograde and anterograde tracing study. Neuroscience 70:963-988.
111. LeDoux JE, Ruggiero DA, Reis DJ. 1985. Projections to the subcortical forebrain from anatomically defined regions of the medial geniculate body in the rat. J Comp Neurol 242:182-213.
112. Legradi G, Lechan RM. 1998. The arcuate nucleus is the major source for neuropeptide Y-innervation of thyrotropin-releasing hormone neurons in the hypothalamic paraventricular nucleus. Endocrinology 139:3262-3270.
113. Levin MC, Sawchenko PE, Howe PR, Bloom SR, Polak JM. 1987. Organization of galanin-immunoreactive inputs to the paraventricular nucleus with special reference to their relationship to catecholaminergic afferents. J Comp Neurol 261:562-582.
114. Levine JE, Bauer-Dantoin AC, Besecke LM, Conaghan LA, Legan SJ, Meredith JM, Strobl FJ, Urban JH, Vogelsong KM, Wolfe AM. 1991. Neuroendocrine regulation of the luteinizing hormone-releasing hormone pulse generator in the rat. Prog Horm Res 47:97-151.
115. Li HY, Sawchenko PE. 1998. Hypothalamic effector neurons and extended circuitries activated in "neurogenic" stress: a comparison of footshock effects exerted acutely, chronically, and in animals with controlled glucocorticoid levels. J Comp Neurol 393:244-266.
116. Liao YJ, Jan YN, Jan JY. 1996. Heteromultimerization of G-protein-gated inwardly rectifying K+ channel proteins GIRK1 and GIRK2 and their altered expression in weaver brain. J Neurosci 16:7137-150.
117. Lind RW. 1986. Bi-directional, chemically specified neural connections between the subfornical organ and the midbrain raphe system. Brain Res 384:250-261.
118. Lisciotto CA, Morrell JI. 1994. Sex differences in the distribution and projections of testosterone target neurons in the medial preoptic area and the bed nucleus of the stria terminalis of rats. Horm Behav 28: 492-502.
119. Lund TD, Munson DJ, Haldy ME, Handa RJ. 2004. Dihydrotestosterone may inhibit hypothalamo-pituitary-adrenal activity by acting through estrogen receptor in the male mouse. Neurosci Lett 365:43-47.
120. Lund TD, Hinds LR, Handa RJ. 2006. The androgen 5alpha- dihydrotestosterone and its metabolite 5alpha-androstan-3beta, 17beta-diol inhibit the hypothalamo-pituitary-adrenal response to stress by acting through estrogen receptor beta-expressing neurons in the hypothalamus. J Neurosci 26:1448-1456.
121. Makara GB, Kiss A, Lolait SJ, Aguilera G. 1996. Hypothalamic-pituitary corticotroph function after shunting of magnocellular vasopressin and oxytocin to the hypophyseal portal circulation. Endocrinology 137:580-586.
122. McEwen BS, Wingfield JC. 2003. The concept of allostasis in biology and biomedicine. Horm Behav 43:2-15.
123. McGinnis MY, Williams GW, Lumia AR. 1996. Inhibition of male sex behavior by androgen receptor blockade in preoptic area or hypothalamus, but not amygdala or septum. Physiol Behav 60:783-789.
124. McKellar S, Loewy AD. 1981. Organization of some brain stem afferents to the paraventricular nucleus of the hypothalamus in the rat. Brain Res 217:351-357.
125. Moga MM, Saper CB. 1994. Neuropeptide-immunoreactive neurons projecting to the paraventricular hypothalamic nucleus in the rat. J Comp Neurol 346:137-150.
126. Mulders WH, Meek J, Hafmans TG, Cools AR. 1997. Plasticity in the stress-regulating circuit: decreased input from the bed nucleus of the stria terminalis to the hypothalamic paraventricular nucleus in Wistar rats following adrenalectomy. Eur J Neurosci 9:2462-2471.
127. Murphy AZ, Hoffman GE. 2001. Distribution of gonadal steroid receptor-containing neurons in the preoptic-periaqueductal gray-brainstem pathway: a potential circuit for the initiation of male sexual behavior. J Comp Neurol 438:191-212.
128. Nappi RE, Bonneau MJ, Rivest S. 1997. Influence of the estrous cycle on c-fos and CRH gene transcription in the brain of endotoxin-challenged female rats. Neuroendocrinology 65:29-46.
129. Ono T, Luiten PG, Nishijo H, Fukuda M, Nishino H. 1985. Topographic organization of projections from the amygdala to the hypothalamus of the rat. Neurosci Res 2:221-238.
130. Pacak K, Palkovits M. 2001. Stressor specificity of central neuroendocrine responses: implications for stress-related disorders. Endocr Rev 22: 502-548.
131. Palkovits M, Baffi JS, Pacak K. 1997. Stress-induced Fos-like immunoreactivity in the pons and the medulla oblongata of rats. Stress 1:155-168.
132. Pan B, Castro-Lopes JM, Coimbra A. 1999. Central afferent pathways conveying nociceptive input to the hypothalamic paraventricular nucleus as revealed by a combination of retrograde labeling and c-fos activation. J Comp Neurol 413:129-145.
133. Patchev VK, Almeida OF. 1998. Gender specificity in the neural regulation of the response to stress: new leads from classical paradigms. Mol Neurobiol 16:63-77.
134. Petrov T, Krukoff TL, Jhamandas JH. 1992. The hypothalamic paraventricular and lateral parabrachial nuclei receive collaterals from raphe nucleus neurons: a combined double retrograde and immunocytochemical study. J Comp Neurol 318:18-26.
135. Pfaff D, Keiner M. 1973. Atlas of estradiol-concentrating cells in the central nervous system of the female rat. J Comp Neurol 151:121-158.
136. Plotsky PM, Sutton SW, Bruhn TO, Ferguson AV. 1988. Analysis of the role of angiotensin II in mediation of adrenocorticotropin secretion. Endocrinology 122:538-545.
137. Poggioli R, Vergoni AV, Santi R, Carani C, Baraghini GF, Zini D, Marrama P, Bertolini A. 1984. Sexual behavior of male rats: influence of short-and long-term adrenalectomy. Horm Behav 18:79-85.
138. Polston EK, Simerly RB. 2003. Sex-specific patterns of galanin, cholecystokinin, and substance P expression in neurons of the principal bed nucleus of the stria terminalis are differentially reflected within three efferent preoptic pathways in the juvenile rat. J Comp Neurol 465:551-559.
139. Prewitt CM, Herman JP. 1998. Anatomical interactions between the central amygdaloid nucleus and the hypothalamic paraventricular nucleus of the rat: a dual tract-tracing analysis. J Chem Neuroanat 15:173-185.
140. Price JL. 1995. Thalamus. In: Paxinos G, editor. The rat nervous system, 2nd ed. New York: Academic Press. p 629-648.
141. Prins GS, Birch L, Greene GL. 1991. Androgen receptor localization in different cell types of the adult rat prostate. Endocrinology 129:3187-3199.
142. Rachman IM, Unnerstall JR, Pfaff DW, Cohen RS. 1998. Estrogen alters behavior and forebrain c-fos expression in ovariectomized rats subjected to the forced swim test. Proc Natl Acad Sci U S A 95:13941-13946.
143. Radley JJ, Arias CM, Sawchenko PE. 2006. Regional differentiation of the medial prefrontal cortex in regulating adaptive responses to acute emotional stress. J Neurosci 26:12967-12976.
144. Rho JH, Swanson LW. 1989. A morphometric analysis of functionally defined subpopulations of neurons in the paraventricular nucleus of the rat with observations on the effects of colchicine. J Neurosci 9:1375-1388.
145. Rhodes ME, Rubin RT. 1999. Functional sex differences ('sexual diergism') of central nervous system cholinergic systems, vasopressin, and hypothalamic-pituitary-adrenal axis activity in mammals: a selective review. Brain Res Brain Res Rev 30:135-152.
146. Rhodes CH, Morrell JI, Pfaff DW. 1982. Estrogen-concentrating neurophysin-containing hypothalamic magnocellular neurons in the vasopressin-deficient (Brattleboro) rat: a study combining steroid autoradiography and immunocytochemistry. J Neurosci 2:1718-1724.
147. Rinaman L, Hoffman GE, Dohanics J, Le WW, Strieker EM, Verbalis JG. 1995. Cholecystokinin activates catecholaminergic neurons in the caudal medulla that innervate the paraventricular nucleus of the hypothalamus in rats. J Comp Neurol 360:246-256.
148. Risold PY, Swanson LW. 1997. Connections of the rat lateral septal complex. Brain Res Brain Res Rev 24:115-195.
149. Risold PY, Canteras NS, Swanson LW. 1994. Organization of projections from the anterior hypothalamic nucleus: a Phaseolus vulgaris-leucoagglutinin study in the rat. J Comp Neurol 348:1-40.
150. Risold PY, Thompson RH, Swanson LW. 1997. The structural organization of connections between hypothalamus and cerebral cortex. Brain Res Brain Res Rev 24:197-254.
151. Rivier C, Rivest S. 1991. Effect of stress on the activity of the hypothalamic-pituitary-gonadal axis: peripheral and central mechanisms. Biol Reprod 45:523-532.
152. Rivier C, Rivier J, Vale W. 1986. Stress-induced inhibition of reproductive functions: role of endogenous corticotropin-releasing factor. Science 231:607-609.
153. Roberts V, Meunier H, Vaughan J, Rivier J, Rivier C, Vale W, Sawchenko P. 1989. Production and regulation of inhibin subunits in pituitary gonadotropes. Endocrinology 124:552-554.
154. 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.
155. Romeo RD, Diedrich SL, Sisk CL. 2000. Effects of gonadal steroids during pubertal development on androgen and estrogen receptor-alpha immunoreactivity in the hypothalamus and amygdala. J Neurobiol 44:361-368.
156. Romeo RD, Lee SJ, Chhua N, McPherson CR, McEwen BS. 2004. Testosterone cannot activate an adult-like stress response in prepubertal male rats. Neuroendocrinology 79:125-132.
157. Romero LM, Levine S, Sapolsky RM. 1995. Patterns of adrenocorticotropin secretagog release in response to social interactions and various degrees of novelty. Psychoneuroendocrinology 20:183-191.
158. Ronnekleiv OK, Kelly MJ. 2005. Diversity of ovarian steroid signaling in the hypothalamus. Front Neuroendocrinol 26:65-84.
159. Roselli CE, Resko JA. 1993. Aromatase activity in the rat brain: hormonal regulation and sex differences. J Steroid Biochem Mol Biol 44:499-508.
160. Rubinow DR, Schmidt PJ. 1996. Androgens, brain, and behavior. Am J Psychiatry 153:974-984.
161. Ruggiero DA, Giuliano R, Anwar M, Stornetta R, Reis DJ. 1990. Anatomical substrates of cholinergic-autonomic regulation in the rat. J Comp Neurol 292:1-53.
162. Rye DB, Saper CB, Lee HJ, Wainer BH. 1987. Pedunculopontine tegmental nucleus of the rat: cytoarchitecture, cytochemistry, and some extrapyramidal connections of the mesopontine tegmentum. J Comp Neurol 259:483-528.
163. Saper CB, Loewy AD. 1980. Efferent connections of the parabrachial nucleus in the rat. Brain Res 197:291-317.
164. Saper CB, Swanson LW, Cowan WM. 1976. The efferent connections of the ventromedial nucleus of the hypothalamus of the rat. J Comp Neurol 169:409-442.
165. Saper CB, Swanson LW, Cowan WM. 1979. An autoradiographic study of the efferent connections of the lateral hypothalamic area in the rat. J Comp Neurol 183:689-706.
166. Sar M, Stumpf WE. 1975. Distribution of androgen-concentrating neurons in the rat brain. In: Stumpf WE, Grant LD, editors. Anatomical endocrinology. New York: Karger. p 120-133.
167. Sawchenko PE, Swanson LW. 1982. The organization of noradrenergic pathways from the brainstem to the paraventricular and supraoptic nuclei in the rat. Brain Res Rev 4:275-325.
168. Sawchenko PE, Swanson LW. 1983. The organization of forebrain afferents to the paraventricular and supraoptic nuclei of the rat. J Comp Neurol 218:121-144.
169. Sawchenko PE, Swanson LW, Joseph SA. 1982. The distribution and cells of origin of ACTH(1-39)-stained varicosities in the paraventricular and supraoptic nuclei. Brain Res 232:365-374.
170. Sawchenko PE, Swanson LW, Steinbusch HW, Verhofstad AA. 1983. The distribution and cells of origin of serotonergic inputs to the paraventricular and supraoptic nuclei of the rat. Brain Res 277:355-360.
171. Sawchenko PE, Swanson LW, Grzanna R, Howe PR, Bloom SR, Polak JM. 1985. Colocalization of neuropeptide Y immunoreactivity in brainstem catecholaminergic neurons that project to the paraventricular nucleus of the hypothalamus. J Comp Neurol 241:138-153.
172. Sawchenko PE, Benoit R, Brown MR. 1988. Somatostatin 28-immunoreactive inputs to the paraventricular and supraoptic nuclei: principal origin from non-aminergic neurons in the nucleus of the solitary tract. J Chem Neuroanat 1:81-94.
173. Sawchenko PE, Arias C, Bittencourt JC. 1990. Inhibin beta, somatostatin, and enkephalin immunoreactivities coexist in caudal medullary neurons that project to the paraventricular nucleus of the hypothalamus. J Comp Neurol 291:269-280.
174. Sawchenko PE, Li HY, Ericsson A. 2000. Circuits and mechanisms governing hypothalamic responses to stress: a tale of two paradigms. Prog Brain Res 122:61-78.
175. Schmued LC, Fallon JH. 1986. Fluoro-Gold: a new fluorescent retrograde axonal tracer with numerous unique properties. Brain Res 377:147-154.
176. Seeman TE, Singer B, Wilkinson CW, McEwen B. 2001. Gender differences in age-related changes in HPA axis reactivity. Psychoneuroendocrinology 26:225-240.
177. Selvage DJ, Rivier C. 2003. Importance of the paraventricular nucleus of the hypothalamus as a component of a neural pathway between the brain and the testes that modulates testosterone secretion independently of the pituitary. Endocrinology 144:594-598.
178. Selvage DJ, Lee SY, Parsons LH, Seo DO, Rivier CL. 2004. A hypothalamic-testicular neural pathway is influenced by brain catecholamines, but not testicular blood flow. Endocrinology 145:1750-1759.
179. Sencar-Cupovic I, Milkovic S. 1976. 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 5:1-9.
180. Sesack SR, Deutch AY, Roth RH, Bunney BS. 1989. Topographical organization of the efferent projections of the medial prefrontal cortex in the rat: an anterograde tract-tracing study with Phaseolus vulgaris leucoagglutinin. J Comp Neurol 290:213-242.
181. Shughrue PJ, Lane MV, Merchenthaler I. 1997. Comparative distribution of estrogen receptor-alpha and -beta mRNA in the rat central nervous system. J Comp Neurol 388:507-525.
182. Silverman AJ, Hoffman DL, Zimmerman EA. 1981. The descending afferent connections of the paraventricular nucleus of the hypothalamus (PVN). Brain Res Bull 6:47-61.
183. Simerly RB. 1989. Hormonal control of the development and regulation of tyrosine hydroxylase expression within a sexually dimorphic population of dopaminergic cells in the hypothalamus. Brain Res Mol Brain Res 6:297-310.
184. Simerly RB. 1993. Distribution and regulation of steroid hormone receptor gene expression in the central nervous system. In: Seil FJ, editor. Advances in neurology. New York: Raven Press. p 207-225.
185. Simerly RB. 2002. Wired for reproduction: organization and development of sexually dimorphic circuits in the mammalian forebrain. Annu Rev Neurosci 25:507-536.
186. Simerly RB, Swanson LW. 1986. The organization of neural inputs to the medial preoptic nucleus of the rat. J Comp Neurol 246:312-342.
187. 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.
188. Simerly RB, Gorski RA, Swanson LW. 1986. Neurotransmitter specificity of cells and fibers in the medial preoptic nucleus: an immunohistochemical study in the rat. J Comp Neurol 246:343-363.
189. Simerly 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.
190. Spencer SJ, Buller KM, Day TA. 2005. Medial prefrontal cortex control of the paraventricular hypothalamic nucleus response to psychological stress: possible role of the bed nucleus of the stria terminalis. J Comp Neurol 481:363-376.
191. Stern JE, Zhang W. 2003. Preautonomic neurons in the paraventricular nucleus of the hypothalamus contain estrogen receptor beta. Brain Res 975:99-109.
192. Stumpf WE. 1970. Estrogen-neurons and estrogen-neuron systems in the periventricular brain. Am J Anat 129:207-217.
193. Stumpf WE, Sar M, Keefer DA. 1975. Atlas of estrogen target cells in the rat brain. In: Stumpf WE, Grant LD, editors. Anatomical endocrinology. New York: Karger. p 104-119.
194. Swanson LW. 1976. An autoradiographic study of the efferent connections of the preoptic region in the rat. J Comp Neurol 167:227-256.
195. Swanson LW. 1982. The projections of the ventral tegmental area and adjacent regions: a combined fluorescent retrograde tracer and immunofluorescence study in the rat. Brain Res Bull 9:321-353.
196. Swanson LW. 1987. The hypothalamus. In: Björklund A, Hökfelt T, Swanson LW, editors. Integrated systems of the CNS. Part I. Hypothalamus, amygdala, hippocampus and retina. Amsterdam: Elsevier. p 1-124.
197. Swanson LW. 1998. Brain maps: structure of the rat brain, 2nd ed. Amsterdam: Elsevier.
198. Swanson LW, Sawchenko PE. 1983. Hypothalamic integration: organization of the paraventricular and supraoptic nuclei. Annu Rev Neurosci 6:269-324.
199. Swanson LW, Sawchenko PE, Berod A, Hartman BK, Helle KB, Vanorden DE. 1981. An immunohistochemical study of the organization of catecholaminergic cells and terminal fields in the paraventricular and supraoptic nuclei of the hypothalamus. J Comp Neurol 196:271-285.
200. Swanson LW, Sawchenko PE, Lind RW, Rho JH. 1987. The CRH motoneuron: differential peptide regulation in neurons with possible synaptic, paracrine, and endocrine outputs. Ann N Y Acad Sci 512:12-23.
201. Tamashiro KL, Nguyen MM, Fujikawa T, Xu T, Yun Ma L, Woods SC, Sakai RR. 2004. Metabolic and endocrine consequences of social stress in a visible burrow system. Physiol Behav 80:683-693.
202. Ter Horst GJ, Luiten PG. 1986. The projections of the dorsomedial hypothalamic nucleus in the rat. Brain Res Bull 16:231-248.
203. Ter Horst GJ, Luiten PG. 1987. Phaseolus vulgaris leuco-agglutinin tracing of intrahypothalamic connections of the lateral, ventromedial, dorsomedial and paraventricular hypothalamic nuclei in the rat. Brain Res Bull 18:191-203.
204. Ter Horst GJ, Groenewegen HJ, Karst H, Luiten PG. 1984. Phaseolus vulgaris leuco-agglutinin immunohistochemistry. A comparison between autoradiographic and lectin tracing of neuronal efferents. Brain Res 307:379-383.
205. Thellier D, Moos F, Richard P, Stoeckel ME. 1994. Evidence for connections between a discrete hypothalamic dorsochiasmatic area and the supraoptic and paraventricular nuclei. Brain Res Bull 34:261-274.
206. Thompson RH, Swanson LW. 1998. Organization of inputs to the dorsomedial nucleus of the hypothalamus: a reexamination with FluoroGold and PHAL in the rat. Brain Res Brain Res Rev 27:89-118.
207. Thompson RH, Swanson LW. 2003. Structural characterization of a hypothalamic visceromotor pattern generator network. Brain Res Brain Res Rev 41:153-202.
208. Thompson RH, Canteras NS, Swanson LW. 1996. Organization of projections from the dorsomedial nucleus of the hypothalamus: a PHA-L study in the rat. J Comp Neurol 376:143-173.
209. Tillet Y, Batailler M, Thiery JC, Thibault J. 2000. Neuronal projections to the lateral retrochiasmatic area of sheep with special reference to catecholaminergic afferents: immunohistochemical and retrograde tract-tracing studies. J Chem Neuroanat 19:47-67.
210. Toufexis DJ, Myers KM, Davis M. 2006. The effect of gonadal hormones and gender on anxiety and emotional learning. Horm Behav 50:539-549.
211. Tribollet E, Dreifuss JJ. 1981. Localization of neurones projecting to the hypothalamic paraventricular nucleus area of the rat: a horseradish peroxidase study. Neuroscience 6:1315-1328.
212. Tribollet E, Raufaste D, Maffrand J, Serradeil-Le Gal C. 1999. Binding of the non-peptide vasopressin V1a receptor antagonist SR-49059 in the rat brain: an in vitro and in vivo autoradiographic study. Neuroendocrinology 69:113-120.
213. Ulrich-Lai YM, Arnhold MM, Engeland WC. 2006. Adrenal splanchnic innervation contributes to the diurnal rhythm of plasma corticosterone in rats by modulating adrenal sensitivity to ACTH. Am J Physiol Regul Integr Comp Physiol 290:R1128-1135.
214. Van den Berghe G. 2002. Dynamic neuroendocrine responses to critical illness. Front Neuroendocrinol 23:370-391.
215. Van den Pol AN, Wuarin JP, Dudek FE. 1990. Glutamate, the dominant excitatory transmitter in neuroendocrine regulation. Science 250: 1276-1278.
216. Verbalis JG, Rinamin L, Hoffman GH, Strieker EM. 1995. Functional neural connections between the hypothalamus and the dorsal vagal complex. In: Singer MV and Ziegler R, editors. Gastrointestinal tract and endocrine system. Dordrecht: Kluwer Academic. p 3-16.
217. Viau V. 2002. Functional cross-talk between the hypothalamic-pituitary- gonadal and -adrenal axes. J Neuroendocrinol 14:506-513.
218. Viau V, Meaney MJ. 1991. Variations in the hypothalamic-pituitary-adrenal response to stress during the estrous cycle in the rat. Endocrinology 129:2503-2511.
219. Viau V, Meaney MJ. 1996. The inhibitory effect of testosterone on hypothalamic-pituitary-adrenal responses to stress is mediated by the medial preoptic area. J Neurosci 16:1866-1876.
220. Viau V, Chu A, Soriano L, Dallman MF. 1999. 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 19:6684-6693.
221. Viau V, Soriano L, Dallman MF. 2001. Androgens alter corticotropin releasing hormone and arginine vasopressin mRNA within forebrain sites known to regulate activity in the hypothalamic-pituitary-adrenal axis. J Neuroendocrinol 13:442-452.
222. Viau V, Lee P, Sampson J, Wu J. 2003. A testicular influence on restraint-induced activation of medial parvocellular neurons in the paraventricular nucleus in the male rat. Endocrinology 144:3067-3075.
223. Viau V, Bingham B, Davis J, Lee P, Wong M. 2005. 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 146:137-146.
224. Vreeburg JT, de Greef WJ, Ooms MP, van Wouw P, Weber RF. 1984. Effects of adrenocorticotropin and corticosterone on the negative feedback action of testosterone in the adult male rat. Endocrinology 115: 977-983.
225. Wagner CK, Morrell JI. 1997. Neuroanatomical distribution of aromatase mRNA in the rat brain: indications of regional regulation. J Steroid Biochem Mol Biol 61:307-314.
226. Watts AG, Swanson LW. 1987. Efferent projections of the suprachiasmatic nucleus. II. Studies using retrograde transport of fluorescent dyes and simultaneous peptide immunohistochemistry in the rat. J Comp Neurol 258:230-252.
227. Watts AG, Swanson LW, Sanchez-Watts G. 1987. Efferent projections of the suprachiasmatic nucleus. I. Studies using anterograde transport of Phaseolus vulgaris leucoagglutinin in the rat. J Comp Neurol 258:204-229.
228. Weiss ML, Hatton GI. 1990. Collateral input to the paraventricular and supraoptic nuclei in rat. I. Afferents from the subfornical organ and the anteroventral third ventricle region. Brain Res Bull 24:231-238.
229. Wiegand SJ, Terasawa E. 1982. Discrete lesions reveal functional heterogeneity of suprachiasmatic structures in regulation of gonadotropin secretion in the female rat. Neuroendocrinology 34:395-404.
230. Williamson M, Viau V. 2006. Lesions of the medial preoptic nucleus alter the hypothalamic-pituitary-adrenal (HPA) axis response to plasma testosterone. Soc Neurosci Abstr 32. 563.567.
231. Williamson M, Bingham B, Viau V. 2004. Immunohistochemical detection of androgen receptor-expressing neurons that project to the paraventricular nucleus of the hypothalamus. Soc Neurosci Abstr 30. 425.412.
232. Williamson M, Bingham B, Viau V. 2005. 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. Prog Neuropsychopharmacol Biol Psychiatry 29:1239-1248.
233. Wingfield JC, Sapolsky RM. 2003. Reproduction and resistance to stress: when and how. J Neuroendocrinol 15:711-724.
234. Wotjak CT, Kubota M, Liebsch G, Montkowski A, Holsboer F, Neumann I, Landgraf R. 1996. Release of vasopressin within the rat paraventricular nucleus in response to emotional stress: a novel mechanism of regulating adrenocorticotropic hormone secretion? J Neurosci 16:7725-7732.
235. Wyss JM, Swanson LW, Cowan WM. 1979. A study of subcortical afferents to the hippocampal formation in the rat. Neuroscience 4:463-476.
236. Yokosuka M, Hayashi S. 1996. Colocalization of neuronal nitric oxide synthase and androgen receptor immunoreactivity in the premammillary nucleus in rats. Neurosci Res 26:309-314.
237. Young EA. 1998. Sex differences and the HPA axis: implications for psychiatric disease. J Gend Specif Med 1:21-27.
238. Young EA, Altemus M. 2004. Puberty, ovarian steroids, and stress. Ann N Y Acad Sci 1021:124-133.
239. Zhao C, Fujinaga R, Tanaka M, Yanai A, Nakahama K, Shinoda K. 2007. Region-specific expression and sex-steroidal regulation on aromatase and its mRNA in the male rat brain: immunohistochemical and in situ hybridization analyses. J Comp Neurol 500:557-573.
240. 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.