Synaptic regulation of the hypothalamic-pituitary-adrenal axis and its modulation by glucocorticoids and stress

Frontiers in Cellular Neuroscience

Volumn , Issue MAY 2012, 2012, Pages

  Levy, Benjamin H ^a   Tasker, Jeffrey G ^a,b  

^a TULANE UNIVERSITY   (United States)

^b Tulane University   (United States)

Author keywords

Corticosteroid; Depression; GABA; Glutamate; Neural circuits; Norepinephrine; Paraventricular nucleus; Synaptic plasticity

Indexed keywords

4 AMINOBUTYRIC ACID; CORTICOTROPIN RELEASING FACTOR; GLUCOCORTICOID; GLUTAMIC ACID; NORADRENALIN;

ACTION POTENTIAL; DOWN REGULATION; ENZYME ACTIVITY; ENZYME REGULATION; GABAERGIC TRANSMISSION; GENE EXPRESSION PROFILING; HIPPOCAMPUS; HUMAN; HYPOTHALAMIC PARAVENTRICULAR NUCLEUS; HYPOTHALAMUS HYPOPHYSIS ADRENAL SYSTEM; IMMUNOREACTIVITY; MEMBRANE DEPOLARIZATION; MORPHOLOGY; NERVE CELL PLASTICITY; NEUROMODULATION; NEUROSECRETORY CELL; NEUROTRANSMISSION; NONHUMAN; NORADRENERGIC SYSTEM; PREFRONTAL CORTEX; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; REVIEW; SEX DIFFERENCE; SOLITARY TRACT NUCLEUS; STRESS; STRIA TERMINALIS; SYNAPSE; SYNAPTIC REGULATION; SYNAPTIC TRANSMISSION; TOPOGRAPHY;

EID: 84864020078     PISSN: 16625102     EISSN: None     Source Type: Journal    
DOI: 10.3389/fncel.2012.00024     Document Type: Review

References (132)

1. Abelson, J. L., Khan, S., Liberzon, I., and Young, E. A. (2007). HPA axis activity in patients with panic disorder: review and synthesis of four studies. Depress. Anxiety 24, 66-76.
2. Ahrens, T., Deuschle, M., Krumm, B., Van Der Pompe, G., Den Boer, J. A., and Lederbogen, F. (2008). Pituitary-adrenal and sympathetic nervous system responses to stress in women remitted from recurrent major depression. Psychosom. Med. 70, 461-467.
3. Alon, T., Zhou, L., Perez, C. A., Garfield, A. S., Friedman, J. M., and Heisler, L. K. (2009). Transgenic mice expressing green fluorescent protein under the control of the corticotropin-releasing hormone promoter. Endocrinology 150, 5626-5632.
4. Aubry, J. M., Bartanusz, V., Pagliusi, S., Schulz, P., and Kiss, J. Z. (1996). Expression of ionotropic glutamate receptor subunit mRNAs byparaven-tricular corticotropin-releasing factor (CRF) neurons. Neurosci. Lett. 205, 95-98.
5. Bali, B., and Kovacs, K. J. (2003). GABAergic control of neuropeptide gene expression in parvocellular neurons of the hypothalamic paraventricular nucleus. Eur. J. Neurosci. 18, 1518-1526.
6. Bartanusz, V., Aubry, J. M., Pagliusi, S., Jezova, D., Baffi, J., and Kiss, J. Z. (1995). Stress-induced changes in messenger RNA levels of N-methyl-D-aspartate and AMPA receptor subunits in selected regions of the rat hippocampus and hypothalamus. Neuroscience 66, 247-252.
7. Boudaba, C., Schrader, L. A., and Tasker, J. G. (1997). Physiological evidence for local excitatorysynaptic circuits in the rat hypothalamus. J. Neurophysiol. 77, 3396-3400.
8. Boudaba, C., Szabo, K., and Tasker, J. G. (1996). Physiological mapping of local inhibitory inputs to the hypothalamic paraventricular nucleus. J. Neurosci. 16, 7151-7160.
9. Boyle, M. P., Brewer, J. A., Funatsu, M., Wozniak, D. F., Tsien, J. Z., Izumi, Y., and Muglia, L. J. (2005). Acquired deficit of forebrain glucocorticoid receptor produces depression-like changes in adrenal axis regulation and behavior. Proc. Natl. Acad. Sci. U.S.A. 102, 473-478.
10. Bradbury, M. J., Giracello, D. R., Chapman, D. F., Holtz, G., Schaffhauser, H., Rao, S. P., Varney, M. A., and Anderson, J. J. (2003). Metabotropic glutamate receptor 5 antagonist-induced stimulation of hypothalamic-pituitary-adrenal axis activity: interaction with serotonergic systems. Neuropharmacology 44, 562-572.
11. Brawman-Mintzer, O., Monnier, J., Wolitzky, K. B., and Falsetti, S. A. (2005). Patients with generalized anxiety disorder and a history of trauma: somatic symptom endorsement. J. Psychiatr. Pract. 11, 212-215.
12. Calogero, A. E., Gallucci, W. T., Chrousos, G. P., and Gold, P. W. (1988). Catecholamine effects upon rat hypothalamic corticotropin-releasing hormone secretion in vitro. J. Clin. Invest. 82, 839-846.
13. Choi, D. C., Furay, A. R., Evanson, N. K., Ostrander, M. M., Ulrich-Lai, Y. M., and Herman, J. P. (2007). Bed nucleus of the stria terminalis subregions differentially regulate hypothalamic-pituitary-adrenal axis activity: implications for the integration of limbic inputs. J. Neurosci. 27, 2025-2034.
14. Choi, D. C., Furay, A. R., Evanson, N. K., Ulrich-Lai, Y. M., Nguyen, M. M., Ostrander, M. M., and Herman, J. P. (2008). The role of the posterior medial bed nucleus of the stria termi-nalis in modulating hypothalamic-pituitary-adrenocortical axis responsiveness to acute and chronic stress. Psychoneuroendocrinology 33, 659-669.
15. Chuluyan, H. E., Saphier, D., Rohn, W. M., and Dunn, A. J. (1992). Noradrenergic innervation of the hypothalamus participates in adrenocortical responses to interleukin-1. Neuroendocrinology 56, 106-111.
16. Cole, M. A., Kim, P. J., Kalman, B. A., and Spencer, R. L. (2000). Dex-amethasone suppression of corticosteroid secretion: evaluation of the site of action by receptor measures and functional studies. Psychoneuroendocrinology 25, 151-167.
17. Cole, R. L., and Sawchenko, P. E. (2002). Neurotransmitter regulation of cellular activation and neuropeptide gene expression in the paraventricular nucleus of the hypothalamus. J. Neurosci. 22, 959-969.
18. Cole, T. J., Blendy, J. A., Monaghan, A.P., Krieglstein, K., Schmid, W., Aguzzi, A., Fantuzzi, G., Hummler, E., Unsicker, K., and Schutz, G. (1995). Targeted disruption of the glucocorticoid receptor gene blocks adrenergic chromaffin cell development and severely retards lung maturation. GenesDev. 9, 1608-1621.
19. Cowley, M. A., Pronchuk, N., Fan, W., Dinulescu, D. M., Colmers, W. F., and Cone, R. D. (1999). Integration of NPY, AGRP, andmelanocortin signals in the hypothalamic paraventricular nucleus: evidence of a cellular basis for the adipostat. Neuron 24, 155-163.
20. Csaki, A., Kocsis, K., Halasz, B., and Kiss, J. (2000). Localization of glutamater-gic/aspartatergic neurons projecting to the hypothalamic paraventricular nucleus studied by retrograde transport of [3H]D-aspartate autoradiography. Neuroscience 101, 637-655.
21. Cull-Candy, S., Brickley, S., and Far-rant, M. (2001). NMDA receptor subunits: diversity, development and disease. Curr. Opin. Neurobiol. 11, 327-335.
22. Cullinan, W. E. (2000). GABA(A) receptor subunit expression within hypophysiotropic CRH neurons: a dual hybridization histochemical study. J. Comp. Neurol. 419, 344-351.
23. Cullinan, W. E., and Wolfe, T. J. (2000). Chronic stress regulates levels of mRNA transcripts encoding beta subunits of the GABA(A) receptor in the rat stress axis. Brain Res. 887, 118-124.
24. Cummings, S., and Seybold, V. (1988). Relationship of alpha-1-and alpha-2-adrenergic-binding sites to regions of the paraventricular nucleus of the hypothalamus containing corticotropin-releasing factor and vasopressin neurons. Neuroendocrinology 47, 523-532.
25. Daban, C., Vieta, E., Mackin, P., and Young, A. H. (2005). Hypothalamic-pituitary-adrenal axis and bipolar disorder. Psychiatr. Clin. North Am. 28, 469-480.
26. Daftary, S. S., Boudaba, C., Szabo, K., and Tasker, J. G. (1998). Noradrenergic excitation ofmagnocellular neurons in the rat hypothalamic paraventricular nucleus via intranuclear glutamatergic circuits. J. Neurosci. 18, 10619-10628.
27. Daftary, S. S., Boudaba, C., and Tasker, J. G. (2000). Noradrenergic regulation of parvocellular neurons in the rat hypothalamic paraventricular nucleus. Neuroscience 96, 743-751.
28. Day, H. E., Campeau, S., Watson, S. J. Jr., and Akil, H. (1999). Expression of alpha(1b) adrenoceptor mRNA in corticotropin-releasing hormone-containing cells of the rat hypothalamus and its regulation by corticosterone. J. Neurosci. 19, 10098-10106.
29. Dayas, C. V., Buller, K. M., and Day, T. A. (2001). Medullary neurones regulate hypothalamic corticotropin-releasing factor cell responses to an emotional stressor. Neuroscience 105, 707-719.
30. Di, S., Malcher-Lopes, R., Halmos, K. C., and Tasker, J. G. (2003). Nongenomic glucocorticoid inhibition via endo-cannabinoid release in the hypothalamus: a fast feedback mechanism. J. Neurosci. 23, 4850-4857.
31. Dimitrov, E. L., Dejoseph, M. R., Brownfield, M. S., and Urban, J. H. (2007). Involvement of neuropeptide Y Y1 receptors in the regulation of neuroendocrine corticotropin-releasing hormone neuronal activity. Endocrinology 148, 3666-3673.
32. Durand, D., Pampillo, M., Caruso, C., and Lasaga, M. (2008). Role of metabotropic glutamate receptors in the control of neuroendocrine function. Neuropharmacology 55, 577-583.
33. Fava, G. A., Carson, S. W., Perini, G. I., Morphy, M. A., Molnar, G., and Jusko, W. J. (1984). The metyrapone test in affective disorders and schizophrenia. J. Affect. Disord. 6, 241-247.
34. Feldman, S., and Weidenfeld, J. (1997). Hypothalamic mechanisms mediating glutamate effects on the hypothalamo-pituitary-adrenocort-ical axis. J. Neural Transm. 104, 633-642.
35. Feldman, S., and Weidenfeld, J. (2004). Involvement of endoge-neous glutamate in the stimulatory effect of norepinephrine and serotonin on the hypothalamo-pituitary-adrenocortical axis. Neuroendocrinology 79, 43-53.
36. Feuvrier, E., Aubert, M., Mausset, A. L., Alonso, G., Gaillet, S., Malaval, F., and Szafarczyk, A. (1998). Glucocorticoids provoke a shift from alpha2-to alpha1-adrenoreceptor activities in cultured hypothalamic slices leading to opposite noradrenaline effect on corticotropin-releasing hormone release. J. Neurochem. 70, 1199-1209.
37. Flak, J. N., Ostrander, M. M., Tasker, J. G., and Herman, J. P. (2009). Chronic stress-induced neurotransmitter plasticityin the PVN. J. Comp. Neurol. 517, 156-165.
38. Franco, A. J., Zsombok, A., and Tasker, J. G. (2007). Rapid Glucocorticoid-Induced, Endocannabinoid-Mediated Inhibition ofSynapticExcitation in the Hypothalamus Maintained Following Chronic Variable Stress. Program No. 298.25/TT27. Washington, DC: Neuroscience Meeting Planner, Society for Neuroscience. Available at: http://www.sfn.org/index.aspx?pagename=abstracts_ampublications
39. Freund, T. F., Katona, I., and Piomelli, D. (2003). Role of endogenous cannabi-noids in synaptic signaling. Physiol. Rev. 83, 1017-1066.
40. Galanopoulou, A. S., and Moshe, S. L. (2003). Role of sex hormones in the sexually dimorphic expression of KCC2 in rat substantia nigra. Exp. Neurol. 184, 1003-1009.
41. Garno, J. L., Goldberg, J. F., Ramirez, P. M., and Ritzler, B. A. (2005). Impact of childhood abuse on the clinical course ofbipolar disorder. Br. J. Psychiatry 186, 121-125.
42. Gillespie, C. F., and Nemeroff, C.B. (2005). Hypercortisolemia and depression. Psychosom. Med. 67(Suppl. 1), S26-S28.
43. Goodwin, R. D., Fergusson, D. M., and Horwood, L. J. (2005). Childhood abuse and familial violence and the risk of panic attacks and panic disorder in young adulthood. Psychol. Med. 35, 881-890.
44. Gupta, A., and Silman, A. J. (2004). Psychological stress and fibromyalgia: a review of the evidence suggesting a neuroendocrine link. Arthritis Res. Ther. 6, 98-106.
45. Gustafsson, P. E., Gustafsson, P. A., Ivarsson, T., and Nelson, N. (2008). Diurnal cortisol levels and cortisol response in youths with obsessive-compulsive disorder. Neuropsychobiology 57, 14-21.
46. Haam, J., Popescu, I. R., Morton, L. A., Halmos, K. C., Teruyama, R., Ueta, U., and Tasker, J. G. (2012). GABA is excitatory in adult vasopressinergic neuroendocrine cells. J. Neurosci. 32, 572-582.
47. Han, S. K., Chong, W., Li, L. H., Lee, I. S, Murase, K., and Ryu, P. D. (2002). Noradrenaline excites and inhibits GABAergic transmission in parvo-cellular neurons of rat hypothalamic paraventricular nucleus. J. Neurophysiol. 87, 2287-2296.
48. Harris, C. C., and Tasker, J. G. (2011). A Calcium Requirement For Rapid Glucocorticoid Dependent Modulation Of Glutamate Release In The Supraoptic Nucleus. Program No. 501.01/VV32. Washington, DC: Neuroscience Meeting Planner, Society for Neuroscience. Available at: http:// www.sfn.org/am2011/pdf/prelim/ MON_Poster_PM_v2.pdf
49. Hatcher, S., and House, A. (2003). Life events, difficulties and dilemmas in the onset of chronic fatigue syndrome: a case-control study. Psychol. Med. 33, 1185-1192.
50. Heifets, B. D., and Castillo, P. E. (2009). Endocannabinoid signaling and long-term synaptic plasticity. Annu. Rev. Physiol. 71, 283-306.
51. Herman, J. P., Adams, D., and Prewitt, C. (1995). Regulatory changes in neuroendocrine stress-integrative circuitry produced by a variable stress paradigm. Neuroendocrinology 61, 180-190.
52. Herman, J. P., Eyigor, O., Ziegler, D. R., and Jennes, L. (2000). Expression of ionotropic glutamate receptor subunit mRNAs in the hypothalamic paraventricular nucleus of the rat. J. Comp. Neurol. 422, 352-362.
53. Herman, J. P., Figueiredo, H., Mueller, N. K., Ulrich-Lai, Y., Ostrander, M. M., Choi, D. C., and Cullinan, W. E. (2003). Central mechanisms of stress integration: hierarchical circuitry controlling hypothalamo-pituitary-adrenocortical responsiveness. Front. Neuroendocrinol. 24, 151-180.
54. Hewitt, S. A., Wamsteeker, J. I., Kurz, E.U., and Bains, J. S. (2009). Altered chloride homeostasis removes synaptic inhibitory constraint of the stress axis. Nat. Neurosci. 12, 438-443.
55. Hrabovszky, E., and Liposits, Z. (2008). Novel aspects of glutamatergic signalling in the neuroendocrine system. J. Neuroendocrinol. 20, 743-751.
56. Isenovic, E. R., Radojcic, M., Zakula, Z., Koricanac, G., and Ribarac-Stepic, N. (2006). Effect ofacute adrenalectomy on rat liver glucocorticoid receptor. Arch. Biol. Sci. 58, 153-159.
57. Itoi, K., Suda, T., Tozawa, F., Dobashi, I., Ohmori, N., Sakai, Y., Abe, K., and Demura, H. (1994). Microinjection of norepinephrine into the paraventricular nucleus of the hypothalamus stimulates corticotropin-releasing factor gene expression in conscious rats. Endocrinology 135, 2177-2182.
58. Jacobson, L., and Sapolsky, R. (1993). Augmented ACTH responses to stress in adrenalectomized rats replaced with constant, physiological levels of corticosterone are partially normalized by acute increases in corticosterone. Neuroendocrinology 58, 420-429.
59. Joels, M., Karst, H., Alfarez, D., Heine, V. M., Qin, Y., Van Riel, E., Verkuyl, M., Lucassen, P. J., and Krugers, H. J. (2004). Effects of chronic stress on structure and cell function in rat hippocampus and hypothalamus. Stress 7, 221-231.
60. Johnson, M. P., Kelly, G., and Chamberlain, M. (2001). Changes in rat serum corticosterone after treatment with metabotropic glutamate receptor agonists or antagonists. J. Neu-roendocrinol. 13, 670-677.
61. Juruena, M. F., Cleare, A. J., Papadopou-los, A. S., Poon, L., Lightman, S., and Pariante, C. M. (2006). Different responses to dexamethasone and prednisolone in the same depressed patients. Psychopharmacology (Berl.) 189, 225-235.
62. Kendler, K. S., Kessler, R. C., Walters, E. E., Maclean, C., Neale, M. C., Heath, A. C., and Eaves, L. J. (1995). Stressful life events, genetic liability, and onset of an episode of major depression in women. Am. J. Psychiatry 152, 833-842.
63. Kim, J. S., Kim, W. B., Kim, Y. B., Lee, Y., Kim, Y. S., Shen, F. Y., Lee, S. W., Park, D., Choi, H. J., Hur, J., Park, J. J., Han, H. C., Colwell, C. S., Cho, Y.W., and Kim, Y. I. (2011). Chronic hyperosmotic stress converts GABAergic inhibition into excitation in vasopressin and oxytocin neurons in the rat. J. Neurosci. 31, 13312-13322.
64. King, J. A., Mandansky, D., King, S., Fletcher, K. E., and Brewer, J. (2001). Early sexual abuse and low cortisol. Psychiatry Clin. Neurosci. 55, 71-74.
65. Kitraki, E., Karandrea, D., and Kit-tas, C. (1999). Long-lasting effects of stress on glucocorticoid receptor gene expression in the rat brain. Neuroendocrinology 69, 331-338.
66. Kocsis, K., Kiss, J., Gorcs, T., and Halasz, B. (1998). Metabotropic glutamate receptor in vasopressin, CRF andVIP hypothalamic neurones. Neuroreport 9, 4029-4033.
67. Korosi, A., Shanabrough, M., Mcclelland, S., Liu, Z. W., Borok, E., Gao, X. B., Horvath, T. L., and Baram, T. Z. (2010). Early-life experience reduces excitation to stress-responsive hypothalamic neurons and reprograms the expression of corticotropin-releasing hormone. J. Neurosci. 30, 703-713.
68. Kuzmiski, J. B., Marty, V., Baimoukha-metova, D. V., and Bains, J. S. (2010). Stress-induced priming of glutamate synapses unmasks associative shortterm plasticity. Nat. Neurosci. 13, 1257-1264.
69. Lang, C. H., and Ajmal, M. (1995). Metabolic, hormonal, and hemodynamic changes induced by metabotropic excitatory amino acid agonist (1S, 3R)-ACPD. Am. J. Physiol. 268, R1026-R1033.
70. Lenze, E. J., Mantella, R. C., Shi, P., Goate, A. M., Nowotny, P., Butters, M. A., Andreescu, C., Thompson, P. A., and Rollman, B. L. (2011). Elevated cortisol in older adults with generalized anxiety disorder is reduced by treatment: a placebo-controlledevaluation of esc-italopram. Am. J. Geriatr. Psychiatry 19, 482-490.
71. Li, H. Y., Ericsson, A., and Sawchenko, P. E. (1996). Distinct mechanisms underlie activation of hypothalamic neurosecretory neurons and their medullary catecholaminergic affer-ents in categorically different stress paradigms. Proc. Natl. Acad. Sci. U.S.A. 93, 2359-2364.
72. Liposits, Z., Phelix, C., and Paull, W. K. (1986). Adrenergic innervation of corticotropin releasing factor (CRF)-synthesizing neurons in the hypothalamic paraventricular nucleus of the rat. A combined light and electron microscopic immunocyto-chemical study. Histochemistry 84, 201-205.
73. Liu, D., Diorio, J., Tannenbaum, B., Caldji, C., Francis, D., Freedman, A., Sharma, S., Pearson, D., Plotsky, P. M., and Meaney, M. J. (1997). Maternal care, hippocampal glucocorticoid receptors, and hypothalamic-pituitary-adrenal responses to stress. Science 277, 1659-1662.
74. Louvart, H., Maccari, S., Ducrocq, F., Thomas, P., and Darnaudery, M. (2005). Long-term behavioural alterations in female rats after a single intense footshock followed by situational reminders. Psychoneuroendocrinology 30, 316-324.
75. Luther, J. A., Daftary, S. S., Boudaba, C., Gould, G. C., Halmos, K. C., and Tasker, J. G. (2002). Neurosecretory and non-neurosecretory parvocellu-lar neurones of the hypothalamic paraventricular nucleus express distinct electrophysiological properties. J. Neuroendocrinol. 14, 929-932.
76. Luther, J. A., and Tasker, J. G. (2000). Voltage-gated currents distinguish parvocellular from magnocel-lular neurones in the rat hypothalamic paraventricular nucleus. J. Physiol. 523(Pt 1), 193-209.
77. Ma, S., and Morilak, D. A. (2005). Chronic intermittent cold stress sensitises the hypothalamic-pituitary-adrenal response to a novel acute stress by enhancing noradrenergic influence in the rat paraventricular nucleus. J. Neuroendocrinol. 17, 761-769.
78. Majewska, M. D., Bisserbe, J. C., and Eskay, R. L. (1985). Glucocorticoids are modulators of GABAA receptors in brain. Brain Res. 339, 178-182.
79. Malcher-Lopes, R., Di, S., Marcheselli, V. S., Weng, F. J., Stuart, C. T., Bazan, N. G., and Tasker, J. G. (2006). Opposing crosstalk between leptin and glucocorticoids rapidly modulates synaptic excitation via endo-cannabinoid release. J. Neurosci. 26, 6643-6650.
80. Miklos, I. H., and Kovacs, K. J. (2002). GABAergic innervation of corticotropin-releasing hormone (CRH)-secreting parvocellular neurons and its plasticity as demonstrated by quantitative immunoelectron microscopy. Neuroscience 113, 581-592.
81. Modell, S., Yassouridis, A., Huber, J., and Holsboer, F. (1997). Corticosteroid receptor function is decreased in depressed patients. Neuroendocrinology 65, 216-222.
82. Morphy, M. A., Fava, G. A., Perini, G.I., and Molnar, G. (1985). The metyrapone test in depressed males. Prog. Neuropsychopharmacol. Biol. Psychiatry 9, 187-191.
83. Nahar, J., Haam, J., Glatzer, N. R., Hal-mos, K. C., Muglia, L. J., Dohanich, G.P., and Tasker, J. G. (2012). Rapid glucocorticoid actions in hypothalamic neuroendocrine cells are dependent on the glucocorticoid receptor. Endocrinology (submitted).
84. O'Regan, D., Kenyon, C. J., Seckl, J. R., and Holmes, M. C. (2010). Environmental disturbance confounds prenatal glucocorticoid programming experiments in Wistar rats. Lab. Anim. 44, 199-205.
85. Olpe, H. R., and McEwen, B. S. (1976). Glucocorticoid binding to receptorlike proteins in rat brain and pituitary: ontogenetic and experimentally induced changes. Brain Res. 105, 121-128.
86. Ostrander, M. M., Ulrich-Lai, Y. M., Choi, D. C., Richtand, N. M., and Herman, J. P. (2006). Hypoactiv-ity of the hypothalamo-pituitary-adrenocortical axis during recovery from chronic variable stress. Endocrinology 147, 2008-2017.
87. Pacak, K., Kvetnansky, R., Palkovits, M., Fukuhara, K., Yadid, G., Kopin, I. J., and Goldstein, D. S. (1993). Adrenalectomy augments in vivo release of norepinephrine in the paraventricular nucleus during immobilization stress. Endocrinology 133, 1404-1410.
88. Pacak, K., Palkovits, M., Kvetnansky, R., Matern, P., Hart, C., Kopin, I. J., and Goldstein, D. S. (1995). Cate-cholaminergic inhibition by hyper-cortisolemia in the paraventricular nucleus of conscious rats. Endocrinology 136, 4814-4819.
89. Pacak, K., Palkovits, M., Yadid, G., Kvetnansky, R., Kopin, I. J., and Goldstein, D. S. (1998). Heterogeneous neurochemical responses to different stressors: a test of Selye's doctrine of nonspecificity. Am. J. Physiol. 275, R1247-R1255.
90. Packan, D. R., and Sapolsky, R. M. (1990). Glucocorticoid endanger-ment of the hippocampus: tissue, steroid and receptor specificity. Neuroendocrinology 51, 613-618.
91. Penninx, B. W., Beekman, A. T., Bandinelli, S., Corsi, A. M., Brem-mer, M., Hoogendijk, W. J., Guralnik, J. M., and Ferrucci, L. (2007). Late-life depressive symptoms are associated with both hyperactivity and hypoactivity of the hypothalamo-pituitary-adrenal axis. Am. J. Geriatr. Psychiatry 15, 522-529.
92. Plotsky, P. M., Otto, S., and Sutton, S. (1987). Neurotransmitter modulation of corticotropin releasing factor secretion into the hypophysial-portal circulation. Life Sci. 41, 1311-1317.
93. Raadsheer, F. C., Hoogendijk, W. J., Stam, F. C., Tilders, F. J., and Swaab, D.F. (1994). Increased numbers of corticotropin-releasing hormone expressing neurons in the hypothalamic paraventricular nucleus of depressed patients. Neuroendocrinology 60, 436-444.
94. Raadsheer, F. C., Van Heerikhuize, J. J., Lucassen, P. J., Hoogendijk, W. J., Tilders, F. J., and Swaab, D.F. (1995). Corticotropin-releasing hormone mRNA levels in the paraventricular nucleus of patients with Alzheimer's disease and depression. Am. J. Psychiatry 152, 1372-1376.
95. Radley, J. J., Gosselink, K. L., and Sawchenko, P. E. (2009). A discrete GABAergic relay mediates medial prefrontal cortical inhibition of the neuroendocrine stress response. J. Neurosci. 29, 7330-7340.
96. Radley, J. J., andSawchenko, P. E.(2011). A common substrate for prefrontal and hippocampal inhibition of the neuroendocrine stress response. J. Neurosci. 31, 9683-9695.
97. Raiteri, M., Bonanno, G., Maura, G., Pende, M., Andrioli, G. C., and Ruelle, A. (1992). Subclassification of release-regulating alpha 2-autoreceptors in human brain cortex. Br. J. Pharmacol. 107, 1146-1151.
98. Roland, B. L., and Sawchenko, P. E. (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.
99. Sarkhel, S., Praharaj, S. K., and Sinha, V. K. (2011). Role of life events in obsessive compulsive disorder. Isr. J. Psychiatry Relat. Sci. 48, 182-185.
100. Sawchenko, P. E. (1988). Effects of catecholamine-depleting medullary knife cuts on corticotropin-releasing factor and vasopressin immunoreac-tivity in the hypothalamus of normal and steroid-manipulated rats. Neuroendocrinology 48, 459-470.
101. Schrader, L. A., and Tasker, J. G. (1997). Presynaptic modulation by metabotropic glutamate receptors of excitatory and inhibitory synaptic inputs to hypothalamic magnocel-lular neurons. J. Neurophysiol. 77, 527-536.
102. Shimizu, K. (1984). Effect of alpha 1-and alpha 2-adrenoceptor agonists and antagonists on ACTH secretion in intact and in hypothalamic deaf-ferentated rats. Jpn. J. Pharmacol. 36, 23-33.
103. Simmons, D. M., and Swanson, L. W. (2009). Comparison of the spatial distribution of seven types of neuroendocrine neurons in the rat paraventricular nucleus: toward a global 3D model. J. Comp. Neurol. 516, 423-441.
104. Stein, M. B., Yehuda, R., Koverola, C., andHanna, C. (1997). Enhanceddex-amethasone suppression of plasma cortisol in adult women traumatized by childhood sexual abuse. Biol. Psychiatry 42, 680-686.
105. Stern, J. E. (2001). Electrophysio-logical and morphological properties of pre-autonomic neurones in the rat hypothalamic paraventricular nucleus. J. Physiol. 537, 161-177.
106. Svec, F., Gordon, S., and Tate, D. (1989). Glucocorticoid receptor regulation: the effects of adrenalectomy, exogenous glucocorticoid, and stress on hepatic receptor number in male and female mice. Biochem. Med. Metab. Biol. 41, 224-233.
107. Szafarczyk, A., Feuvrier, E., Siaud, P., Rondouin, G., Lacoste, M., Gaillet, S., Malaval, F., and Assenmacher, I. (1995). Removal of adrenal steroids from the medium reverses the stimulating effect of catecholamines on corticotropin-releasing hormone neurons in organotypic cultures. Neuroendocrinology 61, 517-524.
108. Szafarczyk, A., Gaillet, S., Barbanel, G., Malaval, F., and Assenmacher, I. (1990). [Implication of alpha-2 adrenergic post-synaptic receptors in the central catecholaminergic stimulation of the corticotropic axis in rats]. C R Acad. Sci. III. 311, 81-88.
109. Tanriverdi, F., Karaca, Z., Unluhizarci, K., and Kelestimur, F. (2007). The hypothalamo-pituitary-adrenal axis in chronic fatigue syndrome and fibromyalgia syndrome. Stress 10, 13-25.
110. Tasker, J. G., Boudaba, C., and Schrader, L. A. (1998). Local glu-tamatergic and GABAergic synaptic circuits and metabotropic glutamate receptors in the hypothalamic paraventricular and supraoptic nuclei. Adv. Exp. Med. Biol. 449, 117-121.
111. Tasker, J. G., and Dudek, F. E. (1991). Electrophysiological properties of neurones in the region of the paraventricular nucleus in slices of rat hypothalamus. J. Physiol. 434, 271-293.
112. Tuchelt, H., Dekker, K., Bahr, V., and Oelkers, W. (2000). Dose-response relationship between plasma ACTH and serum cortisol in the insulin-hypoglycaemiatest in 25 healthysub-jects and 109 patients with pituitary disease. Clin. Endocrinol. (Oxf.) 53, 301-307.
113. Ulrich-Lai, Y. M., Jones, K. R., Ziegler, D.R., Cullinan, W. E., and Herman, J. P. (2011). Forebrain origins of glutamatergic innervation to the rat paraventricular nucleus of the hypothalamus: differential inputs to the anterior versus posterior subregions. J. Comp. Neurol. 519, 1301-1319.
114. Ur, E., Dinan, T. G., O'keane, V., Clare, A. W., Mcloughlin, L., Rees, L. H., Turner, T. H., Grossman, A., and Besser, G. M. (1992). Effect of metyrapone on the pituitary-adrenal axis in depression: relation to dexam-ethasone suppressor status. Neuroendocrinology 56, 533-538.
115. van Dijken, H. H., De Goeij, D. C., Sutanto, W., Mos, J., De Kloet, E.R., and Tilders, F. J. (1993). Short inescapable stress produces long-lasting changes in the brain-pituitary-adrenal axis of adult male rats. Neuroendocrinology 58, 57-64.
116. Van Houdenhove, B., Van Den Eede, F., and Luyten, P. (2009). Does hypothalamic-pituitary-adrenal axis hypofunction in chronic fatigue syndrome reflect a "crash" in the stress system? Med. Hypotheses 72, 701-705.
117. Verkuyl, J. M., Hemby, S. E., and Joels, M. (2004). Chronic stress attenuates GABAergic inhibition and alters gene expression of parvocellular neurons in rat hypothalamus. Eur. J. Neurosci. 20, 1665-1673.
118. Verkuyl, J. M., and Joels, M. (2003). Effect of adrenalectomy on miniature inhibitory postsynaptic currents in the paraventricular nucleus of the hypothalamus. J. Neurophysiol. 89, 237-245.
119. Verkuyl, J. M., Karst, H., and Joels, M. (2005). GABAergic transmission in the rat paraventricular nucleus of the hypothalamus is suppressed by corticosterone and stress. Eur. J. Neurosci. 21, 113-121.
120. Wall, N. R., Wickersham, I. R., Cetin, A., De La Parra, M., and Callaway, E. M. (2010). Monosynaptic circuit tracing in vivo through Cre-dependent targeting and complementation of modified rabies virus. Proc. Natl. Acad. Sci. U.S.A. 107, 21848-21853.
121. Wamsteeker, J. I., Kuzmiski, J. B., and Bains, J. S. (2010). Repeated stress impairs endocannabinoid signaling in the paraventricular nucleus of the hypothalamus. J. Neurosci. 30, 11188-11196.
122. Wang, R., Liu, X., Hentges, S. T., Dunn-Meynell, A. A., Levin, B. E., Wang, W., and Routh, V. H. (2004). The regulation of glucose-excited neurons in the hypothalamic arcuate nucleus by glucose and feedingrelevant peptides. Diabetes 53, 1959-1965.
123. Webster, M. J., Knable, M. B., O'grady, J., Orthmann, J., and Weickert, C. S. (2002). Regional specificity of brain glucocorticoid receptor mRNA alterations in subjects with schizophrenia and mood disorders. Mol. Psychiatry 7, 985-994; 924.
124. Wittmann, G., Lechan, R. M., Liposits, Z., and Fekete, C. (2005). Glutamatergic innervation of corticotropin-releasing hormone-and thyrotropin-releasing hormone-synthesizing neurons in the hypothalamic paraventricular nucleus of the rat. Brain Res. 1039, 53-62.
125. Yang, J. H., Li, L. H., Lee, S., Jo, I. H., Lee, S. Y., and Ryu, P. D. (2007). Effects of adrenalectomy on the excitability of neurosecretory parvocellular neurones in the hypothalamic paraventricular nucleus. J. Neuroendocrinol. 19, 293-301.
126. Yang, J. H., Li, L. H., Shin, S. Y., Lee, S., Lee, S. Y., Han, S. K., and Ryu, P. D. (2008). Adrenalectomy potentiates noradrenergic suppression of GABAergic transmission in parvocellular neurosecretory neurons ofhypothalamic paraventricular nucleus. J. Neurophysiol. 99, 514-523.
127. Yehuda, R. (2006). Advances in understanding neuroendocrine alterations in PTSD and their therapeutic implications. Ann. N.Y. Acad. Sci. 1071, 137-166.
128. Yehuda, R., Boisoneau, D., Lowy, M. T., and Giller, E. L. Jr. (1995). Dose-response changes in plasma cortisol and lymphocyte glucocorticoid receptors following dexam-ethasone administration in combat veterans with and without posttrau-matic stress disorder. Arch. Gen. Psychiatry 52, 583-593.
129. Young, E. A., Altemus, M., Lopez, J. F., Kocsis, J. H., Schatzberg, A. F., Debat-tista, C., and Zubieta, J. K. (2004). HPA axis activation in major depression and response to fluoxetine: a pilot study. Psychoneuroendocrinology 29, 1198-1204.
130. Ziegler, D. R., Cullinan, W. E., and Herman, J. P. (2005). Organization and regulation of paraventricular nucleus glutamate signaling systems: N-methyl-D-aspartate receptors. J. Comp. Neurol. 484, 43-56.
131. Ziegler, D. R., and Herman, J. P. (2000). Local integration ofglutamate signaling in the hypothalamic paraventricular region: regulation of glucocorticoid stress responses. Endocrinology 141, 4801-4804.
132. Ziegler, D. R., and Herman, J. P. (2002). Neurocircuitry of stress integration: anatomical pathways regulating the hypothalamo-pituitary-adrenocortical axis of the rat. Integr. Comp. Biol. 42, 541-551.