Regulation of hypophysiotrophic corticotrophin-releasing hormone- and thyrotrophin-releasing hormone-synthesising neurones by brainstem catecholaminergic neurones

Journal of Neuroendocrinology

Volumn 20, Issue 7, 2008, Pages 952-960

  Wittmann, Gábor ^a  

^a INSTITUTE OF EXPERIMENTAL MEDICINE   (Hungary)

Author keywords

Adrenergic; CRH; Noradrenergic; Paraventricular nucleus; TRH

Indexed keywords

ADRENALIN; CATECHOLAMINE; CORTICOTROPIN RELEASING FACTOR; GLUCOCORTICOID; NEUROTRANSMITTER; NORADRENALIN; PROTIRELIN; THYROID HORMONE;

ARTICLE; BRAIN STEM; CARDIOVASCULAR SYSTEM; CATECHOLAMINE NERVE CELL; CELL POPULATION; COLD; GLUCOSE BLOOD LEVEL; HORMONAL REGULATION; HYPOTHALAMUS PERIVENTRICULAR NUCLEUS; IMMUNE SYSTEM; INNERVATION; MENTAL STRESS; NERVE FIBER; NEUROSECRETORY CELL; NONHUMAN; PRIORITY JOURNAL; RAT; THYROID HORMONE RELEASE;

ANIMALS; BLOOD GLUCOSE; BRAIN STEM; CATECHOLAMINES; COLD; CORTICOTROPIN-RELEASING HORMONE; ENVIRONMENT; IMMUNE SYSTEM; NEURONS; PARAVENTRICULAR HYPOTHALAMIC NUCLEUS; PITUITARY HORMONE-RELEASING HORMONES; RATS; STRESS, PSYCHOLOGICAL; THYROTROPIN-RELEASING HORMONE;

EID: 45749109818     PISSN: 09538194     EISSN: 13652826     Source Type: Journal    
DOI: 10.1111/j.1365-2826.2008.01748.x     Document Type: Article

References (98)

1. Swanson LW, Sawchenko PE. Hypothalamic integration: Organization of the paraventricular and supraoptic nuclei. Annu Rev Neurosci 1983; 6: 269-324.
2. Fuzesi T, Wittmann G, Liposits Z, Lechan RM, Fekete C. Contribution of noradrenergic and adrenergic cell groups of the brainstem and agouti-related protein-synthesizing neurons of the arcuate nucleus to neuropeptide-y innervation of corticotropin-releasing hormone neurons in hypothalamic paraventricular nucleus of the rat. Endocrinology 2007; 148: 5442-5450.
3. Lechan RM, Fekete C. The TRH neuron: A hypothalamic integrator of energy metabolism. Prog Brain Res 2006; 153: 209-235.
4. Liposits Z, Phelix C, Paull WK. Synaptic interaction of serotonergic axons and corticotropin releasing factor (CRF) synthesizing neurons in the hypothalamic paraventricular nucleus of the rat. A light and electron microscopic immunocytochemical study. Histochemistry 1987; 86: 541-549.
5. Wittmann G, Liposits Z, Lechan RM, Fekete C. Origin of cocaine- and amphetamine-regulated transcript-containing axons innervating hypophysiotropic corticotropin-releasing hormone-synthesizing neurons in the rat. Endocrinology 2005; 146: 2985-2991.
6. Sawchenko PE, Swanson LW. The organization of noradrenergic pathways from the brainstem to the paraventricular and supraoptic nuclei in the rat. Brain Res 1982; 257: 275-325.
7. Sawchenko PE, Swanson LW, Grzanna R, Howe PR, Bloom SR, Polak JM. Colocalization of neuropeptide Y immunoreactivity in brainstem catecholaminergic neurons that project to the paraventricular nucleus of the hypothalamus. J Comp Neurol 1985; 241: 138-153.
8. Cunningham ET Jr, Bohn MC, Sawchenko PE. Organization of adrenergic inputs to the paraventricular and supraoptic nuclei of the hypothalamus in the rat. J Comp Neurol 1990; 292: 651-667.
9. Cunningham ET Jr, Sawchenko PE. Anatomical specificity of noradrenergic inputs to the paraventricular and supraoptic nuclei of the rat hypothalamus. J Comp Neurol 1988; 274: 60-76.
10. Dun SL, Ng YK, Brailoiu GC, Ling EA, Dun NJ. Cocaine- and amphetamine-regulated transcript peptide-immunoreactivity in adrenergic C1 neurons projecting to the intermediolateral cell column of the rat. J Chem Neuroanat 2002; 23: 123-132.
11. Fekete C, Wittmann G, Liposits Z, Lechan RM. Origin of cocaine- and amphetamine-regulated transcript (CART)-immunoreactive innervation of the hypothalamic paraventricular nucleus. J Comp Neurol 2004; 469: 340-350.
12. Das M, Vihlen CS, Legradi G. Hypothalamic and brainstem sources of pituitary adenylate cyclase-activating polypeptide nerve fibers innervating the hypothalamic paraventricular nucleus in the rat. J Comp Neurol 2007; 500: 761-776.
13. Levin MC, Sawchenko PE, Howe PR, Bloom SR, Polak JM. Organization of galanin-immunoreactive inputs to the paraventricular nucleus with special reference to their relationship to catecholaminergic afferents. J Comp Neurol 1987; 261: 562-582.
14. Stornetta RL, Sevigny CP, Guyenet PG. Vesicular glutamate transporter DNPI/VGLUT2 mRNA is present in C1 and several other groups of brainstem catecholaminergic neurons. J Comp Neurol 2002; 444: 191-206.
15. Liposits Z, Paull WK, Wu P, Jackson IM, Lechan RM. Hypophysiotrophic thyrotropin releasing hormone (TRH) synthesizing neurons. Ultrastructure, adrenergic innervation and putative transmitter action. Histochemistry 1987; 88: 1-10.
16. Liposits Z, Phelix C, Paull WK. Adrenergic innervation of corticotropin releasing factor (CRF)-synthesizing neurons in the hypothalamic paraventricular nucleus of the rat. A combined light and electron microscopic immunocytochemical study. Histochemistry 1986; 84: 201-205.
17. Wittmann G, Liposits Z, Lechan RM, Fekete C. Medullary adrenergic neurons contribute to the neuropeptide Y-ergic innervation of hypophysiotropic thyrotropin-releasing hormone-synthesizing neurons in the rat. Neurosci Lett 2002; 324: 69-73.
18. Wittmann G, Liposits Z, Lechan RM, Fekete C. Medullary adrenergic neurons contribute to the cocaine- and amphetamine-regulated transcript-immunoreactive innervation of thyrotropin-releasing hormone synthesizing neurons in the hypothalamic paraventricular nucleus. Brain Res 2004; 1006: 1-7.
19. Hornby PJ, Piekut DT. Opiocortin and catecholamine input to CRF-immunoreactive neurons in rat forebrain. Peptides 1989; 10: 1139-1146.
20. Legradi G, Lechan RM. The arcuate nucleus is the major source for neuropeptide Y-innervation of thyrotropin-releasing hormone neurons in the hypothalamic paraventricular nucleus. Endocrinology 1998; 139: 3262-3270.
21. Legradi G, Hannibal J, Lechan RM. Association between pituitary adenylate cyclase-activating polypeptide and thyrotropin-releasing hormone in the rat hypothalamus. J Chem Neuroanat 1997; 13: 265-279.
22. Plotsky PM. Facilitation of immunoreactive corticotropin-releasing factor secretion into the hypophysial-portal circulation after activation of catecholaminergic pathways or central norepinephrine injection. Endocrinology 1987; 121: 924-930.
23. Itoi K, Suda T, Tozawa F, Dobashi I, Ohmori N, Sakai Y, Abe K, Demura H. Microinjection of norepinephrine into the paraventricular nucleus of the hypothalamus stimulates corticotropin-releasing factor gene expression in conscious rats. Endocrinology 1994; 135: 2177-2182.
24. Day HE, Campeau S, Watson SJ Jr, Akil H. Expression of alpha(1b) adrenoceptor mRNA in corticotropin-releasing hormone-containing cells of the rat hypothalamus and its regulation by corticosterone. J Neurosci 1999; 19: 10098-10106.
25. Cole RL, Sawchenko PE. Neurotransmitter regulation of cellular activation and neuropeptide gene expression in the paraventricular nucleus of the hypothalamus. J Neurosci 2002; 22: 959-969.
26. Itoi K, Helmreich DL, Lopez-Figueroa MO, Watson SJ. Differential regulation of corticotropin-releasing hormone and vasopressin gene transcription in the hypothalamus by norepinephrine. J Neurosci 1999; 19: 5464-5472.
27. Khan AM, Ponzio TA, Sanchez-Watts G, Stanley BG, Hatton GI, Watts AG. Catecholaminergic control of mitogen-activated protein kinase signaling in paraventricular neuroendocrine neurons in vivo and in vitro: A proposed role during glycemic challenges. J Neurosci 2007; 27: 7344-7360.
28. Davis S, Vanhoutte P, Pages C, Caboche J, Laroche S. The MAPK/ERK cascade targets both Elk-1 and cAMP response element-binding protein to control long-term potentiation-dependent gene expression in the dentate gyrus in vivo. J Neurosci 2000; 20: 4563-4572.
29. Sgambato V, Pages C, Rogard M, Besson MJ, Caboche J. Extracellular signal-regulated kinase (ERK) controls immediate early gene induction on corticostriatal stimulation. J Neurosci 1998; 18: 8814-8825.
30. Guardiola-Diaz HM, Boswell C, Seasholtz AF. The cAMP-responsive element in the corticotropin-releasing hormone gene mediates transcriptional regulation by depolarization. J Biol Chem 1994; 269: 14784-14791.
31. Kovacs KJ, Sawchenko PE. Sequence of stress-induced alterations in indices of synaptic and transcriptional activation in parvocellular neurosecretory neurons. J Neurosci 1996; 16: 262-273.
32. Seasholtz AF, Thompson RC, Douglass JO. Identification of a cyclic adenosine monophosphate-responsive element in the rat corticotropin-releasing hormone gene. Mol Endocrinol 1988; 2: 1311-1319.
33. Wolfl S, Martinez C, Majzoub JA. Inducible binding of cyclic adenosine 3′,5′-monophosphate (cAMP)-responsive element binding protein (CREB) to a cAMP-responsive promoter in vivo. Mol Endocrinol 1999; 13: 659-669.
34. Khan AM, Watts AG. Intravenous 2-deoxy-D-glucose injection rapidly elevates levels of the phosphorylated forms of p44/42 mitogen-activated protein kinases (extracellularly regulated kinases 1/2) in rat hypothalamic parvicellular paraventricular neurons. Endocrinology 2004; 145: 351-359.
35. Ritter S, Watts AG, Dinh TT, Sanchez-Watts G, Pedrow C. Immunotoxin lesion of hypothalamically projecting norepinephrine and epinephrine neurons differentially affects circadian and stressor-stimulated corticosterone secretion. Endocrinology 2003; 144: 1357-1367.
36. Singru PS, Sanchez E, Acharya R, Fekete C, Lechan RM. MAP kinase contributes to lipopolysaccharide-induced activation of corticotropin-releasing hormone in the hypothalamic paraventricular nucleus. Endocrinology 2008; 149: 2283-2292.
37. Kobilka B. Adrenergic receptors as models for G protein-coupled receptors. Annu Rev Neurosci 1992; 15: 87-114.
38. Krulich L. Neurotransmitter control of thyrotropin secretion. Neuroendocrinology 1982; 35: 139-147.
39. Perello M, Stuart RC, Varslet CA, Nillni EA. Cold exposure increases the biosynthesis and proteolytic processing of prothyrotropin releasing hormone in the hypothalamic paraventricular nucleus via beta-adrenoreceptors. Endocrinology 2007; 148: 4952-4964.
40. Harris M, Aschkenasi C, Elias CF, Chandrankunnel A, Nillni EA, Bjoorbaek C, Elmquist JK, Flier JS, Hollenberg AN. Transcriptional regulation of the thyrotropin-releasing hormone gene by leptin and melanocortin signaling. J Clin Invest 2001; 107: 111-120.
41. Lee SL, Stewart K, Goodman RH. Structure of the gene encoding rat thyrotropin releasing hormone. J Biol Chem 1988; 263: 16604-16609.
42. Tapia-Arancibia L, Arancibia S, Astier H. Evidence for alpha 1-adrenergic stimulatory control of in vitro release of immunoreactive thyrotropin-releasing hormone from rat median eminence: In vivo corroboration. Endocrinology 1985; 116: 2314-2319.
43. Boudaba C, Di S, Tasker JG. Presynaptic noradrenergic regulation of glutamate inputs to hypothalamic magnocellular neurones. J Neuroendocrinol 2003; 15: 803-810.
44. Chen Q, Li DP, Pan HL. Presynaptic alpha1 adrenergic receptors differentially regulate synaptic glutamate and GABA release to hypothalamic presympathetic neurons. J Pharmacol Exp Ther 2006; 316: 733-742.
45. Gordon GR, Baimoukhametova DV, Hewitt SA, Rajapaksha WR, Fisher TE, Bains JS. Norepinephrine triggers release of glial ATP to increase postsynaptic efficacy. Nat Neurosci 2005; 8: 1078-1086.
46. Gordon GR, Bains JS. Priming of excitatory synapses by alpha1 adrenoceptor-mediated inhibition of group III metabotropic glutamate receptors. J Neurosci 2003; 23: 6223-6231.
47. Han SK, Chong W, Li LH, Lee IS, Murase K, Ryu PD. Noradrenaline excites and inhibits GABAergic transmission in parvocellular neurons of rat hypothalamic paraventricular nucleus. J Neurophysiol 2002; 87: 2287-2296.
48. Daftary SS, Boudaba C, Tasker JG. Noradrenergic regulation of parvocellular neurons in the rat hypothalamic paraventricular nucleus. Neuroscience 2000; 96: 743-751.
49. Feldman S, Weidenfeld J. Involvement of endogeneous glutamate in the stimulatory effect of norepinephrine and serotonin on the hypothalamo-pituitary-adrenocortical axis. Neuroendocrinology 2004; 79: 43-53.
50. Sarkar S, Lechan RM. Central administration of neuropeptide Y reduces alpha-melanocyte-stimulating hormone-induced cyclic adenosine 5′-monophosphate response element binding protein (CREB) phosphorylation in pro-thyrotropin-releasing hormone neurons and increases CREB phosphorylation in corticotropin-releasing hormone neurons in the hypothalamic paraventricular nucleus. Endocrinology 2003; 144: 281-291.
51. Fekete C, Kelly J, Mihaly E, Sarkar S, Rand WM, Legradi G, Emerson CH, Lechan RM. Neuropeptide Y has a central inhibitory action on the hypothalamic-pituitary-thyroid axis. Endocrinology 2001; 142: 2606-2613.
52. Michel MC, Beck-Sickinger A, Cox H, Doods HN, Herzog H, Larhammar D, Quirion R, Schwartz T, Westfall T. XVI. International Union of Pharmacology recommendations for the nomenclature of neuropeptide Y, peptide YY, and pancreatic polypeptide receptors. Pharmacol Rev 1998; 50: 143-150.
53. Brunton PJ, Bales J, Russell JA. Neuroendocrine stress but not feeding responses to centrally administered neuropeptide Y are suppressed in pregnant rats. Endocrinology 2006; 147: 3737-3745.
54. Kopp J, Xu ZQ, Zhang X, Pedrazzini T, Herzog H, Kresse A, Wong H, Walsh JH, Hokfelt T. Expression of the neuropeptide Y Y1 receptor in the CNS of rat and of wild-type and Y1 receptor knock-out mice. Focus on immunohistochemical localization. Neuroscience 2002; 111: 443-532.
55. Pronchuk N, Beck-Sickinger AG, Colmers WF. Multiple NPY receptors Inhibit GABA(A) synaptic responses of rat medial parvocellular effector neurons in the hypothalamic paraventricular nucleus. Endocrinology 2002; 143: 535-543.
56. Bali B, Kovacs KJ. GABAergic control of neuropeptide gene expression in parvocellular neurons of the hypothalamic paraventricular nucleus. Eur J Neurosci 2003; 18: 1518-1526.
57. Fekete C, Mihaly E, Luo LG, Kelly J, Clausen JT, Mao Q, Rand WM, Moss LG, Kuhar M, Emerson CH, Jackson IM, Lechan RM. Association of cocaine- and amphetamine-regulated transcript-immunoreactive elements with thyrotropin-releasing hormone-synthesizing neurons in the hypothalamic paraventricular nucleus and its role in the regulation of the hypothalamic-pituitary-thyroid axis during fasting. J Neurosci 2000; 20: 9224-9234.
58. Smith SM, Vaughan JM, Donaldson CJ, Rivier J, Li C, Chen A, Vale WW. Cocaine- and amphetamine-regulated transcript activates the hypothalamic-pituitary-adrenal axis through a corticotropin-releasing factor receptor-dependent mechanism. Endocrinology 2004; 145: 5202-5209.
59. Sarkar S, Wittmann G, Fekete C, Lechan RM. Central administration of cocaine- and amphetamine-regulated transcript increases phosphorylation of cAMP response element binding protein in corticotropin-releasing hormone-producing neurons but not in prothyrotropin-releasing hormone-producing neurons in the hypothalamic paraventricular nucleus. Brain Res 2004; 999: 181-192.
60. Agarwal A, Halvorson LM, Legradi G. Pituitary adenylate cyclase-activating polypeptide (PACAP) mimics neuroendocrine and behavioral manifestations of stress: Evidence for PKA-mediated expression of the corticotropin-releasing hormone (CRH) gene. Brain Res Mol Brain Res 2005; 138: 45-57.
61. Lightman SL, Harbuz MS. Expression of corticotropin-releasing factor mRNA in response to stress. Ciba Found Symp 1993; 172: 173-187.
62. Ritter S, Llewellyn-Smith I, Dinh TT. Subgroups of hindbrain catecholamine neurons are selectively activated by 2-deoxy-D-glucose induced metabolic challenge. Brain Res 1998; 805: 41-54.
63. Ritter S, Dinh TT, Zhang Y. Localization of hindbrain glucoreceptive sites controlling food intake and blood glucose. Brain Res 2000; 856: 37-47.
64. Li AJ, Ritter S. Glucoprivation increases expression of neuropeptide Y mRNA in hindbrain neurons that innervate the hypothalamus. Eur J Neurosci 2004; 19: 2147-2154.
65. Ritter S, Dinh TT, Li AJ. Hindbrain catecholamine neurons control multiple glucoregulatory responses. Physiol Behav 2006; 89: 490-500.
66. Li AJ, Wang Q, Ritter S. Differential responsiveness of dopamine-beta-hydroxylase gene expression to glucoprivation in different catecholamine cell groups. Endocrinology 2006; 147: 3428-3434.
67. Sapolsky R, Rivier C, Yamamoto G, Plotsky P, Vale W. Interleukin-1 stimulates the secretion of hypothalamic corticotropin-releasing factor. Science 1987; 238: 522-524.
68. Ericsson A, Kovacs KJ, Sawchenko PE. A functional anatomical analysis of central pathways subserving the effects of interleukin-1 on stress-related neuroendocrine neurons. J Neurosci 1994; 14: 897-913.
69. Li HY, Ericsson A, Sawchenko PE. Distinct mechanisms underlie activation of hypothalamic neurosecretory neurons and their medullary catecholaminergic afferents in categorically different stress paradigms. Proc Natl Acad Sci USA 1996; 93: 2359-2364.
70. Buller KM, Xu Y, Day TA. Indomethacin attenuates oxytocin and hypothalamic-pituitary-adrenal axis responses to systemic interleukin-1 beta. J Neuroendocrinol 1998; 10: 519-528.
71. Ericsson A, Arias C, Sawchenko PE. Evidence for an intramedullary prostaglandin-dependent mechanism in the activation of stress-related neuroendocrine circuitry by intravenous interleukin-1. J Neurosci 1997; 17: 7166-7179.
72. Lacroix S, Rivest S. Functional circuitry in the brain of immune-challenged rats: Partial involvement of prostaglandins. J Comp Neurol 1997; 387: 307-324.
73. Schiltz JC, Sawchenko PE. Distinct brain vascular cell types manifest inducible cyclooxygenase expression as a function of the strength and nature of immune insults. J Neurosci 2002; 22: 5606-5618.
74. Ek M, Arias C, Sawchenko P, Ericsson-Dahlstrand A. Distribution of the EP3 prostaglandin E(2) receptor subtype in the rat brain: Relationship to sites of interleukin-1-induced cellular responsiveness. J Comp Neurol 2000; 428: 5-20.
75. Zhang J, Rivest S. A functional analysis of EP4 receptor-expressing neurons in mediating the action of prostaglandin E2 within specific nuclei of the brain in response to circulating interleukin-1beta. J Neurochem 2000; 74: 2134-2145.
76. Fekete C, Singru PS, Sarkar S, Rand WM, Lechan RM. Ascending brainstem pathways are not involved in lipopolysaccharide-induced suppression of thyrotropin-releasing hormone gene expression in the hypothalamic paraventricular nucleus. Endocrinology 2005; 146: 1357-1363.
77. Schiltz JC, Sawchenko PE. Specificity and generality of the involvement of catecholaminergic afferents in hypothalamic responses to immune insults. J Comp Neurol 2007; 502: 455-467.
78. Kakucska I, Romero LI, Clark BD, Rondeel JM, Qi Y, Alex S, Emerson CH, Lechan RM. Suppression of thyrotropin-releasing hormone gene expression by interleukin-1-beta in the rat: Implications for nonthyroidal illness. Neuroendocrinology 1994; 59: 129-137.
79. Perez Castro C, Penalva R, Paez Pereda M, Renner U, Reul JM, Stalla GK, Holsboer F, Arzt E. Early activation of thyrotropin-releasing-hormone and prolactin plays a critical role during a T cell-dependent immune response. Endocrinology 1999; 140: 690-697.
80. Serrats J, Sawchenko PE. CNS activational responses to staphylococcal enterotoxin B: T-lymphocyte-dependent immune challenge effects on stress-related circuitry. J Comp Neurol 2006; 495: 236-254.
81. Uribe RM, Redondo JL, Charli JL, Joseph-Bravo P. Suckling and cold stress rapidly and transiently increase TRH mRNA in the paraventricular nucleus. Neuroendocrinology 1993; 58: 140-145.
82. Zoeller RT, Kabeer N, Albers HE. Cold exposure elevates cellular levels of messenger ribonucleic acid encoding thyrotropin-releasing hormone in paraventricular nucleus despite elevated levels of thyroid hormones. Endocrinology 1990; 127: 2955-2962.
83. Rondeel JM, de Greef WJ, Hop WC, Rowland DL, Visser TJ. Effect of cold exposure on the hypothalamic release of thyrotropin-releasing hormone and catecholamines. Neuroendocrinology 1991; 54: 477-481.
84. Baffi JS, Palkovits M. Fine topography of brain areas activated by cold stress. A fos immunohistochemical study in rats. Neuroendocrinology 2000; 72: 102-113.
85. Plotsky PM, Vale W. Hemorrhage-induced secretion of corticotropin-releasing factor-like immunoreactivity into the rat hypophysial portal circulation and its inhibition by glucocorticoids. Endocrinology 1984; 114: 164-169.
86. Chan RK, Brown ER, Ericsson A, Kovacs KJ, Sawchenko PE. A comparison of two immediate-early genes, c-fos and NGFI-B, as markers for functional activation in stress-related neuroendocrine circuitry. J Neurosci 1993; 13: 5126-5138.
87. Chan RK, Sawchenko PE. Spatially and temporally differentiated patterns of c-fos expression in brainstem catecholaminergic cell groups induced by cardiovascular challenges in the rat. J Comp Neurol 1994; 348: 433-460.
88. Chan RK, Sawchenko PE. Hemodynamic regulation of tyrosine hydroxylase messenger RNA in medullary catecholamine neurons: A c-fos-guided hybridization histochemical study. Neuroscience 1995; 66: 377-390.
89. Chan RK, Sawchenko PE. Differential time- and dose-related effects of haemorrhage on tyrosine hydroxylase and neuropeptide Y mRNA expression in medullary catecholamine neurons. Eur J Neurosci 1998; 10: 3747-3758.
90. Card JP, Sved JC, Craig B, Raizada M, Vazquez J, Sved AF. Efferent projections of rat rostroventrolateral medulla C1 catecholamine neurons: implications for the central control of cardiovascular regulation. J Comp Neurol 2006; 499: 840-859.
91. Stornetta RL, Akey PJ, Guyenet PG. Location and electrophysiological characterization of rostral medullary adrenergic neurons that contain neuropeptide Y mRNA in rat medulla. J Comp Neurol 1999; 415: 482-500.
92. Verberne AJ, Stornetta RL, Guyenet PG. Properties of C1 and other ventrolateral medullary neurones with hypothalamic projections in the rat. J Physiol 1999; 517: 477-494.
93. Haselton JR, Guyenet PG. Ascending collaterals of medullary barosensitive neurons and C1 cells in rats. Am J Physiol 1990; 258: R1051-R1063.
94. Chan RK, Sawchenko PE. Organization and transmitter specificity of medullary neurons activated by sustained hypertension: Implications for understanding baroreceptor reflex circuitry. J Neurosci 1998; 18: 371-387.
95. Dayas CV, Buller KM, Crane JW, Xu Y, Day TA. Stressor categorization: acute physical and psychological stressors elicit distinctive recruitment patterns in the amygdala and in medullary noradrenergic cell groups. Eur J Neurosci 2001; 14: 1143-1152.
96. Li HY, Sawchenko PE. 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 1998; 393: 244-266.
97. Buller K, Xu Y, Dayas C, Day T. Dorsal and ventral medullary catecholamine cell groups contribute differentially to systemic interleukin-1beta-induced hypothalamic pituitary adrenal axis responses. Neuroendocrinology 2001; 73: 129-138.
98. Rinaman L, Hoffman GE, Dohanics J, Le WW, Stricker EM, Verbalis JG. Cholecystokinin activates catecholaminergic neurons in the caudal medulla that innervate the paraventricular nucleus of the hypothalamus in rats. J Comp Neurol 1995; 360: 246-256.