Role of the hypothalamic arcuate nucleus in cardiovascular regulation

Autonomic Neuroscience: Basic and Clinical

Volumn 175, Issue 1-2, 2013, Pages 38-50

  Sapru, Hreday N ^a  

^a RUTGERS NEW JERSEY MEDICAL SCHOOL   (United States)

Author keywords

Angiotensin II; Angiotensin (1 12); Blood pressure; Insulin; Leptin; Sympathetic nerve activity

Indexed keywords

4 AMINOBUTYRIC ACID A RECEPTOR; ADENOSINE TRIPHOSPHATE; ALPHA INTERMEDIN; ANGIOTENSIN II; BETA ENDORPHIN; COCAINE AND AMPHETAMINE REGULATED TRANSCRIPT PEPTIDE; CORTICOTROPIN; GLUCOSE; INSULIN; IONOTROPIC RECEPTOR; LEPTIN; LEPTIN RECEPTOR; NEUROPEPTIDE Y1 RECEPTOR; OPIATE RECEPTOR; PROOPIOMELANOCORTIN;

ARCUATE NUCLEUS; BLOOD BRAIN BARRIER; CARDIOVASCULAR EFFECT; CARDIOVASCULAR FUNCTION; CARDIOVASCULAR RESPONSE; DEPRESSOR RESPONSE; ELECTROACUPUNCTURE; GLUCOSE BLOOD LEVEL; HEART EXCITATION; HUMAN; HYPOGLYCEMIA; HYPOTHALAMIC PARAVENTRICULAR NUCLEUS; MICROINJECTION; NERVE CELL STIMULATION; NERVE CONDUCTION; NERVE PROJECTION; NONHUMAN; PHENOTYPE; PRESSOR RESPONSE; PRIORITY JOURNAL; REGULATORY MECHANISM; REVIEW; SIGNAL TRANSDUCTION; STIMULATION; SYMPATHETIC NERVE; SYMPATHETIC TONE; TACHYCARDIA; TRANSCYTOSIS; VAGUS NERVE STIMULATION;

ANIMALS; ARCUATE NUCLEUS; CARDIOVASCULAR PHYSIOLOGICAL PROCESSES; HUMANS; SYMPATHETIC NERVOUS SYSTEM;

EID: 84877069100     PISSN: 15660702     EISSN: 18727484     Source Type: Journal    
DOI: 10.1016/j.autneu.2012.10.016     Document Type: Review

References (134)

1. Albers H.E., Ottenweller J.E., Liou S.Y., Lumpkin M.D., Anderson E.R. Neuropeptide Y in the hypothalamus: effect on corticosterone and single-unit activity. Am. J. Physiol. Regul. Integr. Comp. Physiol. 1990, 258:R376-R382.
2. Arakawa H., Chitravanshi V.C., Sapru H.N. Hypothalamic arcuate nucleus: a new site of cardiovascular action of angiotensin-(1-12) and angiotensin II. Am. J. Physiol. Heart Circ. Physiol. 2011, 300:H951-H960.
3. Arakawa, H., Kawabe, K., Sapru, H.N., in press. Angiotensin-(1-12) in the rostral ventrolateral medullary pressor area of the rat elicits sympathoexcitatory responses. Exp. Physiol. (Published on line on June 15).
4. Arnold A.C., Isa K., Shaltout H.A., Nautiyal M., Ferrario C.M., Chappell M.C., Diz D.I. Angiotensin-(1-12) requires angiotensin converting enzyme and AT1 receptors for cardiovascular actions within the solitary tract nucleus. Am. J. Physiol. Heart Circ. Physiol. 2010, 299:H763-H771.
5. Badoer E. Hypothalamic paraventricular nucleus and cardiovascular regulation. Clin. Exp. Pharmacol. Physiol. 2001, 28:95-99.
6. Banks W.A., Kastin A.J., Huang W., Jaspan J.B., Maness L.M. Leptin enters the brain by a saturable system independent of insulin. Peptides 1996, 17:305-311.
7. Banks A.S., Davis S.M., Bates S.M., Myers M.G. Activation of downstream signals by the long form of the leptin receptor. J. Biol. Chem. 2000, 275:14563-14572.
8. Belgardt B.F., Okamura T., Bruning J.C. Hormone and glucose signalling in POMC and AgRP neurons. J. Physiol. 2009, 587:5305-5314.
9. Bleier R., Byne W. Septum and hypothalamus. The Rat Nervous System 1985, 87-118. Academic Press, Australia. G. Paxinos (Ed.).
10. Broadwell R.D., Brightman M.W. Entry of peroxidase into neurons of the central and peripheral nervous systems from extracerebral and cerebral blood. J. Comp. Neurol. 1976, 166:257-283.
11. Brody M.J., O'Neill T.P., Porter J.P. Role of paraventricular and arcuate nuclei in cardiovascular regulation. Central and Peripheral Mechanisms of Cardiovascular Regulation 1986, 443-464. Plenum Press, New York, U.S.A. A. Magro, W. Osswald, D. Reis, P. Vanhoutte (Eds.).
12. Burguera B., Couce M.E., Curran G.L., Jensen M.D., Lloyd R.V., Cleary M.P., Poduslo J.F. Obesity is associated with a decreased leptin transport across the blood-brain barrier in rats. Diabetes 2000, 49:1219-1223.
13. Carpenter M.B., Sutin J. Human Neuroanatomy 1983, Williams and Wilkins, Baltimore, MD, USA, 557 pp. 8th ed.
14. Cassaglia P.A., Hermes S.M., Aicher S.A., Brooks V.L. Insulin acts in the arcuate nucleus to increase lumbar sympathetic nerve activity and baroreflex function in rats. J. Physiol. 2011, 589:1643-1662.
15. Cechetto D.F., Saper C.B. Neurochemical organization of the hypothalamic projection to spinal cord in the rat. J. Comp. Neurol. 1988, 272:579-604.
16. Chen H., Charlat O., Tartaglia L.A., Woolf E.A., Weng X., Ellis S.J., Lakey N.D., Culpepper J., Moore K.J., Breitbart R.E., Duyk G.M., Tepper R.I., Morgenstern J.P. Evidence that the diabetes gene encodes the leptin receptor: identification of a mutation in the leptin receptor gene in db/db mice. Cell 1996, 84:491-495.
17. Chen Q.H., Haywood J.R., Toney G.M. Sympathoexcitation by PVN-injected bicuculline requires activation of excitatory amino acid receptors. Hypertension 2003, 42:725-731.
18. Chitravanshi V.C., Sapru H.N. Cardiovascular responses elicited by a new endogenous angiotensin in the nucleus tractus solitarius of the rat. Am. J. Physiol. Heart Circ. Physiol. 2011, 300:H230-H240.
19. Chitravanshi V.C., Proddutur A., Sapru H.N. Cardiovascular responses to angiotensin-(1-12) in the hypothalamic paraventricular nucleus of the rat are mediated via angiotensin II. Exp. Physiol. 2012, 97:1001-1017.
20. Chronwall B.M. Anatomy and physiology of the neuroendocrine arcuate nucleus. Peptides 1985, 6(Suppl. 2):1-11.
21. Ciofi P. The arcuate nucleus as a circumventricular organ in the mouse. Neurosci. Lett. 2011, 487:187-190.
22. Ciofi P., Garret M., Lapirot O., Lafon P., Loyens A., Prevot V., Levine J.E. Brain-endocrine interactions: a microvascular route in the mediobasal hypothalamus. Endocrinology 2009, 150:5509-5519.
23. Ciriello J., McMurray J.C., Babic T., de Oliveira C.V.R. Collateral axonal projections from hypothalamic hypocretin neurons to cardiovascular sites in nucleus ambiguus and nucleus tractus solitarius. Brain Res. 2003, 991:133-141.
24. Coote J.H. The hypothalamus and cardiovascular regulation. Neural Mechanisms Of Cardiovascular Regulation 2004, 117-146. Kluwer Academic Publishers, Boston, MA, USA. N.J. Dun, B.H. Machado, P.M. Pilowsky (Eds.).
25. Cowley M.A., Smart J.L., Rubinstein M., Cerdan M.G., Diano S., Horvath T.L., Cone R.D., Low M.J. Leptin activates anorexigenic POMC neurons through a neural network in the arcuate nucleus. Nature 2011, 411:480-484.
26. Dampney R.A. Arcuate nucleus - a gateway for insulin's action on sympathetic activity. J. Physiol. 2011, 589:2109-2110.
27. Dampney R.A., Horiuchi J., Killinger S., Sheriff M.J., Tan P.S., McDowall L.M. Long-term regulation of arterial blood pressure by hypothalamic nuclei: some critical questions. Clin. Exp. Pharmacol. Physiol. 2005, 32:419-425.
28. Davern P.J., Head G.A. Fos-related antigen immunoreactivity after acute and chronic angiotensin II-induced hypertension in the rabbit brain. Hypertension 2007, 49:1170-1177.
29. Dicken M.S., Tooker R.E., Hentges S.T. Regulation of GABA and glutamate release from proopiomelanocortin neuron terminals in intact hypothalamic networks. J. Neurosci. 2012, 32:4042-4048.
30. Donadio M.V., Gomes C.M., Sagae S.C., Franci C.R., Nselmo-Franci J.A., Lucion A.B., Sanvitto G.L. Estradiol and progesterone modulation of angiotensin II receptors in the arcuate nucleus of ovariectomized and lactating rats. Brain Res. 2006, 1083:103-109.
31. Dunbar J.C., Hu Y., Lu H. Intracerebroventricular leptin increases lumbar and renal sympathetic nerve activity and blood pressure in normal rats. Diabetes 1997, 46:2040-2043.
32. Elias C.F., Lee C., Kelly J., Aschkenasi C., Ahima R.S., Couceyro P.R., Kuhar M.J., Saper C.B., Elmquist J.K. Leptin activates hypothalamic CART neurons projecting to the spinal cord. Neuron 1998, 21:1375-1385.
33. Elmquist J.K., Elias C.F., Saper C.B. From lesions to leptin: hypothalamic control of food intake and body weight. Neuron 1999, 22:221-232.
34. Esler M., Rumantir M., Kaye D., Lambert G. The sympathetic neurobiology of essential hypertension: disparate influences of obesity, stress, and noradrenaline transporter dysfunction. Am. J. Hypertens. 2001, 14:139S-146S.
35. Ferguson A.V. Angiotensinergic regulation of autonomic and neuroendocrine outputs: critical roles for the subfornical organ and paraventricular nucleus. Neuroendocrinology 2009, 89:370-376.
36. Ferrario C.M., Varagic J., Habibi J., Nagata S., Kato J., Chappell M.C., Trask A.J., Kitamura K., Whaley-Connell A., Sowers J.R. Differential regulation of angiotensin-(1-12) in plasma and cardiac tissue in response to bilateral nephrectomy. Am. J. Physiol. Heart Circ. Physiol. 2009, 296:H1184-H1192.
37. Fuxe K., Tinner B., Caberlotto L., Bunnemann B., Agnati L.F. NPY Y1 receptor like immunoreactivity exists in a subpopulation of beta-endorphin immunoreactive nerve cells in the arcuate nucleus: a double immunolabelling analysis in the rat. Neurosci. Lett. 1997, 225:49-52.
38. Ghamari-Langroudi M. Electrophysiological analysis of circuits controlling energy homeostasis. Mol. Neurobiol. 2012, 45:258-278.
39. Grobe J.L., Xu D., Sigmund C.D. An intracellular renin-angiotensin system in neurons: fact, hypothesis, or fantasy. Physiology (Bethesda) 2008, 23:187-193.
40. Gross P.M. Circumventricular organ capillaries. Prog. Brain Res. 1992, 91:219-233.
41. Gruber K., Rae-Degueurce A., Wilkin L.D., Mitchell L.D., Johnson A.K. Forebrain and brainstem afferents to the arcuate nucleus in the rat: potential pathways for the modulation of hypophyseal secretions. Neurosci. Lett. 1987, 75:1-5.
42. Guyenet P.G. The sympathetic control of blood pressure. Nat. Rev. Neurosci. 2006, 7:335-346.
43. Gyurko R., Wielbo D., Phillips M.I. Antisense inhibition of AT1 receptor mRNA and angiotensinogen mRNA in the brain of spontaneously hypertensive rats reduces hypertension of neurogenic origin. Regul. Pept. 1993, 49:167-174.
44. Haynes W.G., Morgan D.A., Walsh S.A., Mark A.L., Sivitz W.I. Receptor-mediated regional sympathetic nerve activation by leptin. J. Clin. Invest. 1997, 100:270-278.
45. He S., Gaca M.D., McEuen A.R., Walls A.F. Inhibitors of chymase as mast cell-stabilizing agents: contribution of chymase in the activation of human mast cells. J. Pharmacol. Exp. Ther. 1999, 291:517-523.
46. Hentges S.T., Otero-Corchon V., Pennock R.L., King C.M., Low M.J. Proopiomelanocortin expression in both GABA and glutamate neurons. J. Neurosci. 2009, 29:13684-13690.
47. Holstege G. Some anatomical observations on the projections from the hypothalamus to brainstem and spinal cord: an HRP and autoradiographic tracing study in the cat. J. Comp. Neurol. 1987, 260:98-126.
48. Horvath T.L., Bechmann I., Naftolin F., Kalra S.P., Leranth C. Heterogeneity in the neuropeptide Y-containing neurons of the rat arcuate nucleus: GABAergic and non-GABAergic subpopulations. Brain Res. 1997, 756:283-286.
49. Huang J., Hara Y., Anrather J., Speth R.C., Iadecola C., Pickel V.M. Angiotensin II subtype 1A (AT1A) receptors in the rat sensory vagal complex: Subcellular localization and association with endogenous angiotensin. Neuroscience 2003, 122:21-36.
50. Ibata Y., Kawakami F., Okamura H., Obata-Tsuto H.L., Morimoto N. Light and electron microscopic immunocytochemistry of beta-endorphin/beta-LPH-like immunoreactive neurons in the arcuate nucleus and surrounding areas of the rat hypothalamus. Brain Res. 1985, 341:233-242.
51. Isa K., Garcia-Espinosa M.A., Arnold A.C., Pirro N.T., Tommasi E.N., Ganten D., Chappell M.C., Ferrario C.M., Diz D.I. Chronic immunoneutralization of brain angiotensin-(1-12) lowers blood pressure in transgenic (mRen2)27 hypertensive rats. Am. J. Physiol. Regul. Integr. Comp. Physiol. 2009, 297:R111-R115.
52. Kannan H., Niijima A., Yamashita H. Effects of stimulation of the hypothalamic paraventricular nucleus on blood pressure and renal sympathetic nerve activity. Brain Res. Bull. 1988, 20:779-783.
53. Kastin A.J., Pan W., Maness L.M., Koletsky R.J., Emsberger P. Decreased transport of leptin across the blood-brain barrier in rats lacking the short form of the leptin receptor. Peptides 1999, 20:1449-1453.
54. Kawabe T., Chitravanshi V.C., Kawabe K., Sapru H.N. Cardiovascular function of a glutamatergic projection from the hypothalamic paraventricular nucleus to the nucleus tractus solitarius in the rat. Neuroscience 2008, 153:605-617.
55. Kawabe T., Chitravanshi V.C., Nakamura T., Kawabe K., Sapru H.N. Mechanism of heart rate responses elicited by chemical stimulation of the hypothalamic paraventricular nucleus in the rat. Brain Res. 2009, 1248:115-126.
56. Kawabe T., Kawabe K., Sapru H.N. Cardiovascular responses to chemical stimulation of the hypothalamic arcuate nucleus in the rat: Role of the hypothalamic paraventricular nucleus. PLoS One 2012, 7:e45180. (1-12). 10.1371/journal.pone.0045180.
57. Kawabe, T., Kawabe, K., Sapru, H.N., in press. Effect of barodenervation on cardiovascular responses elicited from the hypothalamic arcuate nucleus of the rat. PLoS One (published on line on Dec. 27).
58. Kow L.M., Pfaff D.W. Responses of hypothalamic paraventricular neurons in vitro to norepinephrine and other feeding-relevant agents. Physiol. Behav. 1989, 46:265-271.
59. Lantos T.A., Gorcs T.J., Palkovits M. Immunohistochemical mapping of neuropeptides in the premamillary region of the hypothalamus in rats. Brain Res. Rev. 1995, 20:209-249.
60. Lark L.A., Weyhenmeyer J.A. The antihypertensive effect of acute intracerebroventricular administration of captopril in Dahl salt-sensitive rats. Eur. J. Pharmacol. 1992, 222:33-37.
61. Lee G.H., Proenca R., Montez J.M., Carroll K.M., Darvishzadeh J.G., Lee J.I., Friedman J.M. Abnormal splicing of the leptin receptor in diabetic mice. Nature 1996, 379:632-635.
62. Li S.J., Scanlon M.N., Jarai Z., Varga K., Gantenberg N.S., Lazar-Wesley E., Kunos G. Alpha-2-Adrenergic activation of proopiomelanocortin-containing neurons in the arcuate nucleus causes opioid-mediated hypotension and bradycardia. Neuroendocrinology 1996, 63:275-283.
63. Li C., Chen P., Smith M.S. Neuropeptide Y (NPY) neurons in the arcuate nucleus (ARH) and dorsomedial nucleus (DMH), areas activated during lactation, project to the paraventricular nucleus of the hypothalamus (PVH). Regul. Pept. 1998, 75-76:93-100.
64. Li P., Tjen-A-Looi S.C., Longhurst J.C. Excitatory projections from arcuate nucleus to ventrolateral periaqueductal gray in electroacupuncture inhibition of cardiovascular reflexes. Am. J. Physiol. Heart Circ. Physiol. 2006, 290:H2535-H2542.
65. Li Y.F., Jackson K.L., Stern J.E., Rabeler B., Patel K.P. Interaction between glutamate and GABA systems in the integration of sympathetic outflow by the paraventricular nucleus of hypothalamus. Am. J. Physiol. Heart Circ. Physiol. 2006, 291:H2847-H2856.
66. Li P., Tjen-A-Looi S.C., Guo Z.L., Fu L.W., Longhurst J.C. Long-loop pathways in cardiovascular electroacupuncture responses. J. Appl. Physiol. 2009, 106:620-630.
67. Li P., Tjen-A-Looi S.C., Longhurst J.C. Nucleus raphe pallidus participates in midbrain-medullary cardiovascular sympathoinhibition during electroacupuncture. Am. J. Physiol. Regul. Integr. Comp. Physiol. 2010, 299:R1369-R1376.
68. Lind R.W., Swanson L.W., Ganten D. Organization of angiotensin II immunoreactive cells and fibers in the rat central nervous system: an immunohistochemical study. Neuroendocrinology 1985, 40:2-24.
69. Lochard N., Silversides D.W., van Kats J.P., Mercure C., Reudelhuber T.L. Brain-specific restoration of angiotensin II corrects renal defects seen in angiotensinogen-deficient mice. J. Biol. Chem. 2003, 278:2184-2189.
70. Marks J.L., Porte D., Stahl W.L., Baskin D.G. Localization of insulin receptor mRNA in rat brain by in situ hybridization. Endocrinology 1990, 127:3234-3236.
71. Mastrianni J.A., Palkovits M., Kunos G. Activation of brainstem endorphinergic neurons causes cardiovascular depression and facilitates baroreflex bradycardia. Neuroscience 1989, 33:559-566.
72. Meister B. Neurotransmitters in key neurons of the hypothalamus that regulate feeding behavior and body weight. Physiol. Behav. 2007, 92:263-271.
73. Montanaro M.S., Allen A.M., Oldfield B.J. Structural and functional evidence supporting a role for leptin in central neural pathways influencing blood pressure in rats. Exp. Physiol. 2005, 90:689-696.
74. Morgan D.A., Balon T.W., Ginsberg B.H., Mark A.L. Nonuniform regional sympathetic nerve responses to hyperinsulinemia in rats. Am. J. Physiol. Regul. Integr. Comp. Physiol. 1993, 264:R423-R427.
75. Morimoto S., Cassell M.D., Beltz T.G., Johnson A.K., Davisson R.L., Sigmund C.D. Elevated blood pressure in transgenic mice with brain-specific expression of human angiotensinogen drive by the glial fibrillary acidic protein promoter. Circ. Res. 2001, 89:365-372.
76. Morimoto S., Cassell M.D., Sigmund C.D. Glia-and neuron-specific expression of the renin-angiotensin system in brain alters blood pressure, water intake, and salt preference. J. Biol. Chem. 2002, 277:33235-33241.
77. Morton G.J., Cummings D.E., Baskin D.G., Barsh G.S., Schwartz M.W. Central nervous system control of food intake and body weight. Nature 2006, 443:289-295.
78. Mullier A., Bouret S.G., Prevot V., Dehouck B. Differential distribution of tight junction proteins suggests a role for tanycytes in blood-hypothalamus barrier regulation in the adult mouse brain. J. Comp. Neurol. 2010, 518:943-962.
79. Muntzel M.S., Morgan D.A., Mark A.L., Johnson A.K. Intracerebroventricular insulin produces nonuniform regional increases in sympathetic nerve activity. Am. J. Physiol. Regul. Integr. Comp. Physiol. 1994, 267:R1350-R1355.
80. Nagata S., Kato J., Sasaki K., Minamino N., Eto T., Kitamura K. Isolation and identification of proangiotensin-12, a possible component of the renin-angiotensin system. Biochem. Biophys. Res. Commun. 2006, 350:1026-1031.
81. Nakamura T., Bhatt S., Sapru H.N. Cardiovascular responses to hypothalamic arcuate nucleus stimulation in the rat: role of sympathetic and vagal efferents. Hypertension 2009, 54:1369-1375.
82. Nicholson C. Diffusion from an injected volume of a substance in brain tissue with arbitrary volume fraction and tortuosity. Brain Res. 1985, 333:325-329.
83. Nishimura M., Milsted A., Block C.H., Brosnihan K.B., Ferrario C.M. Tissue renin-angiotensin systems in renal hypertension. Hypertension 1992, 20:158-167.
84. Norsted E., Gomuc B., Meister B. Protein components of the blood-brain barrier (BBB) in the mediobasal hypothalamus. J. Chem. Neuroanat. 2008, 36:107-121.
85. Okada M., Bunag R.D. Insulin acts centrally to enhance reflex tachycardia in conscious rats. Am. J. Physiol. Regul. Integr. Comp. Physiol. 1994, 266:R481-R486.
86. Ovesjo M.L., Gamstedt M., Collin M., Meister B. GABAergic nature of hypothalamic leptin target neurones in the ventromedial arcuate nucleus. J. Neuroendocrinol. 2001, 13:505-516.
87. Palkovits M., Mezey E., Fodor M., Ganten D., Bahner U., Geiger H., Heidland A. Neurotransmitters and neuropeptides in the baroreceptor reflex arc: connections between the nucleus of the solitary tract and the ventrolateral medulla oblongata in the rat. Clin. Exp. Hypertens. 1995, 17:101-113.
88. Paxinos G., Watson C. The Rat Brain in Stereotaxic Coordinates 2007, Academic Press, London. 6th ed.
89. Penicaud L., Meillon S., Brondel L. Leptin and the central control of feeding behavior. Biochimie 2012, 94:2069-2074.
90. Pennock R.L., Hentges S.T. Differential expression and sensitivity of presynaptic and postsynaptic opioid receptors regulating hypothalamic proopiomelanocortin neurons. J. Neurosci. 2011, 31:281-288.
91. Peruzzo B., Pastor F.E., Blazquez J.L., Amat P., Rodriguez E.M. Polarized endocytosis and transcytosis in the hypothalamic tanycytes of the rat. Cell Tissue Res. 2004, 317:147-164.
92. Pickel V.M., Chan J. Co-localization of angiotensin II and gamma-aminobutyric acid in axon terminals in the rat subfornical organ. Neurosci. Lett. 1995, 193:89-92.
93. Pilowsky P.M., Lung M.S., Spirovski D., McMullan S. Differential regulation of the central neural cardiorespiratory system by metabotropic neurotransmitters. Philos. Trans. R. Soc. B-Biol. Sci. 2009, 364:2537-2552.
94. Pochiero M., Nicoletta P., Losi E., Bianchi A., Caputi A.P. Cardiovascular responses of conscious DOCA-salt hypertensive rats to acute intracerebroventricular and intravenous administration of captopril. Pharmacol. Res. Commun. 1983, 15:173-182.
95. Pricher M.P., Freeman K.L., Brooks V.L. Insulin in the brain increases gain of baroreflex control of heart rate and lumbar sympathetic nerve activity. Hypertension 2008, 51:514-520.
96. Pritchard L.E., Turnbull A.V., White A. Pro-opiomelanocortin processing in the hypothalamus: impact on melanocortin signaling and obesity. J. Endocrinol. 2002, 172:411-421.
97. Pyner S., Coote J.H. Identification of an efferent projection from the paraventricular nucleus of the hypothalamus terminating close to spinally projecting rostral ventrolateral medullary neurons. Neuroscience 1999, 88:949-957.
98. Pyner S., Coote J.H. Identification of branching paraventricular neurons of the hypothalamus that project to the rostroventrolateral medulla and spinal cord. Neuroscience 2000, 100:549-556.
99. Rahmouni K., Morgan D.A. Hypothalamic arcuate nucleus mediates the sympathetic and arterial pressure responses to leptin. Hypertension 2007, 49:647-652.
100. Riediger T., Giannini P., Erguven E., Lutz T. Nitric oxide directly inhibits ghrelin-activated neurons of the arcuate nucleus. Brain Res. 2006, 1125:37-45.
101. Rosas-Arellano M.P., Solano-Flores L.P., Ciriello J. Effect of arcuate nucleus activation on neuronal activity in subfornical organ. Brain Res. 1993, 619:352-356.
102. Rosas-Arellano M.P., Solano-Flores L.P., Ciriello J. Glutamate stimulation of arcuate nucleus inhibits responses of subfornical organ neurons to plasma hypernatremia and angiotensin II. Neurosci. Lett. 1995, 198:201-204.
103. Rosas-Arellano M.P., Solano-Flores L.P., Ciriello J. Arcuate nucleus inputs onto subfornical organ neurons that respond to plasma hypernatremia and angiotensin II. Brain Res. 1996, 707:308-313.
104. Routh V.H. Glucose-sensing neurons: are they physiologically relevant?. Physiol. Behav. 2002, 76:403-413.
105. Routh V.H. Glucose sensing neurons in the ventromedial hypothalamus. Sensors (Basel) 2010, 10:9002-9025.
106. Sakai K., Agassandian K., Morimoto S., Sinnayah P., Cassell M.D., Davisson R.L., Sigmund C.D. Local production of angiotensin II in the subfornical organ causes elevated drinking. J. Clin. Invest. 2007, 117:1088-1095.
107. Sanchez-Lasheras C., Konner A.C., Bruning J.C. Integrative neurobiology of energy homeostasis-neurocircuits, signals and mediators. Front. Neuroendocrinol. 2010, 31:4-15.
108. Sapru H.N. Glutamate circuits in selected medullo-spinal areas regulating cardiovascular function. Clin. Exp. Pharmacol. Physiol. 2002, 29:491-496.
109. Sapru H.N. Neurotransmitters in the nucleus tractus solitarius mediating cardiovascular function. Neural Mechanisms of Cardiovascular Regulation 2004, 81-98. Kluwer Academic Publishers, Boston, MA, USA. N.J. Dun, B.H. Machado, P.M. Pilowsky (Eds.).
110. Schultz H.D., Li Y.L., Ding Y. Arterial chemoreceptors and sympathetic nerve activity: implications for hypertension and heart failure. Hypertension 2007, 50:6-13.
111. Schulz M., Engelhardt B. The circumventricular organs participate in the immunopathogenesis of experimental autoimmune encephalomyelitis. Cerebrospinal Fluid Res. 2005, 2:8. 10.1186/1743-8454-2-8.
112. Schwartz M.W., Woods S.C., Porte D., Seeley R.J., Baskin D.G. Central nervous system control of food intake. Nature 2000, 404:661-671.
113. Shek E.W., Brands M.W., Hall J.E. Chronic leptin infusion increases arterial pressure. Hypertension 1998, 31:409-414.
114. Siegel A., Sapru H.N. Essential Neuroscience 2011, 427-443. Kluwer Academic Publishers, Boston, MA, USA. 2nd ed.
115. Sim L.J., Joseph S.A. Arcuate nucleus projections to brainstem regions which modulate nociception. J. Chem. Neuroanat. 1991, 4:97-109.
116. Stern J. Cellular properties of autonomic-related neurons in the paraventricular nucleus of the hypothalamus. Neural Mechanisms of Cardiovascular Regulation 2004, 147-161. Kluwer Academic Publishers, Boston, MA, U.S.A. N.J. Dun, B.H. Machado, P.M. Pilowsky (Eds.).
117. Sundaram K., Sapru H.N. NMDA receptors in the intermediolateral column of the spinal cord mediate sympathoexcitatory responses elicited from the ventrolateral medullary pressor area. Brain Res. 1991, 544:33-41.
118. Tartaglia L.A. The leptin receptor. J. Biol. Chem. 1997, 272:6093-6096.
119. Tjen-A-Looi S.C., Li P., Longhurst J.C. Role of medullary GABA, opioids, and nociceptin in prolonged inhibition of cardiovascular sympathoexcitatory reflexes during electroacupuncture in cats. Am. J. Physiol. Heart Circ. Physiol. 2007, 293:H3627-H3635.
120. Tjen-A-Looi S.C., Li P., Longhurst J.C. Processing cardiovascular information in the vlPAG during electroacupuncture in rats: roles of endocannabinoids and GABA. J. Appl. Physiol. 2009, 106:1793-1799.
121. Trask A.J., Jessup J.A., Chappell M.C., Ferrario C.M. Angiotensin-(1-12) is an alternate substrate for angiotensin peptide production in the heart. Am. J. Physiol. Heart Circ. Physiol. 2008, 294:H2242-H2247.
122. Van den Pol A.N., Cassidy J.R. The hypothalamic arcuate nucleus of rat - a quantitative Golgi analysis. J. Comp. Neurol. 1982, 204:65-98.
123. Varagic J., Trask A.J., Jessup J.A., Chappell M.C., Ferrario C.M. New angiotensins. J. Mol. Med. 2008, 86:663-671.
124. Veerasingham S.J., Raizada M.K. Brain renin-angiotensin system dysfunction in hypertension: recent advances and perspectives. Brit. J. Pharmacol. 2003, 139:191-202.
125. Werther G.A., Hogg A., Oldfield B.J., McKinley M.J., Figdor R., Allen A.M., Mendelsohn F.A. Localization and characterization of insulin receptors in rat brain and pituitary gland using in vitro autoradiography and computerized densitometry. Endocrinology 1987, 121:1562-1570.
126. Wiegand S.J., Price J.L. Cells of origin of the afferent fibers to the median eminence in the rat. J. Comp. Neurol. 1980, 192:1-19.
127. Willette R.N., Krieger A.J., Barcas P.P., Sapru H.N. Medullary GABA receptors and the regulation of blood pressure in the rat. J. Pharmacol. Exp. Ther. 1983, 226:893-899.
128. Willette R.N., Barcas P.P., Krieger A.J., Sapru H.N. Endogenous GABAergic mechanisms in the medulla and the regulation of blood pressure. J. Pharmacol. Exp. Ther. 1984, 230:34-39.
129. Yang Z., Coote J.H. Influence of the hypothalamic paraventricular nucleus on cardiovascular neurons in the rostral ventrolateral medulla of the rat. J. Physiol. 1998, 513:521-530.
130. Yang Z., Bertram D., Coote J.H. The role of glutamate and vasopressin in the excitation of RVL neurones by paraventricular neurones. Brain Res. 2001, 908:99-103.
131. Yang Z., Wheatley M., Coote J.H. Neuropeptides, amines and amino acids as mediators of the sympathetic effects of paraventricular nucleus activation in the rat. Exp. Physiol. 2002, 87:663-674.
132. Zheng H., Li Y., Wang W., Patel K.P. Enhanced angiotensin-mediated excitation of renal sympathetic nerve activity within the paraventricular nucleus of anesthetized rats with heart failure. Am. J. Physiol. Regul. Integr. Comp. Physiol. 2009, 297:R1364-R1374.
133. Zhou W., Longhurst J.C. Neuroendocrine mechanisms of acupuncture in the treatment of hypertension. Evid. Based Complement. Alternat. Med. 2012, 2012:1-9.
134. Zhu G.Q., Lie G., Patel K.M., Zucker I.H., Wang W. ANG II in the paraventricular nucleus potentiates the cardiac sympathetic afferent reflex in rats with heart failure. J. Appl. Physiol. 2004, 97:1746-1754.