Sweet talk in the brain: Glucosensing, neural networks, and hypoglycemic counterregulation

Frontiers in Neuroendocrinology

Volumn 31, Issue 1, 2010, Pages 32-43

  Watts, Alan G ^a   Donovan, Casey M ^a  

^a UNIVERSITY OF SOUTHERN CALIFORNIA   (United States)

Author keywords

Autonomic; Behavioral; Cellular; Endocrine; Glucose

Indexed keywords

GLUCOSE;

ARCUATE NUCLEUS; BRAIN FUNCTION; CHEMOTAXIS; FOREBRAIN; GLUCOSE BLOOD LEVEL; GLUCOSE HOMEOSTASIS; HYPOGLYCEMIA; HYPOTHALAMUS; HYPOTHALAMUS NUCLEUS; HYPOTHALAMUS VENTROMEDIAL NUCLEUS; LATERAL HYPOTHALAMUS; MESENTERIC VEIN; NERVE CELL NETWORK; NERVOUS SYSTEM; NEUROMODULATION; NONHUMAN; PREMOTOR CORTEX; PRIORITY JOURNAL; REGULATORY MECHANISM; REVIEW; RHOMBENCEPHALON; SENSORIMOTOR CORTEX; SENSORIMOTOR INTEGRATION; SENSORY STIMULATION; THALAMUS MIDLINE NUCLEUS; ZONA INCERTA;

BLOOD GLUCOSE; BRAIN; GLUCOSE; HOMEOSTASIS; HUMANS; HYPOGLYCEMIA; MALE; MESENTERIC VEINS; NERVE NET; NEURONS; PORTAL VEIN;

EID: 72449146204     PISSN: 00913022     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.yfrne.2009.10.006     Document Type: Review

References (132)

1. Adachi A., Shimizu N., Oomura Y., and Kobáshi M. Convergence of hepatoportal glucose-sensitive afferent signals to glucose-sensitive units within the nucleus of the solitary tract. Neurosci. Lett. 46 (1984) 215-218
2. Anand B.K., and Brobeck J.R. Hypothalamic control of food intake in rats and cats. Yale J. Biol. Med. 24 (1951) 123-140
3. Anand B.K., Chhina G.S., Sharma K.N., Dua S., and Singh B. Activity of single neurons in the hypothalamic feeding centers: effect of glucose. Am. J. Physiol. 207 (1964) 1146-1154
4. Andrew S.F., Dinh T.T., and Ritter S. Localized glucoprivation of hindbrain sites elicits corticosterone and glucagon secretion. Am. J. Physiol. Regul. Integr. Comp. Physiol. 292 (2007) R1792-R1798
5. Balfour R.H., Hansen A.M., and Trapp S. Neuronal responses to transient hypoglycaemia in the dorsal vagal complex of the rat brainstem. J. Physiol. 570 (2006) 469-484
6. Barja F., and Mathison R. Adrenergic and peptidergic (substance P and vasoactive intestinal peptide) innervation of the rat portal vein. Blood Vessels 19 (1982) 263-272
7. Barja F., and Mathison R. Sensory innervation of the rat portal vein and the hepatic artery. J. Autonom. Nerv. Syst. 10 (1984) 117-125
8. Baskin D.G., Breininger J.F., and Schwartz M.W. Leptin receptor mRNA identifies a subpopulation of neuropeptide Y neurons activated by fasting in rat hypothalamus. Diabetes 48 (1999) 828-833
9. Bellinger L.L., and Bernardis L.L. The dorsomedial hypothalamic nucleus and its role in ingestive behavior and body weight regulation: lessons learned from lesioning studies. Physiol. Behav. 76 (2002) 431-442
10. Beverly J.L., de Vries M.G., Beverly M.F., and Arseneau L.M. Norepinephrine mediates glucoprivic-induced increase in GABA in the ventromedial hypothalamus of rats. Am. J. Physiol. Regul. Integr. Comp. Physiol. 279 (2000) R990-R996
11. Beverly J.L., de Vries M.G., Bouman S.D., and Arseneau L.M. Noradrenergic and GABAergic systems in the medial hypothalamus are activated during hypoglycemia. Am. J. Physiol. Regul. Integr. Comp. Physiol. 280 (2001) R563-R569
12. Bohland M.A., Khan A.M., Watts A.G., and Donovan C.M. Hypoglycemic activation of select hindbrain neurons is mediated by portal-mesenteric vein glucosensors. Diabetes 54 (2005) A27
13. Borg M.A., Sherwin R.S., Borg W.P., Tamborlane W.V., and Shulman G.I. Local ventromedial hypothalamus glucose perfusion blocks counterregulation during systemic hypoglycemia in awake rats. J. Clin. Invest. 99 (1997) 361-365
14. Borg W.P., During M.J., Sherwin R.S., Borg M.A., Brines M.L., and Shulman G.I. Ventromedial hypothalamic lesions in rats suppress counterregulatory responses to hypoglycemia. J. Clin. Invest. 93 (1994) 1677-1682
15. Brady L.S., Smith M.A., Gold P.W., and Herkenham M. Altered expression of hypothalamic neuropeptide mRNAs in food-restricted and food-deprived rats. Neuroendocrinology 52 (1990) 441-447
16. Broberger C., de Lecea L., Sutcliffe J.G., and Hökfelt T. Hypocretin/orexin- and melanin-concentrating hormone-expressing cells form distinct populations in the rodent lateral hypothalamus: relationship to the neuropeptide Y and agouti gene-related protein systems. J. Comp. Neurol. 402 (1998) 460-474
17. Broberger C., Johansen J., Johansson C., Schalling M., and Hökfelt T. The neuropeptide Y/agouti gene-related protein (AGRP) brain circuitry in normal, anorectic, and monosodium glutamate-treated mice. Proc. Natl. Acad. Sci. USA 95 (1998) 15043-15048
18. Buijs R.M., Chun S.J., Niijima A., Romijn H.J., and Nagai K. Parasympathetic and sympathetic control of the pancreas: a role for the suprachiasmatic nucleus and other hypothalamic centers that are involved in the regulation of food intake. J. Comp. Neurol. 431 (2001) 405-423
19. Buijs R.M., Wortel J., Van Heerikhuize J.J., Feenstra M.G., Ter Horst G.J., Romijn H.J., and Kalsbeek A. Anatomical and functional demonstration of a multisynaptic suprachiasmatic nucleus adrenal (cortex) pathway. Eur. J. Neurosci. 11 (1999) 1535-1544
20. Buijs R.M., la Fleur S.E., Wortel J., Van Heyningen C., Zuiddam L., Mettenleiter T.C., Kalsbeek A., Nagai K., and Niijima A. The suprachiasmatic nucleus balances sympathetic and parasympathetic output to peripheral organs through separate preautonomic neurons. J. Comp. Neurol. 464 (2003) 36-48
21. Canteras N.S., Simerly R.B., and Swanson L.W. Organization of projections from the ventromedial nucleus of the hypothalamus: a Phaseolus vulgaris-leucoagglutinin study in the rat. J. Comp. Neurol. 348 (1994) 41-79
22. Cardin S., Jackson P., Edgerton D., Neal D., Coffey C., and Cherrington A. Effect of vagal cooling on the counterregulatory response to hypoglycemia induced by a low dose of insulin in the concious dog. Diabetes 50 (2001) 558-564
23. Cechetto D.F., and Saper C.B. Neurochemical organization of the hypothalamic projection to the spinal cord in the rat. J. Comp. Neurol. 272 (1988) 579-604
24. Chan O., Zhu W., Ding Y., McCrimmon R.J., and Sherwin R.S. Blockade of GABA(A) receptors in the ventromedial hypothalamus further stimulates glucagon and sympathoadrenal but not the hypothalamo-pituitary-adrenal response to hypoglycemia. Diabetes 55 (2006) 1080-1087
25. Chan O., Cheng H., Herzog R., Czyzyk D., Zhu W., Wang A., McCrimmon R.J., Seashore M.R., and Sherwin R.S. Increased GABAergic tone in the ventromedial hypothalamus contributes to suppression of counterregulatory responses after antecedent hypoglycemia. Diabetes 57 (2008) 1363-1370
26. Cheung C.C., Clifton D.K., and Steiner R.A. Proopiomelanocortin neurons are direct targets for leptin in the hypothalamus. Endocrinology 138 (1997) 4489-4492
27. Clark J.T., Kalra P.S., Crowley W.R., and Kalra S.P. Neuropeptide Y and human pancreatic polypeptide stimulate feeding behavior in rats. Endocrinology 115 (1984) 427-429
28. Cryer P.E. Hierarchy of physiological responses to hypoglycemia: relevance to clinical hypoglycemia in type I (insulin dependent) diabetes mellitus. Horm. Metab. Res. 29 (1997) 92-96
29. Cunningham Jr. E.T., and Sawchenko P.E. Anatomical specificity of noradrenergic inputs to the paraventricular and supraoptic nuclei of the rat hypothalamus. J. Comp. Neurol. 274 (1988) 60-76
30. de Vries M.G., Arseneau L.M., Lawson M.A., and Beverly J.L. Extracellular glucose in rat ventromedial hypothalamus during acute and recurrent hypoglycemia. Diabetes 52 (2003) 2767-2773
31. de Vries M.G., Lawson M.A., and Beverly J.L. Dissociation of hypothalamic noradrenergic activity and sympathoadrenal responses to recurrent hypoglycemia. Am. J. Physiol. Regul. Integr. Comp. Physiol. 286 (2004) R910-R915
32. de Vries M.G., Lawson M.A., and Beverly J.L. Hypoglycemia-induced noradrenergic activation in the VMH is a result of decreased ambient glucose. Am. J. Physiol. Regul. Integr. Comp. Physiol. 289 (2005) R977-R981
33. DiRocco R.J., and Grill H.J. The forebrain is not essential for sympathoadrenal hyperglycemic response to glucoprivation. Science 204 (1979) 1112-1114
34. Donovan C., Hamilton-Wessler M., Halter J., and Bergman R. Primacy of liver glucosensors in the sympathetic response to progressive hypoglycemia. Proc. Natl. Acad. Sci. 91 (1994) 2863-2867
35. Elias C.F., Lee C., Kelly J., Aschkenasi C., Ahima R.S., Couceyro P.R., Kuhar M.J., Saper C.B., and Elmquist J.K. Leptin activates hypothalamic CART neurons projecting to the spinal cord. Neuron 21 (1998) 1375-1385
36. Elmquist J.K., Ahima R.S., Elias C.F., Flier J.S., and Saper C.B. Leptin activates distinct projections from the dorsomedial and ventromedial hypothalamic nuclei. Proc. Natl. Acad. Sci. USA 95 (1998) 741-746
37. Evans S.B., Wilkinson C.W., Gronbeck P., Bennett J.L., Zavosh A., Taborsky Jr G.J., and Figlewicz D.P. Inactivation of the DMH selectively inhibits the ACTH and corticosterone responses to hypoglycemia. Am. J. Physiol. Regul. Integr. Comp. Physiol. 286 (2004) R123-R128
38. Fujita S., and Donovan C.M. Celiac-superior mesenteric ganglionectomy, but not vagotomy, suppresses the sympathoadrenal response to insulin-induced hypoglycemia. Diabetes 54 (2005) 3258-3264
39. Fujita S., Bohland M.A., Sanchez-Watts G., Watts A.G., and Donovan C.M. Hypoglycemic detection at the portal vein is mediated by capsaicin-sensitive primary sensory neurons. Am. J. Physiol.: Endocrinol. Metab. 293 (2007) E96-E101
40. Funahashi M., and Adachi A. Glucose-responsive neurons exist within the area postrema of the rat: in vitro study on the isolated slice preparation. Brain Res. Bull. 32 (1993) 531-535
41. Fuxe K. Evidence for the existence of monoamine neurons in the central nervous system. IV. Distribution of monoamine nerve terminals in the central nervous system. Acta Physiol. Scand. Suppl. 247 (1965) 37-85
42. Füzesi T., Wittmann G., Liposits Z., Lechan R.M., and 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 148 (2007) 5442-5450
43. Goehler L., and Sternini C. Calcitonin gene-related peptide innervation of the rat hepatobiliary system. Peptides 17 (1996) 209-217
44. Gold R.M. Hypothalamic obesity: the myth of the ventromedial nucleus. Science 182 (1973) 488-490
45. Gorton L.M., Khan A.M., Bohland M.A., Sanchez-Watts G., Donovan C.M., and Watts A.G. A role for the forebrain in mediating time-of-day differences in glucocorticoid counterregulatory responses to hypoglycemia. Endocrinology 148 (2007) 6026-6039
46. Hallbeck M., Larhammar D., and Blomqvist A. Neuropeptide expression in rat paraventricular hypothalamic neurons that project to the spinal cord. J. Comp. Neurol. 433 (2001) 222-238
47. Haskell-Luevano C., Chen P., Li C., Chang K., Smith M.S., Cameron J.L., and Cone R.D. Characterization of the neuroanatomical distribution of agouti-related protein immunoreactivity in the rhesus monkey and the rat. Endocrinology 140 (1999) 1408-1415
48. Hevener A., Bergman R., and Donovan C. Novel glucosensor for hypoglycemic detention localized to the portal vein. Diabetes 46 (1997) 1521-1525
49. Hevener A., Bergman R., and Donovan C. Portal vein afferents are critical for hypoglycemic detection. Diabetes 49 (2000) 8-12
50. Jackson P., Cardin S., Coffey C., Neal D., Allen E., Penaloza A., Snead W., and Cherrington A. The effect of hepatic denervation on the counter-regulatory response to insulin-induced hypoglycemia in the dog. Am. J. Physiol. 279 (2000) E1249-E1257
51. Jansen A.S., Hoffman J.L., and Loewy A.D. CNS sites involved in sympathetic and parasympathetic control of the pancreas: a viral tracing study. Brain Res. 766 (1997) 29-38
52. Kalsbeek A., Ruiter M., la Fleur S.E., Van Heijningen C., and Buijs R.M. The diurnal modulation of hormonal responses in the rat varies with different stimuli. J. Neuroendocrinol. 15 (2003) 1144-1155
53. Kalsbeek A., Foppen E., Schalij I., Van Heijningen C., van der Vliet J., Fliers E., and Buijs R.M. Circadian control of the daily plasma glucose rhythm: an interplay of GABA and glutamate. PLoS One 3 (2008) e3194
54. Kelly A.B., and Watts A.G. The region of the pontine parabrachial nucleus is a major target of dehydration-sensitive CRH neurons in the rat lateral hypothalamic area. J. Comp. Neurol. 394 (1998) 48-63
55. Kerman I.A., Akil H., and Watson S.J. Rostral elements of sympatho-motor circuitry: a virally mediated transsynaptic tracing study. J. Neurosci. 26 (2006) 3423-3433
56. Kerman I.A., Bernard R., Rosenthal D., Beals J., Akil H., and Watson S.J. Distinct populations of presympathetic-premotor neurons express orexin or melanin-concentrating hormone in the rat lateral hypothalamus. J. Comp. Neurol. 505 (2007) 586-601
57. Kerman I.A., Enquist L.W., Watson S.J., and Yates B.J. Brainstem substrates of sympatho-motor circuitry identified using trans-synaptic tracing with pseudorabies virus recombinants. J. Neurosci. 23 (2003) 4657-4666
58. A.M. Khan, K.L. Rapp, T.A. Ponzio, G. Sanchez-Watts, A.G. Watts, Stimulus-, circuit- and intracellular-level determinants of MAP kinase and CREB activation in parvicellular hypothalamic paraventricular neurons, 865.23, Society for Neuroscience Meeting Planner, Online.
59. King B.M. The rise, fall, and resurrection of the ventromedial hypothalamus in the regulation of feeding behavior and body weight. Physiol. Behav. 87 (2006) 221-244
60. Kiritsy-Roy J.A., Appel N.M., Bobbitt F.G., and Van Loon G.R. Effects of mu-opioid receptor stimulation in the hypothalamic paraventricular nucleus on basal and stress-induced catecholamine secretion and cardiovascular responses. J. Pharmacol. Exp. Ther. 239 (1986) 814-822
61. Könner A.C., Janoschek R., Plum L., Jordan S.D., Rother E., Ma X., Xu C., Enriori P., Hampel B., Barsh G.S., Kahn C.R., Cowley M.A., Ashcroft F.M., and Brüning J.C. Insulin action in AgRP-expressing neurons is required for suppression of hepatic glucose production. Cell Metab. 5 (2007) 438-449
62. Kurose T., Seino Y., Nishi S., Tsuji K., Taminato T., Tsuda K., and Imura H. Mechanism of sympathetic neural regulation of insulin, somatostatin, and glucagon secretion. Am. J. Physiol. 258 (1990) E220-E227
63. Leibowitz S.F., Sladek C., Spencer L., and Tempel D. Neuropeptide Y, epinephrine and norepinephrine in the paraventricular nucleus: stimulation of feeding and the release of corticosterone, vasopressin and glucose. Brain Res. Bull. 21 (1988) 905-912
64. Levin B.E., Routh V.H., Kang L., Sanders N.M., and Dunn-Meynell A.A. Neuronal glucosensing: what do we know after 50 years. Diabetes 53 (2004) 2521-2528
65. Levin M.C., Sawchenko P.E., Howe P.R., Bloom S.R., and Polak J.M. Organization of galanin-immunoreactive inputs to the paraventricular nucleus with special reference to their relationship to catecholaminergic afferents. J. Comp. Neurol. 261 (1987) 562-582
66. Levine A.S., and Morley J.E. Neuropeptide Y: a potent inducer of consummatory behavior in rats. Peptides 5 (1984) 1025-1029
67. Loewy A.D. Forebrain nuclei involved in autonomic control. Prog. Brain Res. 87 (1991) 253-268
68. Lynch R.M., Tompkins L.S., Brooks H.L., Dunn-Meynell A.A., and Levin B.E. Localization of glucokinase gene expression in the rat brain. Diabetes 49 (2000) 693-700
69. Marks J.L., Porte Jr. D., Stahl W.L., and Baskin D.G. Localization of insulin receptor mRNA in rat brain by in situ hybridization. Endocrinology 127 (1990) 3234-3236
70. Marty N., Dallaporta M., and Thorens B. Brain glucose sensing, counterregulation, and energy homeostasis. Physiology 22 (2007) 241-251
71. Mayer J. Glucostatic mechanism of regulation of food intake. New Engl. J. Med. 249 (1953) 13-16
72. Millhouse O.E. The organization of the ventromedial hypothalamic nucleus. Brain Res. 55 (1973) 71-87
73. Mizuno Y., and Oomura Y. Glucose responding neurons in the nucleus tractus solitarius of the rat: in vitro study. Brain Res. 307 (1984) 109-116
74. Moga M.M., Saper C.B., and Gray T.S. Neuropeptide organization of the hypothalamic projection to the parabrachial nucleus in the rat. J. Comp. Neurol. 295 (1990) 662-682
75. Moore R.Y., and Bloom F.E. Central catecholamine neuron systems: anatomy and physiology of the norepinephrine and epinephrine systems. Annu. Rev. Neurosci. 2 (1979) 13-68
76. Motawei K., Pyner S., Ranson R.N., Kamel M., and Coote J.H. Terminals of paraventricular spinal neurones are closely associated with adrenal medullary sympathetic preganglionic neurones: immunocytochemical evidence for vasopressin as a possible neurotransmitter in this pathway. Exp. Brain Res. 126 (1999) 68-76
77. Niijima A. Afferent impulse discharges from glucoreceptors in the liver of the guinea pig. Ann. N.Y. Acad. Sci. 157 (1969) 690-700
78. Niijima A. Glucose sensitive afferent nerve fibers in the liver and regulation of blood glucose. Brain Res. Bull. 5 (1980) 175-179
79. Niijima A. Nervous regulation of metabolism. Prog. Neurobiol. 33 (1989) 135-147
80. Ohno K., and Sakurai T. Orexin neuronal circuitry: role in the regulation of sleep and wakefulness. Front. Neuroendocrinol. 29 (2008) 70-87
81. Olney W. Brain lesions, obesity, and other disturbances in mice treated with monosodium glutamate. Science 164 (1969) 719-721
82. Ono T., Nishino H., Fukuda M., Sasaki K., Muramoto K., and Oomura Y. Glucoresponsive neurons in rat ventromedial hypothalamic tissue slices in vitro. Brain Res. 232 (1982) 494-499
83. Oomura Y., Kimura K., Ooyama H., Maeno T., Iki M., and Kuniyoshi M. Reciprocal activities of the ventromedial and lateral hypothalamic areas of cats. Science 143 (1964) 484-485
84. Oomura Y., Ono T., Ooyama H., and Wayner M.J. Glucose and osmosensitive neurones of the rat hypothalamus. Nature 222 (1969) 282-284
85. Oomura Y., Ooyama H., Sugimori M., Nakamura T., and Yamada Y. Glucose inhibition of the glucose-sensitive neurone in the rat lateral hypothalamus. Nature 247 (1974) 284-286
86. Oomura Y., and Yoshimatsu H. Neural network of glucose monitoring system. J. Autonom. Nerv. Syst. 10 (1984) 359-372
87. Paxinos G., and Watson C. The Rat Brain in Stereotaxic Coordinates. seventh ed. (2007), Elsevier
88. Ren X., Zhou L., Terwilliger R., Newton S.S., and de Araujo I.E. Sweet taste signaling functions as a hypothalamic glucose sensor. Front. Integr. Neurosci. 3 (2009) 12
89. Ritter S., Watts A.G., Dinh T.T., Sanchez-Watts G., and Pedrow C. Immunotoxin lesion of hypothalamically projecting norepinephrine and epinephrine neurons differentially affects circadian and stressor-stimulated corticosterone secretion. Endocrinology 144 (2003) 1357-1367
90. Russek M. Participation of hepatic glucoreceptors in the control of intake of food. Nature 197 (1963) 79-80
91. Saberi M., Bohland M., and Donovan C.M. The locus for hypoglycemic detection shifts with the rate of fall in glycemia: the role of portal-superior mesenteric vein glucose sensing. Diabetes 57 (2008) 1380-1386
92. Saper C.B. The central autonomic nervous system: conscious visceral perception and autonomic pattern generation. Annu. Rev. Neurosci. 25 (2002) 433-469
93. Saper C.B., Swanson L.W., and Cowan W.M. The efferent connections of the ventromedial nucleus of the hypothalamus of the rat. J. Comp. Neurol. 169 (1976) 409-442
94. Saper C.B., Loewy A.D., Swanson L.W., and Cowan W.M. Direct hypothalamo-autonomic connections. Brain Res. 117 (1976) 305-312
95. Saper C.B., Lu J., Chou T.C., and Gooley J. The hypothalamic integrator for circadian rhythms. Trends Neurosci. 28 (2005) 152-157
96. Sawchenko P.E., and Swanson L.W. Immunohistochemical identification of neurons in the paraventricular nucleus of the hypothalamus that project to the medulla or to the spinal cord in the rat. J. Comp. Neurol. 205 (1982) 260-272
97. Sawchenko P.E., and Swanson L.W. The organization of forebrain afferents to the paraventricular and supraoptic nuclei of the rat. J. Comp. Neurol. 218 (1983) 121-144
98. Sawchenko P.E., Swanson L.W., Grzanna R., Howe P.R., Bloom S.R., and Polak J.M. Colocalization of neuropeptide Y immunoreactivity in brainstem catecholaminergic neurons that project to the paraventricular nucleus of the hypothalamus. J. Comp. Neurol. 241 (1985) 138-153
99. Schneider J.E., and Watts A.G. Energy partitioning, ingestive behavior and reproductive success. In: Pfaff D.W. (Ed). Hormones, Brain and Behavior. second ed. vol. 1 (2009), Academic Press 205-258
100. Shimizu N., Oomura Y., Novin D., Grijalva C., and Cooper P. Functional correlation between lateral hypothalamic glucose-sensitive neurons and hepatic portal glucose-sensitive units in rats. Brain Res. 265 (1985) 49-54
101. Simmons D.M., and Swanson L.W. 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 (2009) 423-441
102. Song Z., Levin B.E., McArdle J.J., Bakhos N., and Routh V.H. Convergence of pre- and postsynaptic influences on glucosensing neurons in the ventromedial hypothalamic nucleus. Diabetes 50 (2001) 2673-2681
103. Spyer K.M. Annual review prize lecture. Central nervous mechanisms contributing to cardiovascular control. J. Physiol. 474 (1994) 1-19
104. Stanley B.G., and Leibowitz S.F. Neuropeptide Y: stimulation of feeding and drinking by injection into the paraventricular nucleus. Life Sci. 35 (1984) 635-642
105. Stornetta R.L., Sevigny C.P., and Guyenet P.G. Vesicular glutamate transporter DNPI/VGLUT2 mRNA is present in C1 and several other groups of brainstem catecholaminergic neurons. J. Comp. Neurol. 444 (2002) 191-206
106. Strack A.M., Sawyer W.B., Platt K.B., and Loewy A.D. CNS cell groups regulating the sympathetic outflow to adrenal gland as revealed by transneuronal cell body labeling with pseudorabies virus. Brain Res. 491 (1989) 274-296
107. Stricker E., and McCann M. Visceral factors in the control of food intake. Brain Res. Bull. 14 (1985) 687-692
108. Swanson L.W. Cerebral hemisphere regulation of motivated behavior. Brain Res. 886 (2000) 113-164
109. Swanson L.W. Brain Maps: Structure of the Rat Brain. A Laboratory Guide with Printed and Electronic Templates for Data, Models and Schematics. third ed. (2004), Elsevier, Amsterdam
110. Swanson L.W., and Hartman B.K. The central adrenergic system. An immunofluorescence study of the location of cell bodies and their efferent connections in the rat utilizing dopamine-beta-hydroxylase as a marker. J. Comp. Neurol. 163 (1975) 467-505
111. Swanson L.W., and Kuypers H.G. The paraventricular nucleus of the hypothalamus: cytoarchitectonic subdivisions and organization of projections to the pituitary, dorsal vagal complex, and spinal cord as demonstrated by retrograde fluorescence double-labeling methods. J. Comp. Neurol. 194 (1980) 555-570
112. Swanson L.W., and Sawchenko P.E. Hypothalamic integration: organization of the paraventricular and supraoptic nuclei. Annu. Rev. Neurosci. 6 (1983) 269-324
113. Swanson L.W., Sanchez-Watts G., and Watts A.G. Comparison of melanin-concentrating hormone and hypocretin/orexin mRNA expression patterns in a new parcelating scheme of the lateral hypothalamic zone. Neurosci. Lett. 387 (2005) 80-84
114. Szentágothai J., Flerko B., Mess B., and Halasz B. Hypothalamic control of the anterior pituitary; an experimental-morphological study. third ed. (1968), Akadémiai Kiadó, Budapest
115. Thompson R.H., Canteras N.S., and Swanson L.W. Organization of projections from the dorsomedial nucleus of the hypothalamus: a PHA-L study in the rat. J. Comp. Neurol. 376 (1996) 143-173
116. Thompson R.H., and Swanson L.W. 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 (1998) 89-118
117. Thompson R.H., and Swanson L.W. Structural characterization of a hypothalamic visceromotor pattern generator network. Brain Res. Brain Res. Rev. 41 (2003) 153-202
118. Thorens B., and Larsen P.J. Gut-derived signaling molecules and vagal afferents in the control of glucose and energy homeostasis. Curr. Opin. Clin. Nutr. Metab. Care 7 (2004) 471-478
119. Tong Q., Ye C., McCrimmon R.J., Dhillon H., Choi B., Kramer M.D., Yu J., Yang Z., Christiansen L.M., Lee C.E., Choi C.S., Zigman J.M., Shulman G.I., Sherwin R.S., Elmquist J.K., and Lowell B.B. Synaptic glutamate release by ventromedial hypothalamic neurons is part of the neurocircuitry that prevents hypoglycemia. Cell Metab. 5 (2007) 383-393
120. Ulrich-Lai Y.M., and Herman J.P. Neural regulation of endocrine and autonomic stress responses. Nat. Rev. Neurosci. 10 (2009) 397-409
121. van den Pol A.N. The magnocellular and parvocellular paraventricular nucleus of rat: intrinsic organization. J. Comp. Neurol. 206 (1982) 317-345
122. van den Pol A.N., and Cassidy J.R. The hypothalamic arcuate nucleus of rat - a quantitative Golgi analysis. J. Comp. Neurol. 204 (1982) 65-98
123. Wang R., Liu X., Hentges S.T., Dunn-Meynell A.A., Levin B.E., Wang W., and Routh V.H. The regulation of glucose-excited neurons in the hypothalamic arcuate nucleus by glucose and feeding-relevant peptides. Diabetes 53 (2004) 1959-1965
124. Watts A.G. The efferent projections of the suprachiasmatic nucleus. Anatomical insights into the control of circadian rhythms. In: Klein D., Moore R.Y., and Reppert S.M. (Eds). The Suprachiasmatic Nucleus: The Mind's Clock (1991), Oxford University Press 77-104
125. Watts A.G. Glucocorticoid regulation of peptide genes in neuroendocrine CRH neurons: a complexity beyond negative feedback. Front. Neuroendocrinol. 26 (2005) 109-130
126. Watts A.G., and Swanson L.W. 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 (1987) 230-252
127. Watts A.G., and Swanson L.W. Anatomy of motivational systems. In: Pashler H., and Gallistell R. (Eds). 'Stevens' Handbook of Experimental Psychology. Learning, Motivation, and Emotion vol. 3 (2002), John Wiley and Sons 563-632
128. Watts A.G., Sanchez-Watts G., and Kelly A.B. Distinct patterns of neuropeptide gene expression in the lateral hypothalamic area and arcuate nucleus are associated with dehydration induced anorexia. J. Neurosci. 19 (1999) 6111-6121
129. Watts A.G., Khan A.M., Sanchez-Watts G., Salter D., and Neuner C.M. Activation in neural networks controlling ingestive behaviors: what does it mean, and how do we map and measure it?. Physiol. Behav. 89 (2006) 501-510
130. White J.D., Olchovsky D., Kershaw M., and Berelowitz M. Increased hypothalamic content of preproneuropeptide-Y messenger ribonucleic acid in streptozotocin-diabetic rats. Endocrinology 126 (1990) 765-772
131. Willesen M.G., Kristensen P., and Rømer J. Co-localization of growth hormone secretagogue receptor and NPY mRNA in the arcuate nucleus of the rat. Neuroendocrinology 70 (1999) 306-316
132. Zhang Y.H., Lu J., Elmquist J.K., and Saper C.B. Lipopolysaccharide activates specific populations of hypothalamic and brainstem neurons that project to the spinal cord. J. Neurosci. 20 (2000) 6578-6586