Characterization of the projections to the hypothalamic paraventricular and periventricular nuclei in the female sheep brain, using retrograde tracing and immunohistochemistry

Neuroendocrinology

Volumn 90, Issue 1, 2009, Pages 31-53

  Qi, Yue ^a   Namavar, M R ^b   Iqbal, J ^a   Oldfield, B J ^a   Clarke, I J ^a  

^a MONASH UNIVERSITY   (Australia)

^b SHIRAZ UNIVERSITY OF MEDICAL SCIENCES   (Iran)

Author keywords

Appetite; Body weight; Food intake; Neuropeptides

Indexed keywords

FLUOROGOLD; GAMMA INTERMEDIN; MELANIN CONCENTRATING HORMONE; NEUROPEPTIDE Y; OREXIN; TRACER;

ADULT ANIMAL; ANIMAL EXPERIMENT; ANTERIOR HYPOTHALAMUS; ARCUATE NUCLEUS; ARTICLE; BRAIN; BRAIN REGION; BRAIN STEM; CATECHOLAMINE NERVE CELL; CONTROLLED STUDY; EWE; FEMALE; HYPOTHALAMUS; IMMUNOHISTOCHEMISTRY; NERVE CELL; NONHUMAN; PRIORITY JOURNAL; SEROTONINERGIC NERVE; SHEEP; THALAMUS MIDLINE NUCLEUS;

ANIMALS; ARCUATE NUCLEUS; CATECHOLAMINES; FEMALE; FLUORESCENT DYES; GAMMA-MSH; HYPOTHALAMIC HORMONES; HYPOTHALAMUS; IMMUNOHISTOCHEMISTRY; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; MELANINS; NEURAL PATHWAYS; NEURONS; NEURONS, AFFERENT; NEUROPEPTIDE Y; NEUROPEPTIDES; PARAVENTRICULAR HYPOTHALAMIC NUCLEUS; PITUITARY HORMONES; SEROTONIN; SHEEP;

EID: 67651111836     PISSN: 00283835     EISSN: None     Source Type: Journal    
DOI: 10.1159/000221304     Document Type: Article

References (126)

1. Elmquist JK: Anatomic basis of leptin action in the hypothalamus. Front Horm Res 2000; 26: 21-41.
2. Elmquist JK: Hypothalamic pathways underlying the endocrine, autonomic, and behavioral effects of leptin. Physiol Behav 2001; 74: 703-708. (Pubitemid 34076617)
3. Elmquist JK, Elias CF, Saper CB: From lesions to leptin: hypothalamic control of food intake and body weight. Neuron 1999; 22: 221-232. (Pubitemid 29109657)
4. Chaillou E, Baumont R, Tramu G, Tillet Y: Effect of feeding on fos protein expression in sheep hypothalamus with special reference to the supraoptic and paraventricular nuclei: an immunohistochemical study. Eur J Neurosci 2000; 12: 4515-4524. (Pubitemid 32037859)
5. Chaillou E, Baumont R, Tramu G, Tillet Y: Long-term undernutrition followed by shortterm refeeding effects on the corticotropinreleasing hormone containing neurones in the paraventricular nucleus: an immunohistochemical study in sheep. J Neuroendocrinol 2002; 14: 269-275. (Pubitemid 34285296)
6. Kenney MJ, Weiss ML, Mendes T, Wang Y, Fels RJ: Role of paraventricular nucleus in regulation of sympathetic nerve frequency components. Am J Physiol Heart Circ Physiol 2003; 284: H1710-H1720. (Pubitemid 36460786)
7. Segar JL, Ellsbury DL, Smith OM: Inhibition of sympathetic responses at birth in sheep by lesion of the paraventricular nucleus. Am J Physiol Regul Integr Comp Physiol 2002; 283: R1395-R1403.
8. Rinaman L: Postnatal development of catecholamine inputs to the paraventricular nucleus of the hypothalamus in rats. J Comp Neurol 2001; 438: 411-422. (Pubitemid 32831306)
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. Sawchenko PE, Arias C, Bittencourt JC: Inhibin β, somatostatin, and enkephalin immunoreactivities coexist in caudal medullary neurons that project to the paraventricular nucleus of the hypothalamus. J Comp Neurol 1990; 291: 269-280. (Pubitemid 20032434)
11. Argiolas A, Melis MR: The neurophysiology of the sexual cycle. J Endocrinol Invest 2003; 26: 20-22.
12. Hashimoto H, Fukui K, Noto T, Nakajima T, Kato N: Distribution of vasopressin and oxytocin in rat brain. Endocrinol Jpn 1985; 32: 89-97.
13. Hou-Yu A, Lamme AT, Zimmerman EA, Silverman AJ: Comparative distribution of vasopressin and oxytocin neurons in the rat brain using a double-label procedure. Neuroendocrinology 1986; 44: 235-246. (Pubitemid 17175335)
14. Luiten PG, ter Horst GJ, Steffens AB: The hypothalamus, intrinsic connections and outflow pathways to the endocrine system in relation to the control of feeding and metabolism. Prog Neurobiol 1987; 28: 1-54.
15. Rafols JA, Aronin N, Difiglia M: A Golgi study of the monkey paraventricular nucleus: neuronal types, afferent and efferent fibers. J Comp Neurol 1987; 257: 595-613. (Pubitemid 17035206)
16. 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. (Pubitemid 13224880)
17. 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. (Pubitemid 20076644)
18. Estacio MA, Tsukamura H, Reyes BA, Uenoyama Y, L'Anson H, Maeda K: Involvement of brainstem catecholaminergic inputs to the hypothalamic paraventricular nucleus in estrogen receptor alpha expression in this nucleus during different stress conditions in female rats. Endocrinology 2004; 145: 4917-4926. (Pubitemid 39551108)
19. Larsen PJ, Mikkelsen JD: Functional identification of central afferent projections conveying information of acute 'stress' to the hypothalamic paraventricular nucleus. J Neurosci 1995; 15: 2609-2627.
20. Shioda S, Nakai Y: Medullary synaptic inputs to thyrotropin-releasing hormone (trh)- containing neurons in the hypothalamus: an ultrastructural study combining WGA-HRP anterograde tracing with TRH immunocytochemistry. Brain Res 1993; 625: 9-15. (Pubitemid 23285437)
21. Floyd NS, Keay KA, Arias CM, Sawchenko PE, Bandler R: Projections from the ventrolateral periaqueductal gray to endocrine regulatory subdivisions of the paraventricular nucleus of the hypothalamus in the rat. Neurosci Lett 1996; 220: 105-108.
22. Li C, Chen P, Smith MS: Identification of neuronal input to the arcuate nucleus (ARH) activated during lactation: implications in the activation of neuropeptide Y neurons. Brain Res 1999; 824: 267-276. (Pubitemid 29225533)
23. Saper CB, Loewy AD: Efferent connections of the parabrachial nucleus in the rat. Brain Res 1980; 197: 291-317. (Pubitemid 10040293)
24. Swanson LW, Sawchenko PE: Paraventricular nucleus: a site for the integration of neuroendocrine and autonomic mechanisms. Neuroendocrinology 1980; 31: 410-417.
25. Swanson LW, Sawchenko PE, Berod A, Hartman BK, Helle KB, Vanorden DE: An immunohistochemical study of the organization of catecholaminergic cells and terminal fields in the paraventricular and supraoptic nuclei of the hypothalamus. J Comp Neurol 1981; 196: 271-285. (Pubitemid 11098864)
26. Swanson LW, Sawchenko PE, Rivier J, Vale WW: Organization of ovine corticotropinreleasing factor immunoreactive cells and fibers in the rat brain: an immunohistochemical study. Neuroendocrinology 1983; 36: 165-186. (Pubitemid 13138041)
27. Welento J, Szteyn S, Milart Z: Observations on the stereotaxic configuration of the hypothalamus nuclei in the sheep. Anat Anz 1969; 124: 1-27.
28. Moga MM, Saper CB: Neuropeptide-immunoreactive neurons projecting to the paraventricular hypothalamic nucleus in the rat. J Comp Neurol 1994; 346: 137-150. (Pubitemid 2118697)
29. Ter Horst GJ, Luiten PG: Phaseolus vulgaris leuco-agglutinin tracing of intrahypothalamic connections of the lateral, ventromedial, dorsomedial and paraventricular hypothalamic nuclei in the rat. Brain Res Bull 1987; 18: 191-203.
30. Qi Y, Iqbal J, Oldfield BJ, Clarke IJ: Neural connectivity in the mediobasal hypothalamus of the sheep brain. Neuroendocrinology 2008; 87: 91-112. (Pubitemid 351301280)
31. Reddy S, Oliver JR, Elliott RB: Immunohistochemical demonstration of somatostatin in the pancreas of fetal and adult sheep. Aust J Biol Sci 1984; 37: 25-29.
32. Willoughby JO, Oliver JR, Fletcher TP, Clarke IJ: Distribution of somatostatin immunoreactivity in sheep hypothalamus: a comparison with that of the rat. Arch Histol Cytol 1995; 58: 31-36.
33. Ben-Barak Y, Russell JT, Whitnall MH, Ozato K, Gainer H: Neurophysin in the hypothalamo- neurohypophysial system. I. Production and characterization of monoclonal antibodies. J Neurosci 1985; 5: 81-97.
34. Date Y, Ueta Y, Yamashita H, Yamaguchi H, Matsukura S, Kangawa K, Sakurai T, Yanagisawa M, Nakazato M: Orexins, orexigenic hypothalamic peptides, interact with autonomic, neuroendocrine and neuroregulatory systems. Proc Natl Acad Sci USA 1999; 96: 748-753. (Pubitemid 29061280)
35. Iqbal J, Pompolo S, Murakami T, Grouzmann E, Sakurai T, Meister B, Clarke IJ: Immunohistochemical characterization of localization of long-form leptin receptor (ob-rb) in neurochemically defined cells in the ovine hypothalamus. Brain Res 2001; 920: 55-64. (Pubitemid 33086779)
36. Bittencourt JC, Presse F, Arias C, Peto C, Vaughan J, Nahon JL, Vale W, Sawchenko PE: The melanin-concentrating hormone system of the rat brain: an immuno- and hybridization histochemical characterization. J Comp Neurol 1992; 319: 218-245.
37. Carey DG, Iismaa TP, Ho KY, Rajkovic IA, Kelly J, Kraegen EW, Ferguson J, Inglis AS, Shine J, Chisholm DJ: Potent effects of human galanin in man: growth hormone secretion and vagal blockade. J Clin Endocrinol Metab 1993; 77: 90-93. (Pubitemid 23206782)
38. Christie MJ, Beart PM, Jarrott B, Maccarrone C: Distribution of neuropeptide Y immunoreactivity in the rat basal ganglia: effects of excitotoxin lesions to caudate-putamen. Neurosci Lett 1986; 63: 305-309. (Pubitemid 16147676)
39. Iqbal J, Manley TR, Yue Q, Namavar MR, Clarke IJ: Noradrenergic regulation of hypothalamic cells that produce growth hormone- releasing hormone and somatostatin and the effect of altered adiposity in sheep. J Neuroendocrinol 2005; 17: 341-352. (Pubitemid 40796990)
40. Herz A, Gramsch C, Hollt V, Meo T, Riethmuller G: Characteristics of a monoclonal β- endorphin antibody recognizing the N-terminus of opioid peptides. Life Sci 1982; 31: 1721-1724. (Pubitemid 13207150)
41. Franceschini I, Lomet D, Cateau M, Delsol G, Tillet Y, Caraty A: Kisspeptin immunoreactive cells of the ovine preoptic area and arcuate nucleus co-express estrogen receptor α. Neurosci Lett 2006; 401: 225-230. (Pubitemid 43729526)
42. Kitahama K, Denoroy L, Goldstein M, Jouvet M, Pearson J: Immunohistochemistry of tyrosine hydroxylase and phenylethanolamine N-methyltransferase in the human brain stem: description of adrenergic perikarya and characterization of longitudinal catecholaminergic pathways. Neuroscience 1988; 25: 97-111. (Pubitemid 18126860)
43. Berod A, Hartman BK, Keller A, Joh TH, Pujol JF: A new double labeling technique using tyrosine hydroxylase and dopamine- β-hydroxylase immunohistochemistry: evidence for dopaminergic cells lying in the pons of the beef brain. Brain Res 1982; 240: 235-243.
44. Clarke IJ, Pompolo S, Scott CJ, Rawson JA, Caddy D, Jakubowska AE, Pereira AM: Cells of the arcuate nucleus and ventromedial nucleus of the ovariectomized ewe that respond to oestrogen: a study using fos immunohistochemistry. J Neuroendocrinol 2001; 13: 934-941. (Pubitemid 33019177)
45. Iqbal J, Pompolo S, Dumont LM, Wu CS, Mountjoy KG, Henry BA, Clarke IJ: Longterm alterations in body weight do not affect the expression of melanocortin receptor-3 and -4 mRNA in the ovine hypothalamus. Neuroscience 2001; 105: 931-940. (Pubitemid 32786806)
46. Iqbal J, Henry BA, Pompolo S, Rao A, Clarke IJ: Long-term alteration in bodyweight and food restriction does not affect the gene expression of either preproorexin or prodynorphin in the sheep. Neuroscience 2003; 118: 217-226. (Pubitemid 36369544)
47. Iqbal J, Manley TR, Ciofi P, Clarke IJ: Reduction in adiposity affects the extent of afferent projections to growth hormone-releasing hormone and somatostatin neurons and the degree of colocalization of neuropeptides in growth hormone-releasing hormone and somatostatin cells of the ovine hypothalamus. Endocrinology 2005; 146: 4776-4785. (Pubitemid 41446615)
48. Scott CJ, Clarke IJ, Tilbrook AJ: Neuronal inputs from the hypothalamus and brain stem to the medial preoptic area of the ram: neurochemical correlates and comparison to the ewe. Biol Reprod 2003; 68: 1119-1133.
49. Grayson BE, Allen SE, Billes SK, Williams SM, Smith MS, Grove KL: Prenatal development of hypothalamic neuropeptide systems in the nonhuman primate. Neuroscience 2006; 143: 975-986.
50. Richard P: Atlas stéréotaxique du cerveau de brebis Préalpes-du-Sud. Paris, Institut National de la Recherche Agronomique, 1967.
51. Hahn TM, Breininger JF, Baskin DG, Schwartz MW: Coexpression of AGRP and NPY in fasting-activated hypothalamic neurons. Nat Neurosci 1998; 1: 271-272.
52. Haskell-Luevano C, Chen P, Li C, Chang K, Smith MS, Cameron JL, Cone RD: Characterization of the neuroanatomical distribution of agouti-related protein immunoreactivity in the rhesus monkey and the rat. Endocrinology 1999; 140: 1408-1415. (Pubitemid 29104247)
53. Adam CL, Archer ZA, Findlay PA, Thomas L, Marie M: Hypothalamic gene expression in sheep for cocaine- and amphetamine-regulated transcript, pro-opiomelanocortin, neuropeptide Y, agouti-related peptide and leptin receptor and responses to negative energy balance. Neuroendocrinology 2002; 75: 250-256. (Pubitemid 34455098)
54. Elmquist JK, Saper CB: Activation of neurons projecting to the paraventricular hypothalamic nucleus by intravenous lipopolysaccharide. J Comp Neurol 1996; 374: 315-331. (Pubitemid 26354795)
55. Li C, Chen P, Smith MS: Neural populations in the rat forebrain and brainstem activated by the suckling stimulus as demonstrated by cfos expression. Neuroscience 1999; 94: 117-129. (Pubitemid 29457602)
56. Li C, Chen P, Smith MS: The acute suckling stimulus induces expression of neuropeptide Y (NPY) in cells in the dorsomedial hypothalamus and increases NPY expression in the arcuate nucleus. Endocrinology 1998; 139: 1645-1652. (Pubitemid 28513820)
57. Smith MS: Lactation alters neuropeptide-Y and proopiomelanocortin gene expression in the arcuate nucleus of the rat. Endocrinology 1993; 133: 1258-1265.
58. Harlan RE, Shivers BD, Romano GJ, Howells RD, Pfaff DW: Localization of preproenkephalin mRNA in the rat brain and spinal cord by in situ hybridization. J Comp Neurol 1987; 258: 159-184. (Pubitemid 17050995)
59. Simerly RB, Swanson LW: The distribution of neurotransmitter-specific cells and fibers in the anteroventral periventricular nucleus: implications for the control of gonadotropin secretion in the rat. Brain Res 1987; 400: 11-34.
60. Gray TS: Amygdaloid CRF pathways. Role in autonomic, neuroendocrine, and behavioral responses to stress. Ann NY Acad Sci 1993; 697: 53-60.
61. Gray TS, Carney ME, Magnuson DJ: Direct projections from the central amygdaloid nucleus to the hypothalamic paraventricular nucleus: possible role in stress-induced adrenocorticotropin release. Neuroendocrinology 1989; 50: 433-446.
62. Gray TS, Magnuson DJ: Neuropeptide neuronal efferents from the bed nucleus of the stria terminalis and central amygdaloid nucleus to the dorsal vagal complex in the rat. J Comp Neurol 1987; 262: 365-374. (Pubitemid 17141426)
63. Oldfield BJ, Silverman AJ: A light microscopic HRP study of limbic projections to the vasopressin-containing nuclear groups of the hypothalamus. Brain Res Bull 1985; 14: 143-157.
64. Herman JP, Ostrander MM, Mueller NK, Figueiredo H: Limbic system mechanisms of stress regulation: hypothalamo-pituitaryadrenocortical axis. Prog Neuropsychopharmacol Biol Psychiatry 2005; 29: 1201-1213.
65. Cullinan WE, Herman JP, Watson SJ: Ventral subicular interaction with the hypothalamic paraventricular nucleus: evidence for a relay in the bed nucleus of the stria terminalis. J Comp Neurol 1993; 332: 1-20.
66. Crane JW, Buller KM, Day TA: Evidence that the bed nucleus of the stria terminalis contributes to the modulation of hypophysiotropic corticotropin-releasing factor cell responses to systemic interleukin-1β. J Comp Neurol 2003; 467: 232-242.
67. Herman JP, Cullinan WE, Watson SJ: Involvement of the bed nucleus of the stria terminalis in tonic regulation of paraventricular hypothalamic CRH and AVP mRNA expression. J Neuroendocrinol 1994; 6: 433-442.
68. Dunn JD: Plasma corticosterone responses to electrical stimulation of the bed nucleus of the stria terminalis. Brain Res 1987; 407: 327-331. (Pubitemid 17085791)
69. Pecori Giraldi F, Cavagnini F: Corticotropin- releasing hormone is produced by rat corticotropes and modulates ACTH secretion in a paracrine/autocrine fashion. J Clin Invest 1998; 101: 2478-2484.
70. 2 -adrenoceptors. Am J Physiol 1992; 262:R407-R411.
71. Chen XM, Hosono T, Yoda T, Fukuda Y, Kanosue K: Efferent projection from the preoptic area for the control of non-shivering thermogenesis in rats. J Physiol 1998; 512: 883-892. (Pubitemid 28505316)
72. Nakamura K, Morrison SF: Preoptic mechanism for cold-defensive responses to skin cooling. J Physiol 2008; 586: 2611-2620. (Pubitemid 351689815)
73. Krieger MS, Conrad LC, Pfaff DW: An autoradiographic study of the efferent connections of the ventromedial nucleus of the hypothalamus. J Comp Neurol 1979; 183: 785-815.
74. Saper CB, Swanson LW, Cowan WM: The efferent connections of the ventromedial nucleus of the hypothalamus of the rat. J Comp Neurol 1976; 169: 409-442.
75. Sawchenko PE, Swanson LW: The organization of forebrain afferents to the paraventricular and supraoptic nuclei of the rat. J Comp Neurol 1983; 218: 121-144.
76. 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. (Pubitemid 28512358)
77. Baker RA, Herkenham M: Arcuate nucleus neurons that project to the hypothalamic paraventricular nucleus: neuropeptidergic identity and consequences of adrenalectomy on mRNA levels in the rat. J Comp Neurol 1995; 358: 518-530.
78. Blevins JE, Schwartz MW, Baskin DG: Evidence that paraventricular nucleus oxytocin neurons link hypothalamic leptin action to caudal brain stem nuclei controlling meal size. Am J Physiol Regul Integr Comp Physiol 2004; 287:R87-R96.
79. Goodman RL, Lehman MN, Smith JT, Coolen LM, de Oliveira CV, Jafarzadehshirazi MR, Pereira A, Iqbal J, Caraty A, Ciofi P, Clarke IJ: Kisspeptin neurons in the arcuate nucleus of the ewe express both dynorphin A and neurokinin B. Endocrinology 2007; 148: 5752-5760. (Pubitemid 350146171)
80. Chaillou E, Tramu G, Tillet Y: Distribution of galanin immunoreactivity in the sheep diencephalon. J Chem Neuroanat 1999; 17: 129-146.
81. Cheung CC, Hohmann JG, Clifton DK, Steiner RA: Distribution of galanin messenger rna-expressing cells in murine brain and their regulation by leptin in regions of the hypothalamus. Neuroscience 2001; 103: 423-432.
82. Stanley BG, Leibowitz SF: Neuropeptide Y injected in the paraventricular hypothalamus: a powerful stimulant of feeding behavior. Proc Natl Acad Sci USA 1985; 82: 3940-3943.
83. Li G, Mobbs CV, Scarpace PJ: Central proopiomelanocortin gene delivery results in hypophagia, reduced visceral adiposity, and improved insulin sensitivity in genetically obese zucker rats. Diabetes 2003; 52: 1951-1957. (Pubitemid 36919786)
84. Yasuda T, Masaki T, Kakuma T, Yoshimatsu H: Hypothalamic melanocortin system regulates sympathetic nerve activity in brown adipose tissue. Exp Biol Med (Maywood) 2004; 229: 235-239. (Pubitemid 38280597)
85. Pompolo S, Rawson JA, Clarke IJ: Projections from the arcuate/ventromedial region of the hypothalamus to the preoptic area and bed nucleus of stria terminalis in the brain of the ewe; lack of direct input to gonadotropinreleasing hormone neurons. Brain Res 2001; 904: 1-12. (Pubitemid 32545349)
86. Commons KG, Kow LM, Milner TA, Pfaff DW: In the ventromedial nucleus of the rat hypothalamus, GABA-immunolabeled neurons are abundant and are innervated by both enkephalin- and GABA-immunolabeled axon terminals. Brain Res 1999; 816: 58-67.
87. Iqbal J, Pompolo S, Sakurai T, Clarke IJ: Evidence that orexin-containing neurones provide direct input to gonadotropin-releasing hormone neurones in the ovine hypothalamus. J Neuroendocrinol 2001; 13: 1033-1041. (Pubitemid 33100220)
88. Tillet Y, Batailler M, Fellmann D: Distribution of melanin-concentrating hormone (MCH)-like immunoreactivity in neurons of the diencephalon of sheep. J Chem Neuroanat 1996; 12: 135-145. (Pubitemid 27058693)
89. Sakurai T: Orexin: a link between energy homeostasis and adaptive behaviour. Curr Opin Clin Nutr Metab Care 2003; 6: 353-360. (Pubitemid 40684584)
90. Centeno ML, Sanchez RL, Cameron JL, Bethea CL: Hypothalamic gonadotrophinreleasing hormone expression in female monkeys with different sensitivity to stress. J Neuroendocrinol 2007; 19: 594-604. (Pubitemid 47065105)
91. Watts AG, Swanson LW, Sanchez-Watts G: Efferent projections of the suprachiasmatic nucleus. I. Studies using anterograde transport of Phaseolus vulgaris leucoagglutinin in the rat. J Comp Neurol 1987; 258: 204-229.
92. Watts AG, Swanson LW: Efferent projections of the suprachiasmatic nucleus: II. Studies using retrograde transport of fluorescent dyes and simultaneous peptide immunohistochemistry in the rat. J Comp Neurol 1987; 258: 230-252. (Pubitemid 17050998)
93. Werther GA, Hogg A, Oldfield BJ, McKinley MJ, Figdor R, Allen AM, Mendelsohn FA: Localization and characterization of insulin receptors in rat brain and pituitary gland using in vitro autoradiography and computerized densitometry. Endocrinology 1987; 121: 1562-1570. (Pubitemid 17155909)
94. Casatti CA, Elias CF, Sita LV, Frigo L, Furlani VC, Bauer JA, Bittencourt JC: Distribution of melanin-concentrating hormone neurons projecting to the medial mammillary nucleus. Neuroscience 2002; 115: 899-915. (Pubitemid 35336032)
95. Kirouac GJ, Parsons MP, Li S: Innervation of the paraventricular nucleus of the thalamus from cocaine- and amphetamine-regulated transcript (CART) containing neurons of the hypothalamus. J Comp Neurol 2006; 497: 155-165.
96. Csaki A, Kocsis K, Halasz B, Kiss J: Localization of glutamatergic/ aspartatergic neurons projecting to the hypothalamic paraventricular nucleus studied by retrograde transport of [ 3 H] D -aspartate autoradiography. Neuroscience 2000; 101: 637-655. (Pubitemid 30953121)
97. Kawano H, Daikoku S: Somatostatin-containing neuron systems in the rat hypothalamus: retrograde tracing and immunohistochemical studies. J Comp Neurol 1988; 271: 293-299. (Pubitemid 18133008)
98. Cheung CC, Clifton DK, Steiner RA: Proopiomelanocortin neurons are direct targets for leptin in the hypothalamus. Endocrinology 1997; 138: 4489-4492.
99. Henry BA, Rao A, Tilbrook AJ, Clarke IJ: Chronic food-restriction alters the expression of somatostatin and growth hormonereleasing hormone in the ovariectomised ewe. J Endocrinol 2001; 170: R1-R5. (Pubitemid 32677592)
100. Langevin H, Emson PC: Distribution of substance P, somatostatin and neurotensin in the human hypothalamus. Brain Res 1982; 246: 65-69. (Pubitemid 12048841)
101. Cheung S, Johnson JD, Moore KE, Lookingland KJ: Dopamine receptor-mediated regulation of expression of fos and its related antigens (FRA) in somatostatin neurons in the hypothalamic periventricular nucleus. Brain Res 1997; 770: 176-183. (Pubitemid 27468065)
102. Walsh JP, Rao A, Thompson RC, Clarke IJ: Proenkephalin and opioid μ-receptor mRNA expression in ovine hypothalamus across the estrous cycle. Neuroendocrinology 2001; 73: 26-36. (Pubitemid 32171107)
103. Henry BA, Tilbrook AJ, Dunshea FR, Rao A, Blache D, Martin GB, Clarke IJ: Longterm alterations in adiposity affect the expression of melanin- concentrating hormone and enkephalin but not proopiomelanocortin in the hypothalamus of ovariectomized ewes. Endocrinology 2000; 141: 1506-1514. (Pubitemid 32273176)
104. Rondini TA, Baddini SP, Sousa LF, Bittencourt JC, Elias CF: Hypothalamic cocaineand amphetamine-regulated transcript neurons project to areas expressing gonadotropin releasing hormone immunoreactivity and to the anteroventral periventricular nucleus in male and female rats. Neuroscience 2004; 125: 735-748.
105. Koylu EO, Couceyro PR, Lambert PD, Ling NC, DeSouza EB, Kuhar MJ: Immunohistochemical localization of novel cart peptides in rat hypothalamus, pituitary and adrenal gland. J Neuroendocrinol 1997; 9: 823-833.
106. Henry BA, Rao A, Ikenasio BA, Mountjoy KG, Tilbrook AJ, Clarke IJ: Differential expression of cocaine- and amphetamineregulated transcript and agouti relatedprotein in chronically food-restricted sheep. Brain Res 2001; 918: 40-50. (Pubitemid 33001487)
107. Saeb-Parsy K, Lombardelli S, Khan FZ, Mc- Dowall K, Au-Yong IT, Dyball RE: Neural connections of hypothalamic neuroendocrine nuclei in the rat. J Neuroendocrinol 2000; 12: 635-648. (Pubitemid 30349010)
108. Palkovits M: Interconnections between the neuroendocrine hypothalamus and the central autonomic system. Geoffrey Harris Memorial lecture, Kitakyushu, Japan, October 1998. Front Neuroendocrinol 1999; 20: 270-295.
109. Hosoi T, Kawagishi T, Okuma Y, Tanaka J, Nomura Y: Brain stem is a direct target for leptin's action in the central nervous system. Endocrinology 2002; 143: 3498-3504. (Pubitemid 34925724)
110. Koegler FH, York DA, Bray GA: The effects on feeding of galanin and m40 when injected into the nucleus of the solitary tract, the lateral parabrachial nucleus, and the third ventricle. Physiol Behav 1999; 67: 259-267.
111. Berthoud HR, Sutton GM, Townsend RL, Patterson LM, Zheng H: Brainstem mechanisms integrating gut-derived satiety signals and descending forebrain information in the control of meal size. Physiol Behav 2006; 89: 517-524.
112. Cameron AA, Khan IA, Westlund KN, Cliffer KD, Willis WD: The efferent projections of the periaqueductal gray in the rat: a Phaseolus vulgaris -leucoagglutinin study. I. Ascending projections. J Comp Neurol 1995; 351: 568-584.
113. Cameron AA, Khan IA, Westlund KN, Willis WD: The efferent projections of the periaqueductal gray in the rat: a Phaseolus vulgaris -leucoagglutinin study. II. Descending projections. J Comp Neurol 1995; 351: 585-601.
114. Pan B, Castro-Lopes JM, Coimbra A: Central afferent pathways conveying nociceptive input to the hypothalamic paraventricular nucleus as revealed by a combination of retrograde labeling and c-fos activation. J Comp Neurol 1999; 413: 129-145. (Pubitemid 29409756)
115. Moga MM, Weis RP, Moore RY: Efferent projections of the paraventricular thalamic nucleus in the rat. J Comp Neurol 1995; 359: 221-238.
116. Hasue RH, Shammah-Lagnado SJ: Origin of the dopaminergic innervation of the central extended amygdala and accumbens shell: a combined retrograde tracing and immunohistochemical study in the rat. J Comp Neurol 2002; 454: 15-33.
117. Balthasar N, Dalgaard LT, Lee CE, Yu J, Funahashi H, Williams T, Ferreira M, Tang V, McGovern RA, Kenny CD, Christiansen LM, Edelstein E, Choi B, Boss O, Aschkenasi C, Zhang CY, Mountjoy K, Kishi T, Elmquist JK, Lowell BB: Divergence of melanocortin pathways in the control of food intake and energy expenditure. Cell 2005; 123: 493-505. (Pubitemid 41546678)
118. Trulson ME, Cannon MS, Raese JD: Identification of dopamine-containing cell bodies in the dorsal and median raphe nuclei of the rat brain using tyrosine hydroxylase immunochemistry. Brain Res Bull 1985; 15: 229-234.
119. Nagatsu I, Kondo Y, Inagaki S, Kojima H, Nagatsu T: Immunofluorescent and biochemical studies on tyrosine hydroxylase and dopamine- β-hydroxylase of the bullfrog sciatic nerves. Histochemistry 1979; 61: 103-109. (Pubitemid 9247975)
120. Dabadie H, Mons N, Geffard M: Simultaneous detection of tryptamine and dopamine in rat substantia nigra and raphe nuclei using specific antibodies. Brain Res 1990; 512: 138-142. (Pubitemid 20103837)
121. Wiklund L, Leger L, Persson M: Monoamine cell distribution in the cat brain stem. A fluorescence histochemical study with quantification of indolaminergic and locus coeruleus cell groups. J Comp Neurol 1981; 203: 613-647. (Pubitemid 12200737)
122. Tafti M, Nishino S, Liao W, Dement WC, Mignot E: Mesopontine organization of cholinergic and catecholaminergic cell groups in the normal and narcoleptic dog. J Comp Neurol 1997; 379: 185-197. (Pubitemid 27113613)
123. Arsenault MY, Parent A, Seguela P, Descarries L: Distribution and morphological characteristics of dopamine-immunoreactive neurons in the midbrain of the squirrel monkey (Saimiri sciureus). J Comp Neurol 1988; 267: 489-506. (Pubitemid 18052204)
124. Petrov T, Krukoff TL, Jhamandas JH: The hypothalamic paraventricular and lateral parabrachial nuclei receive collaterals from raphe nucleus neurons: a combined double retrograde and immunocytochemical study. J Comp Neurol 1992; 318: 18-26.
125. Oldfield BJ, Hou-Yu A, Silverman AJ: A combined electron microscopic hrp and immunocytochemical study of the limbic projections to rat hypothalamic nuclei containing vasopressin and oxytocin neurons. J Comp Neurol 1985; 231: 221-231. (Pubitemid 15159973)
126. Kageyama K, Tozawa F, Horiba N, Watanobe H, Suda T: Serotonin stimulates corticotropin- releasing factor gene expression in the hypothalamic paraventricular nucleus of conscious rats. Neurosci Lett 1998; 243: 17-20. (Pubitemid 28109400)