Efferent projections of the suprachiasmatic nucleus based on the distribution of vasoactive intestinal peptide (VIP) and arginine vasopressin (AVP) immunoreactive fibers in the hypothalamus of Sapajus apella

Journal of Chemical Neuroanatomy

Volumn 57-58, Issue , 2014, Pages 42-53

  Campos, L M G ^a   Cruz Rizzolo, R J ^b   Watanabe, Ii Sei ^a   Pinato, L ^b   Nogueira, M I ^a  

^a UNIVERSITY OF SÃO PAULO   (Brazil)

^b SÃO PAULO STATE UNIVERSITY UNESP   (Brazil)

Author keywords

Anticipatory behavior; Circadian rhythms; Neuroanatomy; Primate

Indexed keywords

ARGIPRESSIN; VASOACTIVE INTESTINAL POLYPEPTIDE;

ANIMAL TISSUE; ANTERIOR HYPOTHALAMUS; ARTICLE; BIOLOGICAL RHYTHM; BRAIN REGION; CEBUS APELLA; CELL SUBPOPULATION; CIRCADIAN RHYTHM; EFFERENT NERVE; HYPOTHALAMUS; HYPOTHALAMUS PERIVENTRICULAR NUCLEUS; IMMUNOHISTOCHEMISTRY; IMMUNOREACTIVITY; LATERAL HYPOTHALAMUS; MALE; MORPHOLOGICAL TRAIT; NERVE PROJECTION; NONHUMAN; POSTERIOR HYPOTHALAMUS; PRIMATE; PRIORITY JOURNAL; RODENT; SUPRACHIASMATIC NUCLEUS; ANATOMY AND HISTOLOGY; ANIMAL; CEBUS; METABOLISM; NERVE FIBER; PHYSIOLOGY; PREOPTIC AREA; ULTRASTRUCTURE;

ANIMALS; ARGININE VASOPRESSIN; CEBUS; EFFERENT PATHWAYS; HYPOTHALAMUS; IMMUNOHISTOCHEMISTRY; MALE; NERVE FIBERS; PREOPTIC AREA; SUPRACHIASMATIC NUCLEUS; VASOACTIVE INTESTINAL PEPTIDE;

EID: 84901207611     PISSN: 08910618     EISSN: 18736300     Source Type: Journal    
DOI: 10.1016/j.jchemneu.2014.03.004     Document Type: Article

References (86)

1. Abrahamson E.E., Moore R.Y. Suprachiasmatic nucleus in the mouse: retinal innervation intrinsic organization and efferent projections. Brain Res. 2001, 916:172-191.
2. Acosta-Galvan G., Yi C.X., van der Vliet J., Jhamandas J.H., Panula P., Angeles-Castellanos M., Del Carmen Basualdo M., Escobar C., Buijs R.M. Interaction between hypothalamic dorsomedial nucleus and the suprachiasmatic nucleus determines intensity of food anticipatory behavior. Proc. Natl. Acad. Sci. U. S. A. 2011, 14:5813-5818.
3. Buijs R.M., Markman M.M., Hou Y.X., Shinn S. Projections of the suprachiasmatic nucleus to stress-related areas in the rat hypothalamus: a light and electron microscopical study. J. Comp. Neurol. 1993, 335:42-54.
4. Buijs R.M. Anatomical basis for the expression of circadian rhythms: efferent projections of the suprachiasmatic nucleus. J. Comp. Neurol. 1997, 111:229-240.
5. Buijs R.M., van Eden C.G., Goncharuk V.D., Kalsbeek A. The biological clock tunes the organs of the body: timing by hormones and the autonomic nervous system. J. Endocrinol. 2003, 177:17-26.
6. Card J.P., Moore R.Y. The suprachiasmatic nucleus of the golden hamster: immunohistochemical analysis of the cell and fiber distribution. Neuroscience 1984, 13:415-431.
7. Cassone V.M., Speh J.C., Card J.P., Moore R.Y. Comparative anatomy of the mammalian hypothalamic suprachiasmatic nucleus. J. Biol. Rhythms 1988, 3:71-91.
8. Cavalcante J.S., Alves A.S., Costa M.S.M.O., Britto L.R.G. Differential distribution of afferents containing serotonin and neuropeptide Y within the marmoset suprachiasmatic nucleus. Brain Res. 2002, 927:200-203.
9. Cavalcante J.S., de Pontes A.L., Engelberth R.C., Cavalcante J.C., Nascimento E.S., Borda J.S., Pinato L., Costa M.S., de Toledo C.A. 5-HT (1B) receptor in the suprachiasmatic nucleus of the common marmoset (Callithrix jacchus). Neurosci. Lett. 2011, 488:6-10.
10. Chou T.C., Scammell T.E., Gooley J.J., Gaus S.E., Saper C.B., Lu J. Critical role of dorsomedial hypothalamic nucleus in a wide range of behavioral circadian rhythms. J. Neurosci. 2003, 23:10691-10702.
11. Cipolla-Neto J., Marques N., Menna-Barreto L. Introdução ao estudo da cronobiologia 1988, Ícone/EDUSP, São Paulo.
12. Costa M.S.M.O., Moreira L.F., Alones V., Lu J., Santee U.R., Cavalcante J.S., Moraes P.R.A., Britto L.R.G., Menaker M. Characterization of the circadian system in a Brazilian species of monkey (Callithrix jacchus): immunohistochemical analysis and retinal projections. Biol. Rhythm Res. 1998, 29:510-520.
13. Dai J., Swaab D.F., Van der Vliet J., Buijs R.M. Postmortem tracing reveals the organization of hypothalamic projections of the suprachiasmatic nucleus in the human brain. J. Comp. Neurol. 1998, 400:87-102.
14. Dai J., Swaab D.F., Buijs R.M. Distribution of vasopressin and vasoactive intestinal polypeptide (VIP) fibers in the human hypothalamus with special emphasis on suprachiasmatic nucleus efferent projections. J. Comp. Neurol. 1997, 383:397-414.
15. Daikoku S., Hisano S., Kagotani Y. Neuronal associations in the rat suprachiasmatic nucleus demonstrated by immunoelectron microscopy. J. Comp. Neurol. 1992, 325:559-571.
16. Dalton L.D., Carpenter R.G., Grossman S.P. Ingestive behavior in adult rats with dorsomedial hypothalamic lesions. Physiol. Behav. 1981, 26:117-123.
17. Dum R.P., Strick P.L. Frontal lobe inputs to the digit representations of the motor areas on the lateral surface of the hemisphere. J. Neurosci. 2005, 25:1375-1386.
18. Evans J.A., Leise T.L., Castanon-Cervantes O., Davidson A.J. Intrinsic regulation of spatiotemporal organization within the suprachiasmatic nucleus. PLoS ONE 2011, 6:e15869.
19. Fragaszy D.M., Adams-Curtis L.E. Generative aspects of manipulation in tufted capuchin monkeys (Cebus apella). J. Comp. Psychol. 1991, 105:387-397.
20. Gallo R.V. Effect of electrical stimulation of the dorsomedial hypothalamic nucleus on pulsatile LH release in ovariectomized rats. Neuroendocrinology 1981, 32:134-138.
21. Gooley J.J., Schomer A., Saper C.B. The dorsomedial hypothalamic nucleus is critical for the expression of food-entrainable circadian rhythms. Nat. Neurosci. 2006, 9:398-407.
22. Hamada T., Antle M.C., Silver R. Temporal and spatial expression patterns of canonical clock genes and clock-controlled genes in the suprachiasmatic nucleus. Eur. J. Neurosci. 2004, 19:1741-1748.
23. Hofman M.A., Swaab D.F. Alterations in circadian rhythmicity of the vasopressin-producing neurons of the human suprachiasmatic nucleus (SCN) with aging. Brain Res. 1994, 651:134-142.
24. Honma S., Honma K.I., Nagasaka T., Hiroshige T. The ventromedial hypothalamic nucleus is not essential for the prefeeding corticosterone peak in rats under restricted daily feeding. Physiol. Behav. 1987, 39:211-215.
25. Hoorneman E.M.D., Buijs R.M. Vasopressin fibers pathways in the rat brain following suprachiasmatic nucleus lesioning. Brain Res. 1982, 243:235-241.
26. Horst G.J., Luiten P.G. The projections of the dorsomedial hypothalamic nucleus in the rat. Brain Res. Bull. 1986, 16:23-48.
27. Ibata Y., Okamura H., Tanaka M., Tamada Y., Hayashi S., Iijima N., Matsuda T., Munekawa K., Takamatsu T., Hisa Y., Shigeyoshi Y., Amaya F. Functional morphology of the suprachiasmatic nucleus. Front. Neuroendocrinol. 1999, 20:241-268.
28. Jacomy H., Burlet A., Bosler O. Vasoactive intestinal peptide neurons as synaptic targets for vasopressin neurons in the suprachiasmatic nucleus. Double-label immunocytochemical demonstration in the rat. Neuroscience 1999, 88:859-870.
29. Kalsbeek A. SCN outputs and the hypothalamic balance of life. J. Biol. Rhythms 2006, 21:458-469.
30. Kalsbeek A., Teclemariam-Mesbah R., Pevet P. Efferent projections of the suprachiasmatic nucleus in the golden hamster (Mesocricetus auratus). J. Comp. Neurol. 1993, 332:293-314.
31. Kalsbeek A., La Fleur S., Van Heijningen C., Buijs R.M. Suprachiasmatic GABAergic inputs to the paraventricular nucleus control plasma glucose concentrations in the rat via sympathetic innervation of the liver. J. Neurosci. 2004, 24:7604-7613.
32. Kiba T., Tanaka K., Endo O., Inoue S. Role of vagus nerve in increased DNA synthesis after hypothalamic ventromedial lesions in rat liver. Am. J. Physiol. 1992, 262:483-487.
33. Leak R.K., Moore R.Y. Topographic organization of suprachiasmatic nucleus projection neurons. J. Comp. Neurol. 2001, 433:312-334.
34. Lee S.K., Ryu P.D., Lee S.Y. Differential distributions of neuropeptides in hypothalamic paraventricular nucleus neurons projecting to the rostral ventrolateral medulla in the rat. Neurosci. Lett. 2013, 556:160-165.
35. Lu J., Zhang Y.H., Chou T.C., Gaus S.E., Elmquist J.K., Shiromani P., Saper C.B. Contrasting effects of ibotenate lesions of the paraventricular nucleus and subparaventricular zone on sleep-wake cycle and temperature regulation. J. Neurosci. 2001, 21:4864-4874.
36. Lydic R., Albers H.E., Tepper B., Moore-Ede M.C. Three-dimensional structure of the mammalian suprachiasmatic nuclei: a comparative study of five species. J. Comp. Neurol. 1982, 204:225-237.
37. McGinty D., Szymusiak R. Keeping cool: a hypothesis about the mechanisms and functions of slow-wave sleep. Trends Neurosci. 1990, 13:480-487.
38. Manocha S.L., Shantha T.R., Bourne G.H. A Stereotaxic Atlas of the Brain of the Cebus Monkey (Cebus apella) 1968, Clarendon Press, Oxford.
39. Moore-Ede M.C., Sulaman F.M., Fuller C.A. The Clocks That Time Us: Physiology of the Circadian Timing System 1982, Harvard Univ Press, Cambridge.
40. Moore R.Y. The organization of the human circadian system. Prog. Brain Res. 1992, 93:101-117.
41. Moore R.Y. Organization of the primate circadian system. J. Biol. Rhythms 1993, 8:s3-s9.
42. Moore R.Y., Speh J.C. Serotonin innervation of the primate surpachiasmatic nucleus. Brain Res. 2004, 1010:169-173.
43. Moore R.Y., Speh J.C., Leak R.K. Suprachiasmatic nucleus organization. Cell Tissue Res. 2002, 309:89-98.
44. Moore R.Y. The suprachiasmatic nucleus and the circadian timing system. Prog. Mol. Biol. Transl. Sci. 2013, 119:1-28.
45. Mordel J., Karnas D., Pévet P., Isope P., Challet E., Meissl H. The output signal of Purkinje cells of the cerebellum and circadian rhythmicity. PLOS ONE 2013, 8:e58457.
46. Morin L.P. The circadian visual system. Brain Res. Rev. 1994, 67:102-127.
47. Morin L.P., Allen C.N. The circadian visual system. Brain Res. Rev. 2006, 51:1-60.
48. Morin L.P., Blanchard J., Moore R.Y. Intergeniculate leaflet and suprachiasmatic nucleus organization and connections in the golden hamster. Vis. Neurosci. 1992, 8:219-230.
49. Mrosovsky N., Salmon P.A. A behavioural method for accelerating reentrainment of rhythms to new light-dark cycles. Nature 1987, 330:372-373.
50. Paxinos G., Huang X.F., Toga A.W. The Rhesus Monkey Brain in Stereotaxic Coordinates 2000, Academic Press, San Diego, CA.
51. Pinato L., Allemandi W., Abe L.K., Frazão R., Cruz-Rizzolo R.J., Cavalcante J.S., Costa M.S., Nogueira M.I. A comparative study of cytoarchitecture and serotonergic afferents in the suprachiasmatic nucleus of primates (Cebus apella and Callithrix jacchus) and rats (Wistar and Long Evans strains). Brain Res. 2007, 1149:101-110.
52. Pinato L., Frazão R., Cruz-Rizzolo R.J., Cavalcante J.S., Nogueira M.I. Immunocytochemical characterization of the pregeniculate nucleus and distribution of retinal and neuropeptide Y terminals in the suprachiasmatic nucleus of the Cebus monkey. J. Chem. Neuroanat. 2009, 37:207-213.
53. Poulain D.A., Wakerley J.B. Electrophysiology of hypothalamic magnocellular neurones secreting oxytocin and vasopressin. Neuroscience 1982, 7:773-808.
54. Provencio I., Rollag M.D., Castrucci A.M. Photoreceptive net in the mammalian retina. This mesh of cells may explain how some blind mice can still tell day from night. Nature 2002, 415:493.
55. Ramanathan C., Nunez A.A., Martinez G.S., Schwartz M.D., Smale L. Temporal and spatial distribution of immunoreactive PER1 and PER2 proteins in the suprachiasmatic nucleus and peri-suprachiasmatic region of the diurnal grass rat (Arvicanthis niloticus). Brain Res. 2006, 1073-1074:348-358.
56. Reghunandanan V., Reghunandanan R. Neurotransmitters of the suprachiasmatic nuclei. J. Circadian Rhythms 2006, 4:2.
57. Reppert S.M., Weaver D.R. Molecular analysis of mammalian circadian rhythms. Annu. Rev. Physiol. 2001, 63:647-676.
58. Reppert S.M., Weaver D.R. Coordination of circadian timing in mammals. Nature 2002, 418:935-941.
59. Rocha V.A., Frazão R., Campos L.M., Mello P., Donato J., Cruz-Rizzolo R.J., Nogueira M.I., Pinato L. Intrinsic organization of the suprachiasmatic nucleus in the capuchin monkey. Brain Res. 2014, 1543:65-72.
60. Romijn H.J., van Uum J.F., Emmering J., Goncharuk V., Buijs R.M. Colocalization of VIP with VP in neurons of the human paraventricular, supraoptic and suprachiasmatic nucleus. Brain Res. 1999, 832:47-53.
61. Rose S., Novak C.M., Mahoney M.M., Nunez A.A., Smale L. Fos expression within vasopressin-containing neurons in the suprachiasmatic nucleus of diurnal rodents compared to nocturnal rodents. J. Biol. Rhythms 1999, 14:37-46.
62. Ross A.C., Porter L.M., Power M.L., Sodaro V. Maternal care and infant development in Callimico goeldii and Callithrix jacchus. Primates 2010, 51:315-325.
63. Saper C.B. Image is everything. J. Comp. Neurol. 1999, 412:381-382.
64. Saper C.B., Swanson L.W., Cowan W.N. An autoradiographic study of the efferent connections of the hypothalamic area in the rat. J. Comp. Neurol. 1979, 183:689-706.
65. Saper C.B. The central circadian timing system. Curr. Opin. Neurobiol. 2013, 23:747-751.
66. Satinoff E. Neural organization and evolution of thermal regulation in mammals. Science 1978, 201:16-22.
67. Schlenker E.H. Integration in the PVN: another piece of the puzzle. Am. J. Physiol. Regul. Integr. Comp. Physiol. 2005, 289:653-655.
68. Shekhar A., Katner J.S. Dorsomedial hypothalamic GABA regulates anxiety in the social interaction test. Pharmacol. Biochem. Behav. 1995, 50:253-258.
69. Shepherd G.M., Raastad M. Axonal varicosity distributions along parallel fibers: a new angle on a cerebellar circuit. Cerebellum 2003, 2:110-113.
70. Simonneaux V., Ribelayga C. Generation of the melatonin endocrine message in mammals: a review of the complex regulation of melatonin synthesis by norepinephrine, peptides, and other pineal transmitters. Pharmacol. Rev. 2003, 55:325-395.
71. Simerly R.B. Organization and regulation of sexually dimorphic neuroendocrine pathways. Behav. Brain Res. 1998, 92:195-203.
72. Stephan F.K., Berkley K.J., Moss R.L. Efferent connections of the rat suprachiasmatic nucleus. Neuroscience 1981, 6:2625-2641.
73. Swanson L.W., Sawchenko P.E. Paraventricular nucleus: a site for the integration of neuroendocrine and autonomic mechanisms. Neuroendocrinology 1980, 31:410-417.
74. Thompson R.H., Canteras N.S., Swanson L.W. Organization of projections from the dorsomedial nucleus of the hypothalamus: a PHA-L study in the rat. J. Comp. Neurol. 1996, 376:143-173.
75. Trudel E., Bourque C.W. Central clock excites vasopressin neurons by waking osmosensory afferents during late sleep. Nat. Neurosci. 2010, 13:467-474.
76. Ueda S., Kawata M., Sano Y. Identification of serotonin- and vasopressin immunoreactivities in the suprachiasmatic nucleus of four mammalian species. Cell Tissue Res. 1983, 234:237-248.
77. Ueta Y., Dayanithi G., Fujihara H. Hypothalamic vasopressin response to stress and various physiological stimuli: visualization in transgenic animal models. Horm. Behav. 2011, 59:221-226.
78. Van den Pol A.N., Tsujimoto K.L. Neurotransmitters of the hypothalamic suprachiasmatic nucleus: immunocytochemical analysis of 25 neuronal antigens. Neuroscience 1985, 15:1049-1086.
79. Vasalou C., Henson M.A. A multicellular model for differential regulation of circadian signals in the core and shell regions of the suprachiasmatic nucleus. J. Theor. Biol. 2011, 288:44-56.
80. Vida B., Deli L., Hrabovszky E., Kalamatianos T., Caraty A., Coen C.W., Liposits Z., Kalló I. Evidence for suprachiasmatic vasopressin neurons innervating kisspeptin neurons in the rostral periventricular area of the mouse brain: regulation by estrogen. J. Neuroendocrinol. 2010, 22:1032-1039.
81. Watanabe I., Yamada E. The fine structure of lamellated nerve endings found in the rat gingiva. Arch. Histol. Jpn. 1983, 46:173-182.
82. Watts A.G., Swanson L.W. Efferent projection of the suprachiasmatic nucleus II Studies using retrograde transport of Phuorescente Dyes and Simultaneous Peptides Immunohistochemistry in the Rat. J. Comp. Neurol. 1987, 258:230-252.
83. Watts A.G., Swanson L.W. Efferent projection of the suprachiasmatic nucleus: I. Studies using anterograde transport of Phaseolus vulgares leucoagglutinin in the rat. J. Comp. Neurol. 1987, 258:204-229.
84. Watts A.G. The efferent projections of the suprachiasmatic nucleus: anatomical insights into the control of circadian rhythms. Suprachiasmatic Nucleus: The Mind's Clock 1991, 77-106. Oxford Univ Press, New York. D.C. Klein, R.Y. Moore, S.M. Reppert (Eds.).
85. Watson R.E., Langub M.C., Engle M.G., Maley B.E. Estrogen-receptive neurons in the anteroventral periventricular nucleus are synaptic targets of the suprachiasmatic nucleus and peri-suprachiasmatic region. Brain Res. 1995, 689:254-264.
86. Zhang Z.W., Kang J.I., Vaucher E. Axonal varicosity density as an index of local neuronal interactions. PLoS ONE 2011, 6:e22543.