The Retinohypothalamic tract: Comparison of axonal projection patterns from four major targets

Brain Research Reviews

Volumn 65, Issue 2, 2011, Pages 150-183

  Canteras, Newton S ^a   Ribeiro Barbosa, Érika Renata ^a   Goto, Marina ^a   Cipolla Neto, José ^a   Swanson, Larry W ^b  

^a UNIVERSITY OF SÃO PAULO   (Brazil)

^b UNIVERSITY OF SOUTHERN CALIFORNIA   (United States)

Author keywords

Anterior hypothalamic nucleus; Lateral hypothalamic area; Subparaventricular zone; Suprachiasmatic nucleus

Indexed keywords

CHOLERA TOXIN B SUBUNIT;

BEHAVIOR CONTROL; BRAIN REGION; CIRCADIAN RHYTHM; GENE EXPRESSION; HYPOTHALAMUS; IMMUNOHISTOCHEMISTRY; IMMUNOREACTIVITY; NERVE CELL MEMBRANE POTENTIAL; NERVE PROJECTION; NONHUMAN; OPTIC TRACT; PRIORITY JOURNAL; PROTEIN TRANSPORT; RETINA; RETINOHYPOTHALAMIC TRACT; REVIEW; SYNAPTIC TRANSMISSION;

ANIMALS; ANTERIOR HYPOTHALAMIC NUCLEUS; AXONS; BEHAVIOR, ANIMAL; CIRCADIAN RHYTHM; HYPOTHALAMIC AREA, LATERAL; HYPOTHALAMUS; MALE; NEUROANATOMICAL TRACT-TRACING TECHNIQUES; RATS; RATS, WISTAR; RETINA; SUPRACHIASMATIC NUCLEUS; VISUAL PATHWAYS;

EID: 78649904288     PISSN: 01650173     EISSN: 18726321     Source Type: Journal    
DOI: 10.1016/j.brainresrev.2010.09.006     Document Type: Review

References (160)

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. Antle M.C., Silver R. Orchestrating time: arrangements of the brain circadian clock. Trends Neurosci. 2005, 28:145-151.
3. Arvanitogiannis A., Robinson B., Beaulé C., Amir S. Calbindin-D28k immunoreactivity in the suprachiasmatic nucleus and the circadian response to constant light in the rat. Neuroscience 2000, 99:397-401.
4. Aston-Jones G., Cohen J.D. Adaptive gain and the role of the locus coeruleus-norepinephrine system in optimal performance. J. Comp. Neurol. 2005, 493:99-110.
5. Behbehani M.M. Functional characteristics of the midbrain periaqueductal gray. Prog. Neurobiol. 1995, 46:575-605.
6. Blanchard D.C., Li C.I., Hubbard D., Markham C.M., Yang M., Takahashi L.K., Blanchard R.J. Dorsal premammillary nucleus differentially modulates defensive behaviors induced different threat stimuli in rats. Neurosci. Lett. 2003, 345:145-148.
7. Blok B.F., Holstege G. The neuronal control of micturition and its relation to the emotional motor system. Prog. Brain Res. 1996, 107:113-126.
8. Bourque C.W., Oliet S.H. Osmoreceptors in the central nervous system. Annu. Rev. Physiol. 1997, 59:601-619.
9. Buijs R.M., Markman M., Nunes-Cardoso B., Hou Y.X., Shinn S. Projections of the suprachiasmatic nucleus to stress-related areas in the rat hypothalamus: a light and electron microscopic study. J. Comp. Neurol. 1993, 335:42-54.
10. Buijs R.M., Hou Y.X., Shinn S., Renaud L.P. Ultrastructural evidence for intra- and extranuclear projections of GABAergic neurons of the suprachiasmatic nucleus. J. Comp. Neurol. 1994, 340:381-391.
11. Cameron A.A., Khan I.A., Westlund K.N., Willis W.D. The efferent projections of the periaqueductal gray in the rat: a Phaseolus vulgarisleucoagglutinin study. II. Descending projections. J. Comp. Neurol. 1995, 351:585-601.
12. Canteras N.S. The medial hypothalamic defensive system: hodological organization and functional implications. Pharmacol. Biochem. Behav. 2002, 71:481-491.
13. Canteras N.S., Goto M. Connections of the precommissural nucleus. J. Comp. Neurol. 1999, 408:23-45.
14. Canteras N.S., Swanson L.W. Projections of the ventral subiculum to the amygdala, septum, and hypothalamus: a PHAL anterograde tract-tracing study in the rat. J. Comp. Neurol. 1992, 324:180-194.
15. Canteras N.S., Simerly R.B., Swanson L.W. Connections of the posterior nucleus of the amygdala. J. Comp. Neurol. 1992, 324:143-179.
16. Canteras N.S., Simerly R.B., Swanson L.W. Organization of projections from the ventromedial nucleus of the hypothalamus: a Phaseolus vulgaris-leucoagglutinin study in the rat. J. Comp. Neurol. 1994, 348:41-79.
17. Canteras N.S., Simerly R.B., Swanson L.W. Organization of projections from the medial nucleus of the amygdala: a PHAL study in the rat. J. Comp. Neurol. 1995, 360:213-245.
18. Canteras N.S., Chiavegatto S., Valle L.E., Swanson L.W. Severe reduction of rat defensive behavior to a predator by discrete hypothalamic chemical lesions. Brain Res. Bull. 1997, 44:297-305.
19. Card J.P., Moore R.Y. The suprachiasmatic nucleus of the golden hamster: immunohistochemical analysis of cell and fiber distribution. Neuroscience 1984, 13:415-431.
20. Card J.P., Moore R.Y. Organization of lateral geniculate-hypothalamic connections in the rat. J. Comp. Neurol. 1989, 284:135-147.
21. Card J.P., Brecha N., Karten H.J., Moore R.Y. Immunocytochemical localization of vasoactive intestinal polypeptide-containing cells and processes in the suprachiasmatic nucleus of the rat: light and electron microscopic analysis. J. Neurosci. 1981, 1:1289-1303.
22. Carrive P., Bandler R. Viscerotopic organization of neurons subserving hypotensive reactions within the midbrain periaqueductal grey: a correlative functional and anatomical study. Brain Res. 1991, 541:206-215.
23. Cezario A.F., Ribeiro-Barbosa E.R., Baldo M.V., Canteras N.S. Hypothalamic sites responding to predator threats-the role of the dorsal premammillary nucleus in unconditioned and conditioned antipredatory defensive behavior. Eur. J. Neurosci. 2008, 28:1003-1015.
24. Cheng M.Y., Bullock C.M., Li C., Lee A.G., Bermak J.C., Belluzzi J., Weaver D.R., Leslie F.M., Zhou Q.Y. Prokineticin 2 transmits the behavioural circadian rhythm of the suprachiasmatic nucleus. Nature 2002, 417:405-410.
25. Chou T.C., Bjorkum A.A., Gaus S.E., Lu J., Scammell T.E., Saper C.B. Afferents to the ventrolateral preoptic nucleus. J. Neurosci. 2002, 22:977-990.
26. 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.
27. Comoli E., Ribeiro-Barbosa E.R., Canteras N.S. Afferent connections of the dorsal premammillary nucleus. J. Comp. Neurol. 2000, 423:83-98.
28. Conrad C.D., Stumpf W.E. Endocrine-optic pathways to the hypothalamus. Anat. Neuroendocrinology, Int. Conf. Neurobiology of CNS-Hormone Interactions, Chapel Hill 1974 1975, 62-68. Karger, Basel.
29. Coolen L.M., Peters H.J., Veening J.G. Fos immunoreactivity in the rat brain following consummatory elements of sexual behavior: a sex comparison. Brain Res. 1996, 738:67-82.
30. Costa M.S., Santee U.R., Cavalcante J.S., Moraes P.R., Santos N.P., Britto L.R. Retinohypothalamic projections in the common marmoset (Callithrix jacchus): a study using cholera toxin subunit B. J. Comp. Neurol. 1999, 415:393-403.
31. Damiola F., Le Minh N., Preitner N., Kornmann B., Fleury-Olela F., Schibler U. Restricted feeding uncouples circadian oscillators in peripheral tissues from the central pacemaker in the suprachiasmatic nucleus. Genes Dev. 2000, 14:2950-2961.
32. Denton D.A., McKinley M.J., Weisinger R.S. Hypothalamic integration of body fluid regulation. Proc. Natl Acad. Sci. USA 1996, 93:7397-7404.
33. Deurveilher S., Semba K. Indirect projections from the suprachiasmatic nucleus to major arousal-promoting cell groups in rat: implications for the circadian control of behavioural state. Neuroscience 2005, 130:165-183.
34. Dielenberg R.A., Hunt G.E., McGregor I.S. "When a rat smells a cat": the distribution of c-fos expression in rat brain following exposure to a predator odor. Neuroscience 2001, 104:1085-1097.
35. Dong H.W., Swanson L.W. Projections from bed nuclei of the stria terminalis, posterior division: implications for cerebral hemisphere regulation of defensive and reproductive behaviors. J. Comp. Neurol. 2004, 471:396-433.
36. Dong H.W., Swanson L.W. Projections from bed nuclei of the stria terminalis, dorsomedial nucleus: implications for cerebral hemisphere integration of neuroendocrine, autonomic, and drinking responses. J. Comp. Neurol. 2006, 494:75-107.
37. Dong H.W., Swanson L.W. Projections from bed nuclei of the stria terminalis, magnocellular nucleus: implications for cerebral hemisphere regulation of micturition, defecation, and penile erection. J. Comp. Neurol. 2006, 494:108-141.
38. Edgar D.K., Martin C.E., Dement W.C. Activity feedback to the mammalian circadian pacemaker: influence on observed measures of rhythm period length. J. Biol. Rhythms 1991, 6:185-199.
39. Farkas E., Jansen A.S., Loewy A.D. Periaqueductal gray matter projection to vagal preganglionic neurons and the nucleus tractus solitarius. Brain Res. 1997, 764:257-261.
40. Farkas E., Jansen A.S., Loewy A.D. Periaqueductal gray matter input to cardiac-related sympathetic premotor neurons. Brain Res. 1998, 792:179-192.
41. Fite K.V., Janusonis S. Optic afferents to the parabrachial nucleus. Brain Res. 2002, 943:9-14.
42. Fitzsimons J.T. Angiotensin, thirst, and sodium appetite. Physiol. Ver. 1998, 78:583-686.
43. García-Horsman S.P., Agmo A., Paredes R.G. Infusions of naloxone into the medial preoptic area, ventromedial nucleus of the hypothalamus, and amygdala block conditioned place preference induced by paced mating behavior. Horm. Behav. 2008, 54:709-716.
44. Gaus S.E., Strecker R.E., Tate B.A., Parker R.A., Saper C.B. Ventrolateral preoptic nucleus contains sleep-active, galaninergic neurons in multiple mammalian species. Neuroscience 2002, 115:285-294.
45. Gerfen C.R., Sawchenko P.E. An anterograde neuroanatomical tracing method that shows the detailed morphology of neurons, their axons and terminals: immunohistochemical localization of an axonally transported plant lectin, Phaseolus vulgaris leucoagglutinin (PHA-L). Brain Res. 1984, 290:219-238.
46. Grindstaff R.R., Cunningham J.T. Cardiovascular regulation of vasopressin neurons in the supraoptic nucleus. Exp. Neurol. 2001, 171:219-226.
47. Guarraci F.A., Frohardt R.J., Hines D., Navaira E., Smith J., Wampler L. Intracranial infusions of amphetamine into the medial preoptic area but not the nucleus accumbens affect paced mating behavior in female rats. Pharmacol. Biochem. Behav. 2008, 89:253-262.
48. Hahn J.D., Swanson L.W. Distinct patterns of neural inputs and outputs of the juxtaparaventricular and suprafornical regions of the lateral hypothalamic area in the male rat. Brain Res. Rev. 2010, 64:14-103.
49. Hallanger A.E., Wainer B.H. Ascending projections from the pedunculopontine tegmental nucleus and the adjacent mesopontine tegmentum in the rat. J. Comp. Neurol. 1988, 274:483-515.
50. Hamada T., LeSauter J., Venuti J.M., Silver R. Expression of Period genes: rhythmic and nonrhythmic compartments of the suprachiasmatic nucleus pacemaker. J. Neurosci. 2001, 21:7742-7750.
51. 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.
52. Harris G.C., Wimmer M., Aston-Jones G. A role for lateral hypothalamic orexin neurons in reward seeking. Nature 2005, 437:556-559.
53. Hendrickson A.E., Wagoner N., Cowan W.M. An autoradiographic and electron microscopic study of retino-hypothalamic connections. Z. Zellforsch. Mikrosk. Anat. 1972, 135:1-26.
54. Herbert H., Moga M.M., Saper C.B. Connections of the parabrachial nucleus with the nucleus of the solitary tract and the medullary reticular formation in the rat. J. Comp. Neurol. 1990, 293:540-580.
55. Hull E.M., Dominguez J.M. Getting his act together: roles of glutamate, nitric oxide, and dopamine in the medial preoptic area. Brain Res. 2006, 1126:66-75.
56. Hull E.M., Wood R.I., McKenna K.E. The neurobiology of male sexual behavior. Knobil and Neill's Physiology of Reproduction 2005, 1729-1824. Academic Press, San Diego, New York. third ed. J.D. Neill (Ed.).
57. Jacobowitz D.M., Winsky L. Immunocytochemical localization of calretinin in the forebrain of the rat. J. Comp. Neurol. 1991, 304:198-218.
58. Johnson R.F., Morin L.P., Moore R.Y. Retinohypothalamic projections in the hamster and rat demonstrated using cholera toxin. Brain Res. 1988, 462:301-312.
59. 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.
60. Kelly A.B., Watts A.G. The mediation of dehydration-induced peptidergic gene expression in the rat lateral hypothalamic area by forebrain afferent projections. J. Comp. Neurol. 1996, 370:231-246.
61. Kollack-Walker S., Newman S.W. Mating and agonistic behavior produce different patterns of Fos immunolabeling in the male Syrian hamster brain. Neuroscience 1995, 66:721-736.
62. Kollack-Walker S., Watson S.J., Akil H. Social stress in hamsters: defeat activates specific neurocircuits within the brain. J. Neurosci. 1997, 17:8842-8855.
63. Kollack-Walker S., Don C., Watson S.J., Akil H. Differential expression of c-fos mRNA within neurocircuits of male hamsters exposed to acute or chronic defeat. J. Neuroendocrinol. 1999, 11:547-559.
64. Kramer A., Yang F.C., Snodgrass P., Li X., Scammell T.E., Davis F.C., Weitz C.J. Regulation of daily locomotor activity and sleep by hypothalamic EGF receptor signaling. Science 2001, 294:2511-2515.
65. Kraves S., Weitz C.J. A role for cardiotrophin-like cytokine in the circadian control of mammalian locomotor activity. Nat. Neurosci. 2006, 9:212-219.
66. Krieger D.T. Ventromedial hypothalamic lesions abolish food-shifted circadian adrenal and temperature rhythmicity. Endocrinology 1980, 106:649-654.
67. Krieger D.T., Hauser H., Krey L.C. Suprachiasmatic nuclear lesions do not abolish food-shifted circadian adrenal and temperature rhythmicity. Science 1977, 197:398-399.
68. Kriegsfeld L.J., Leak R.K., Yackulic C.B., LeSauter J., Silver R. Organization of suprachiasmatic nucleus projections in Syrian hamsters (Mesocricetus auratus): an anterograde and retrograde analysis. J. Comp. Neurol. 2004, 468:361-379.
69. Landry G.J., Yamakawa G.R., Mistlberger R.E. Robust food anticipatory circadian rhythms in rats with complete ablation of the thalamic paraventricular nucleus. Brain Res. 2007, 1141:108-118.
70. Larsen P.J., Enquist L.W., Card J.P. Characterization of the multisynaptic neuronal control of the rat pineal gland using viral transneuronal tracing. Eur. J. Neurosci. 1998, 10:128-145.
71. Leak R.K., Moore R.Y. Identification of retinal ganglion cells projecting to the lateral hypothalamic area of the rat. Brain Res. 1997, 770:105-114.
72. Leak R.K., Moore R.Y. Topographic organization of suprachiasmatic nucleus projection neurons. J. Comp. Neurol. 2001, 433:312-334.
73. Leak R.K., Card J.P., Moore R.Y. Suprachiasmatic pacemaker organization analyzed by viral transynaptic transport. Brain Res. 1999, 819:23-32.
74. Levine J.D., Weiss M.L., Rosenwasser A.M., Miselis R.R. Retinohypothalamic tract in the female albino rat: a study using horseradish peroxidase conjugated to cholera toxin. J. Comp. Neurol. 1991, 306:344-360.
75. Loewy A.D., Saper C.B., Baker R.P. Descending projections from the pontine micturition center. Brain Res. 1979, 172:533-538.
76. Lonstein J.S., Stern J.M. Site and behavioral specificity of periaqueductal gray lesions on postpartum sexual, maternal, and aggressive behaviors in rats. Brain Res. 1998, 804:21-35.
77. Lu J., Greco M.A., Shiromani P., Saper C.B. Effect of lesions of the ventrolateral preoptic nucleus on NREM and REM sleep. J. Neurosci. 2000, 20:3830-3842.
78. 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.
79. Lu J., Bjorkum A.A., Xu M., Gaus S.E., Shiromani P.J., Saper C.B. Selective activation of the extended ventrolateral preoptic nucleus during rapid eye movement sleep. J. Neurosci. 2002, 22:4568-4576.
80. Mai J.K. Distribution of retinal axons within the lateral hypothalamic area. Exp. Brain Res. 1979, 34:373-377.
81. McKinley M.J., Pennington G.L., Oldfield B.J. Anteroventral wall of the third ventricle and dorsal lamina terminalis: headquarters for control of body fluid homeostasis?. Clin. Exp. Pharmacol. Physiol. 1996, 23:271-281.
82. McKinley M.J., Allen A.M., Burns P., Colvill L.M., Oldfield B.J. Interaction of circulating hormones with the brain: the roles of the subfornical organ and the organum vasculosum of the lamina terminalis. Clin. Exp. Pharmacol. Physiol. Suppl. 1998, 25:S61-S67.
83. Meyer-Berstein E.L., Jetton A.E., Matsumoto S.I., Markuns J.F., Lehman M.N., Bittman E.L. Effects of suprachiasmatic transplants on circadian rhythms of neuroendocrine function in golden hamsters. Endocrinology 1999, 140:207-218.
84. Mikkelsen J.D., Vrang N. A direct pretectosuprachiasmatic projection in the rat. Neuroscience 1994, 62:497-505.
85. Mikkelsen J.D., Larsen P.J., O'Hare M.M., Wiegand S.J. Gastrin releasing peptide in the rat suprachiasmatic nucleus: an immunohistochemical, chromatographic and radioimmunological study. Neuroscience 1991, 40:55-66.
86. Mistlberger R.E. Circadian food-anticipatory activity: formal models and physiological mechanisms. Neurosci. Biobehav. Rev. 1994, 18:171-195.
87. Mistlberger R.E. Food-anticipatory circadian rhythms: concepts and methods. Eur. J. Neurosci. 2009, 30:1718-1729.
88. Moga M.M., Moore R.Y. Organization of neural inputs to the suprachiasmatic nucleus in the rat. J. Comp. Neurol. 1997, 389:508-534.
89. Moga M.M., Moore R.Y. Paraventricular thalamus lesions alter circadian period and activity distribution in the blinded rat. Biol. Rhythm Res. 2000, 31:212-219.
90. Moore R.Y., Eichler V.B. Loss of a circadian adrenal corticosterone rhythm following suprachiasmatic lesions in the rat. Brain Res. 1972, 42:201-206.
91. Moore R.Y., Lenn N.J. A retinohypothalamic projection in the rat. J. Comp. Neurol. 1972, 146:1-14.
92. Moore R.Y., Halaris A.E., Jones B.E. Serotonin neurons of the midbrain raphe: ascending projections. J. Comp. Neurol. 1978, 180:417-438.
93. Moore R.Y., Speh J.C., Card J.P. The retinohypothalamic tract originates from a distinct subset of retinal ganglion cells. J. Comp. Neurol. 1995, 352:351-366.
94. Moore R.Y., Speh J.C., Leak R.K. Suprachiasmatic nucleus organization. Cell Tissue Res. 2002, 309:89-98.
95. Morin L.P., Goodless-Sanchez N., Smale L., Moore R.Y. Projections of the suprachiasmatic nuclei, subparaventricular zone and retrochiasmatic area in the golden hamster. Neuroscience 1994, 61:391-410.
96. Morin L.P., Shivers K.Y., Blanchard J.H., Muscat L. Complex organization of mouse and rat suprachiasmatic nucleus. Neuroscience 2006, 137:1285-1297.
97. Mota S.R., Canteras N.S., Bartol I., Skorupa A.L., Scialfa J.H., Terra I.M., Afeche S.C., Cipolla-Neto J. Lesions of the dorsomedial hypothalamic nucleus do not influence the daily profile of pineal metabolism in rats. Neuroendocrinology 2001, 73:123-128.
98. Mota-Ortiz S.R., Sukikara M.H., Felicio L.F., Canteras N.S. Afferent connections to the rostrolateral part of the periaqueductal gray: a critical region influencing the motivation drive to hunt and forage. Neural Plast. 2009, 2009:612698.
99. Motta S.C., Goto M., Gouveia F.V., Baldo M.V., Canteras N.S., Swanson L.W. Dissecting the brain's fear system reveals the hypothalamus is critical for responding in subordinate conspecific intruders. Proc. Natl Acad. Sci. USA 2009, 106:4870-4875.
100. Munch I.C., Moller M., Larsen P.J., Vrang N. Light-induced c-Fos expression in suprachiasmatic nuclei neurons targeting the paraventricular nucleus of the hamster hypothalamus: phase dependence and immunochemical identification. J. Comp. Neurol. 2002, 442:48-62.
101. Murakami D.M., Miller J.D., Fuller C.A. The retinohypothalamic tract in the cat: retinal ganglion cell morphology and pattern of projection. Brain Res. 1989, 482:283-296.
102. Murphy A.Z., Hoffman G.E. Distribution of gonadal steroid receptor-containing neurons in the preoptic-periaqueductal gray-brainstem pathway: a potential circuit for the initiation of male sexual behavior. J. Comp. Neurol. 2001, 438:191-212.
103. Novak C.M., Nunez A.A. A sparse projection from the suprachiasmatic nucleus to the sleep-active ventrolateral preoptic area in the rat. NeuroReport 2000, 11:93-96.
104. Numan M. Hypothalamic neural circuits regulating maternal responsiveness toward infants. Behav. Cogn. Neurosci. Rev. 2006, 5:163-190.
105. Nunez A.A., Stephan F.K. The effects of hypothalamic knife cuts on drinking rhythms and the estrous cycle of the rat. Behav. Biol. 1977, 20:224-234.
106. Paredes R.G., Highland L., Karam P. Socio-sexual behavior in male rats after lesions of the medial preoptic area: evidence for reduced sexual motivation. Brain Res. 1993, 618:271-276.
107. Paredes R.G., Tzschentke T., Nakach N. Lesions of the medial preoptic area anterior hypothalamus (MPOA/AH) modify partner preference in male rats. Brain Res. 1998, 813:1-8.
108. Pavcovich L.A., Yang M., Miselis R.R., Valentino R.J. Novel role for the pontine micturition center, Barrington's nucleus: evidence for coordination of colonic and forebrain activity. Brain Res. 1998, 784:355-361.
109. Pfaff D.W., Sakuma Y. Facilitation of the lordosis reflex of female rats from the ventromedial nucleus of the hypothalamus. J. Physiol. 1979, 288:189-202.
110. Pfaff D.W., Sakuma Y. Deficit in the lordosis reflex of female rats caused by lesions in the ventromedial nucleus of the hypothalamus. J. Physiol. 1979, 288:203-210.
111. Pfaus J.G., Phillips A.G. Role of dopamine in anticipatory and consummatory aspects of sexual behavior in the male rat. Behav. Neurosci. 1991, 105:727-743.
112. Plano S.A., Golombek D.A., Chiesa J.J. Circadian entrainment to light-dark cycles involves extracellular nitric oxide communication within the suprachiasmatic nuclei. Eur. J. Neurosci. 2010, 31:876-882.
113. Reppert S.M., Weaver D.R. Molecular analysis of mammalian circadian rhythms. Annu. Rev. Physiol. 2001, 63:647-676.
114. Risold P.Y., Swanson L.W. Connections of the rat lateral septal complex. Brain Res. Brain Res. Rev. 1997, 24:115-195.
115. Risold P.Y., Canteras N.S., Swanson L.W. Organization of projections from the anterior hypothalamic nucleus: a Phaseolus vulgaris-leucoagglutinin study in the rat. J. Comp. Neurol. 1994, 348:1-40.
116. Roland B.L., Sawchenko P.E. Local origins of some GABAergic projections to the paraventricular and supraoptic nuclei of the hypothalamus in the rat. J. Comp. Neurol. 1993, 332:123-143.
117. Romijn H.J., Sluiter A.A., Pool C.W., Wortel J., Buijs R.M. Differences in colocalization between Fos and PHI, GRP, VIP and VP in neurons of the rat suprachiasmatic nucleus after a light stimulus during the phase delay versus the phase advance period of the night. J. Comp. Neurol. 1996, 372:1-8.
118. Rusak B., Zucker I. Neural regulation of circadian rhythms. Physiol. Rev. 1979, 59:449-526.
119. Salazar-Juarez A., Escobar C., Aguilar-Roblero R. Anterior paraventricular thalamus modulates light-induced phase shifts in circadian rhythmicity in rats. Am. J. Physiol. Regul. Integr. Comp. Physiol. 2002, 283:R897-R904.
120. Saper C.B., Levisohn D. Afferent connections of the median preoptic nucleus in the rat: anatomical evidence for a cardiovascular integrative mechanism in the anteroventral third ventricular (AV3V) region. Brain Res. 1983, 288:21-31.
121. Saper C.B., Lu J., Chou T.C., Gooley J. The hypothalamic integrator for circadian rhythms. Trends Neurosci. 2005, 28:152-157.
122. Satoh K., Fibiger H.C. Cholinergic neurons of the laterodorsal tegmental nucleus: efferent and afferent connections. J. Comp. Neurol. 1986, 253:277-302.
123. Satoh K., Shimizu M., Tohyama M., Maeda T. Localization of the micturition reflex center at dorsolateral pontine tegmentum of the rat. Neurosci. Lett. 1978, 8:27-33.
124. Sherin J.E., Shiromani P.J., McCarley R.W., Saper C.B. Activation of ventrolateral preoptic neurons during sleep. Science 1996, 271:216-219.
125. Sherin J.E., Elmquist J.K., Torrealba F., Saper C.B. Innervation of histaminergic tuberomammillary neurons by GABAergic and galaninergic neurons in the ventrolateral preoptic nucleus of the rat. J. Neurosci. 1998, 18:4705-4721.
126. Silver R., LeSauter J., Tresco P.A., Lehman M.N. A diffusible coupling signal from the transplanted suprachiasmatic nucleus controlling circadian locomotor rhythms. Nature 1996, 382:810-813.
127. Silver R., Romero M.T., Besmer H.R., Leak R., Nunez J.M., LeSauter J. Calbindin-D28K cells in the hamster SCN express light-induced Fos. NeuroReport 1996, 7:1224-1228.
128. Simerly R.B., Chang C., Muramatsu M., Swanson L.W. Distribution of androgen and estrogen receptor mRNA-containing cells in the rat brain: an in situ hybridization study. J. Comp. Neurol. 1990, 294:76-95.
129. Speh J.C., Moore R.Y. Retinohypothalamic tract development in the hamster and rat. Brain Res. Dev. Brain Res. 1993, 76:171-181.
130. Stephan F.K. The "other" circadian system: food as a Zeitgeber. J. Biol. Rhythms 2002, 17:284-292.
131. Stephan F.K., Zucker I. Circadian rhythms in drinking behavior and locomotor activity of rats are eliminated by hypothalamic lesions. Proc. Natl Acad. Sci. USA 1972, 69:1583-1586.
132. Stokkan K.A., Yamazaki S., Tei H., Sakaki Y., Menaker M. Entrainment of the circadian clock in the liver by feeding. Science 2001, 291:490-493.
133. Stopa E.G., Minamitani N., Jonassen J.A., King J.C., Wolfe H., Mobtaker H., Albers H.E. Localization of vasoactive intestinal peptide and peptide histidine isoleucine immunoreactivity and mRNA within the rat suprachiasmatic nucleus. Brain Res. 1988, 464:319-325.
134. Sukikara M.H., Mota-Ortiz S.R., Baldo M.V., Felicio L.F., Canteras N.S. A role for the periaqueductal gray in switching adaptive behavioral responses. J. Neurosci. 2006, 26:2583-2589.
135. Swanson L.W. An autoradiographic study of the efferent connections of the preoptic region in the rat. J. Comp. Neurol. 1976, 167:227-256.
136. Swanson L.W. Cerebral hemisphere regulation of motivated behavior. Brain Res. 2000, 886:113-164.
137. Swanson L.W. Brain Maps: Structure of the Rat Brain 2004, 1-215. Academic Press. 3rd edition.
138. Swanson L.W., Cowan W.M. The efferent connections of the suprachiasmatic nucleus of the hypothalamus. J. Comp. Neurol. 1975, 160:1-12.
139. Swanson L.W., Lind R.W. Neural projections subserving the initiation of a specific motivated behavior in the rat: new projections from the subfornical organ. Brain Res. 1986, 379:399-403.
140. Swanson L.W., Cowan W.M., Jones E.G. An autoradiographic study of the efferent connections of the ventral lateral geniculate nucleus in the albino rat and the cat. J. Comp. Neurol. 1974, 156:143-163.
141. Swanson L.W., Sanchez-Watts G., Watts A.G. Comparison of melanin-concentrating hormone and hypocretin/orexin mRNA expression patterns in a new parceling scheme of the lateral hypothalamic zone. Neurosci. Lett. 2005, 387:80-84.
142. Teclemariam-Mesbah R., Kalsbeek A., Pevet P., Buijs R.M. Direct vasoactive intestinal polypeptide-containing projection from the suprachiasmatic nucleus to spinal projecting hypothalamic paraventricular neurons. Brain Res. 1997, 748:71-76.
143. Thompson R.H., 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. 1998, 27:89-118.
144. Thompson R.H., Swanson L.W. Structural characterization of a hypothalamic visceromotor pattern generator network. Brain Res. Brain Res. Rev. 2003, 41:153-202.
145. 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.
146. Valentino R.J., Page M.E., Luppi P.H., Zhu Y., Van Bockstaele E., Aston-Jones G. Evidence for widespread afferents to Barrington's nucleus, a brainstem region rich in corticotrophin releasing hormone neurons. Neuroscience 1994, 62:125-143.
147. Valentino R.J., Kosboth M., Colflesh M., Miselis R.R. Transneuronal labeling from the rat distal colon: anatomic evidence for regulation of distal colon function by a pontine corticotropin-releasing factor system. J. Comp. Neurol. 2000, 417:399-414.
148. Van Bockstaele E.J., Aston-Jones G., Pieribone V.A., Ennis M., Shipley M.T. Subregions of the periaqueductal gray topographically innervate the rostral ventral medulla in the rat. J. Comp. Neurol. 1991, 309:305-327.
149. 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.
150. Vandesande F., Dierickx K., De Mey J. Identification of separate vasopressin-neurophysin II and oxytocin-neurophysin I containing nerve fibres in the external region of the bovine median eminence. Cell Tissue Res. 1975, 158:509-516.
151. Vertes R.P., Hoover W.B. Projections of the paraventricular and paratenial nuclei of the dorsal midline thalamus in the rat. J. Comp. Neurol. 2008, 508:212-237.
152. Vertes R.P., Kocsis B. Brainstem-diencephalo-septohippocampal systems controlling the theta rhythm of the hippocampus. Neuroscience 1997, 81:893-926.
153. Vertes R.P., Crane A.M., Colom L.V., Bland B.H. Ascending projections of the posterior nucleus of the hypothalamus: PHA-L analysis in the rat. J. Comp. Neurol. 1995, 359:90-116.
154. Vertes R.P., Fortin W.J., Crane A.M. Projections of the median raphe nucleus in the rat. J. Comp. Neurol. 1999, 407:555-582.
155. Vertes R.P., Hoover W.B., Do Valle A.C., Sherman A., Rodriguez J.J. Efferent projections of reuniens and rhomboid nuclei of the thalamus in the rat. J. Comp. Neurol. 2006, 499:768-796.
156. Vrang N., Larsen P.J., Mikkelsen J.D. Direct projection from the suprachiasmatic nucleus to hypophysiotrophic corticotropin-releasing factor immunoreactive cells in the paraventricular nucleus of the hypothalamus demonstrated by means of Phaseolus vulgarisleucoagglutinin tract tracing. Brain Res. 1995, 684:61-69.
157. Watts A.G., 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. 1987, 258:230-252.
158. Watts A.G., Swanson L.W., 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.
159. Yan L., Okamura H. Gradients in the circadian expression of Per1 and Per2 genes in the rat suprachiasmatic nucleus. Eur. J. Neurosci. 2002, 15:1153-1162.
160. Yan L., Silver R. Differential induction and localization of mPer1 and mPer2 during advancing and delaying phase shifts. Eur. J. Neurosci. 2002, 16:1531-1540.