Reciprocal connections between the suprachiasmatic nucleus and the midbrain raphe nuclei: A putative role in the circadian control of behavioral states

Serotonin and Sleep: Molecular, Functional and Clinical Aspects

Volumn , Issue , 2008, Pages 103-131

  Deurveilher, Samüel ^a   Semba, Kazue ^a  

^a DALHOUSIE UNIVERSITY   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

EID: 84867608519     PISSN: None     EISSN: None     Source Type: Book    
DOI: 10.1007/978-3-7643-8561-3_4     Document Type: Chapter

References (169)

1. Moore RY, Leak RH (2001) Suprachiasmatic nucleus in circadian clocks. In: JS Takahashi, FW Turek, RY Moore (eds): Handbook of Behavioral Neurobiology, vol. 12. Kluwer Academic/Plenum Publishers, New York, 141-179
2. Rusak B, Zucker I (1979) Neural regulation of circadian rhythms. Physiol Rev 59: 449-526
3. Guilding C, Piggins HD (2007) Challenging the omnipotence of the suprachiasmatic timekeeper: are circadian oscillators present throughout the mammalian brain? Eur J Neurosci 25: 3195-3216
4. Ibuka N, Kawamura H (1975) Loss of circadian rhythm in sleep-wakefulness cycle in the rat by suprachiasmatic nucleus lesions. Brain Res 96: 76-81
5. Mouret J, Coindet J, Debilly G, Chouvet G (1978) Suprachiasmatic nuclei lesions in the rat: alterations in sleep circadian rhythms. Electroencephalogr Clin Neurophysiol 45: 402-408
6. Mendelson WB, Bergmann BM, Tung A (2003) Baseline and post-deprivation recovery sleep in SCN-lesioned rats. Brain Res 980: 185-190
7. Eastman CI, Mistlberger RE, Rechtschaffen A (1984) Suprachiasmatic nuclei lesions eliminate circadian temperature and sleep rhythms in the rat. Physiol Behav 32: 357-368
8. Wurts SW, Edgar DM (2000) Circadian and homeostatic control of rapid eye movement (REM) sleep: promotion of REM tendency by the suprachiasmatic nucleus. J Neurosci 20: 4300-4210
9. Edgar D, Dement W, Fuller C (1993) Effect of SCN lesions in squirrel monkeys: evidence for opponent processes in sleep-wake regulation. J Neurosci 13: 1065-1079
10. Easton A, Meerlo P, Bergmann B, Turek FW (2004) The suprachiasmatic nucleus regulates sleep timing and amount in mice. Sleep 27: 1307-1318
11. Mistlberger RE (2005) Circadian regulation of sleep in mammals: role of the suprachiasmatic nucleus. Brain Res Rev 49: 429-454
12. Pace-Schott EF, Hobson JA (2002) The neurobiology of sleep: genetics, cellular physiology and subcortical networks. Nat Rev Neurosci 3: 591-605
13. Jones BE (2005) From waking to sleeping: neuronal and chemical substrates. Trends Pharmacol Sci 26: 578-586
14. Watts AG (1991) The efferent projections of the suprachiasmatic nucleus: Anatomical insights into the control of circadian rhythms in suprachiasmatic nucleus. In: DC Klein, RY Moore, SM Reppert (eds): The mind's clock. Oxford University Press, New York, 77-106
15. Card JP (1999) Anatomy of the mammalian circadian timekeeping system. In: R Lydic, HA Baghdoyan (eds): Handbook of behavioral state control: Cellular and molecular mechanisms. CRC Press, Boca Raton, 13-29
16. Morin LP, Allen CN (2006) The circadian visual system, 2005. Brain Res Rev 51: 1-60
17. McGinty D, Szymusiak R (2001) Brain structures and mechanisms involved in the generation of NREM sleep: focus on the preoptic hypothalamus. Sleep Med Rev 5: 323-342
18. Novak CM, Nunez AA (2000) A sparse projection from the suprachiasmatic nucleus to the sleep active ventrolateral preoptic area in the rat. Neuroreport 11: 93-96
19. Chou TC, Bjorkum AA, Gaus SE, Lu J, Scammell TE, Saper CB (2002) Afferents to the ventrolateral preoptic nucleus. J Neurosci 22: 977-990
20. Abrahamson EE, Leak RK, Moore RY (2000) The suprachiasmatic nucleus projects to posterior hypothalamic arousal systems. Neuroreport 12: 435-440
21. Hakim H, DeBernardo AP, Silver R (1991) Circadian locomotor rhythms, but not photoperiodic responses, survive surgical isolation of the SCN in hamsters. J Biol Rhythms 6: 97-113
22. Silver R, LeSauter J, Tresco PA, Lehman MN (1996) A diffusible coupling signal from the transplanted suprachiasmatic nucleus controlling circadian locomotor rhythms. Nature 382: 810-813
23. Kramer A, Yang FC, Snodgrass P, Li X, Scammell TE, Davis FC, Weitz CJ (2001) Regulation of daily locomotor activity and sleep by hypothalamic EGF receptor signaling. Science 294: 2511-2515
24. Cheng MY, Bullock CM, Li C, Lee AG, Bermak JC, Belluzzi J, Weaver DR, Leslie FM, Zhou QY (2002) Prokineticin 2 transmits the behavioural circadian rhythm of the suprachiasmatic nucleus. Nature 417: 405-410
25. Kraves S, Weitz CJ (2006) A role for cardiotrophin-like cytokine in the circadian control of mammalian locomotor activity. Nat Neurosci 9: 212-219
26. Meyer-Bernstein EL, Jetton AE, Matsumoto SI, Markuns JF, Lehman MN, Bittman EL (1999) Effects of suprachiasmatic transplants on circadian rhythms of neuroendocrine function in golden hamsters. Endocrinology 140: 207-218
27. Jouvet M (1999) Sleep and serotonin: an unfinished story. Neuropsychopharmacology 21: 24S-27S
28. Portas CM, Bjorvatn B, Ursin R (2000) Serotonin and the sleep/wake cycle: special emphasis on microdialysis studies. Prog Neurobiol 60: 13-35
29. Ursin R (2002) Serotonin and sleep. Sleep Med Rev 6: 55-69
30. Dugovic C (2001) Role of serotonin in sleep mechanisms. Rev Neurol (Paris) 157: S16-19
31. Koella WP, Feldstein A, Czicman JS (1968) The effect of para-chlorophenylalanine on the sleep of cats. Electroencephalogr Clin Neurophysiol 25: 481-490
32. Pujol JF, Buguet A, Froment JL, Jones B, Jouvet M (1971) The central metabolism of serotonin in the cat during insomnia. A neurophysiological and biochemical study after administration of p-chlorophenylalanine or destruction of the Raphe system. Brain Res 29: 195-212
33. Tork I (1985) Raphe nuclei and serotonin containing systems. In: G Paxinos (ed): The rat nervous system. Academic Press, Sydney, 43-78
34. Jouvet M (1969) Biogenic amines and the states of sleep. Science 163: 32-41
35. McGinty DJ, Harper RM (1976) Dorsal raphe neurons: depression of firing during sleep in cats. Brain Res 101: 569-575
36. Trulson ME, Jacobs BL (1979) Raphe unit activity in freely moving cats: Correlation with level of behavioral arousal. Brain Res 163: 135-150
37. Rasmussen K, Heym J, Jacobs BL (1984) Activity of serotonin-containing neurons in nucleus centralis superior of freely moving cats. Exp Neurol 83: 302-317
38. Trulson ME, Crisp T, Trulson VM (1984) Activity of serotonin-containing nucleus centralis superior (Raphe medianus) neurons in freely moving cats. Exp Brain Res 54: 33-44
39. Portas CM, Bjorvatn B, Fagerland S, Gronli J, Mundal V, Sorensen E, Ursin R (1998) On-line detection of extracellular levels of serotonin in dorsal raphe nucleus and frontal cortex over the sleep/wake cycle in the freely moving rat. Neuroscience 83: 807-814
40. Iwakiri H, Matsuyama K, Mori S (1993) Extracellular levels of serotonin in the medial pontine reticular formation in relation to sleep-wake cycle in cats: A microdialysis study. Neurosci Res 18: 157-170
41. Inouye S-IT, Kawamura H (1979) Persistence of circadian rhythmicity in a mammalian hypothalamic "island" containing the suprachiasmatic nucleus. Proc Natl Acad Sci USA 76: 5962-5966
42. Janušonis S, Fite KV (2001) Diurnal variation of c-Fos expression in subdivisions of the dorsal raphe nucleus of the Mongolian gerbil (Meriones unguiculatus). J Comp Neurol 440: 31-42
43. Birkett M, Fite KV (2005) Diurnal variation in serotonin immunoreactivity in the dorsal raphe nucleus. Brain Res 1034: 180-184
44. Kalen P, Rosegren E, Lindvall O, Bjorklund A (1989) Hippocampal noradrenaline and serotonin release over 24 hours as measured by the dialysis technique in freely moving rats: Correlation to behavioural activity state, effect of handling and tail-pinch. Eur J Neurosci 1: 181-188
45. Rueter LE, Jacobs BL (1996) Changes in forebrain serotonin at the light-dark transition: correlation with behaviour. Neuroreport 7: 1107-1111
46. Vertes RP, Fortin WJ, Crane AM (1999) Projections of the median raphe nucleus in the rat. J Comp Neurol 407: 555-582
47. Vertes RP (1991) A PHA-L analysis of ascending projections of the dorsal raphe nucleus in the rat. J Comp Neurol 313: 643-668
48. Dudley TE, DiNardo LA, Glass JD (1998) Endogenous regulation of serotonin release in the hamster suprachiasmatic nucleus. J Neurosci 18: 5045-5052
49. Barassin S, Raison S, Saboureau M, Bienvenu C, Maitre M, Malan A, Pevet P (2002) Circadian tryptophan hydroxylase levels and serotonin release in the suprachiasmatic nucleus of the rat. Eur J Neurosci 15: 833-840
50. Shioiri T, Takahashi K, Yamada N, Takahashi S (1991) Motor activity correlates negatively with free-running period, while positively with serotonin contents in SCN in free-running rats. Physiol Behav 49: 779-786
51. Semba J, Toru M, Mataga N (1984) Twenty-four hour rhythms of norepinephrine and serotonin in nucleus suprachiasmaticus, raphe nuclei, and locus coeruleus in the rat. Sleep 7: 211-218
52. Cagampang FRA, Yamazaki S, Otori Y, Inouye S-IT (1993) Serotonin in the raphe nuclei: Regulation by light and an endogenous pacemaker. Neuroreport 5: 49-52
53. Agren H, Koulu M, Saavedra JM, Potter WZ, Linnoila M (1986) Circadian covariation of norepinephrine and serotonin in the locus coeruleus and dorsal raphe nucleus in the rat. Brain Res 397: 353-358
54. Ozaki N, Duncan WC Jr, Johnson KA, Wehr TA (1993) Diurnal variations of serotonin and dopamine levels in discrete brain regions of Syrian hamsters and their modification by chronic clorgyline treatment. Brain Res 627: 41-48
55. Malek ZS, Pevet P, Raison S (2004) Circadian change in tryptophan hydroxylase protein levels within the rat intergeniculate leaflets and raphe nuclei. Neuroscience 125: 749-758
56. Meyer-Bernstein EL, Morin LP (1996) Differential serotonergic innervation of the suprachiasmatic nucleus and the intergeniculate leaflet and its role in circadian rhythm modulation. J Neurosci 16: 2097-2111
57. Hay-Schmidt A, Vrang N, Larsen PJ, Mikkelsen JD (2003) Projections from the raphe nuclei to the suprachiasmatic nucleus of the rat. J Chem Neuroanat 25: 293-310
58. Moga MM, Moore RY (1997) Organization of neural inputs to the suprachiasmatic nucleus in the rat. J Comp Neurol 389: 508-534
59. Malek ZS, Dardente H, Pevet P, Raison S (2005) Tissue-specific expression of tryptophan hydroxylase mRNAs in the rat midbrain: anatomical evidence and daily profiles. Eur J Neurosci 22: 895-901
60. Kan JP, Chouvet G, Hery F, Debilly G, Mermet A, Glowinski J, Pujol JF (1977) Daily variations of various parameters of serotonin metabolism in the rat brain. I. Circadian variations of tryptophan-5-hydroxylase in the raphe nuclei and the striatum. Brain Res 123: 125-136
61. Malek ZS, Sage D, Pevet P, Raison S (2007) Daily rhythm of tryptophan hydroxylase-2 mRNA within Raphe neurons is induced by corticoid daily surge and modulated by enhanced locomotor activity. Endocrinology doi:10.1210/en.2007-0526
62. Trulson ME, Jacobs BL (1983) Raphe unit activity in freely moving cats: lack of diurnal variation. Neurosci Lett 36: 285-290
63. Juvancz P (1980) The effect of raphe lesion on sleep in the rat. Brain Res 194: 371-376
64. Mouret J, Coindet J (1980) Polygraphic evidence against a critical role of the raphe nuclei in sleep in the rat. Brain Res 186: 273-287
65. Lu J, Sherman D, Devor M, Saper CB (2006) A putative flip-flop switch for control of REM sleep. Nature 441: 589-594
66. Mistlberger RE, Antle MC, Glass JD, Miller JD (2000) Behavioral and serotonergic regulation of circadian rhythms. Biol Rhythm Res 31: 240-283
67. Morin LP (1999) Serotonin and the regulation of mammalian circadian rhythmicity. Ann Med 31: 12-33
68. Deurveilher S, Burns J, Semba K (2002) Indirect projections from the suprachiasmatic nucleus to the ventrolateral preoptic nucleus: A dual tract-tracing study in rat. Eur J Neurosci 16: 1195-1213
69. Deurveilher S, Semba K (2003) Indirect projections from the suprachiasmatic nucleus to the median preoptic nucleus in rat. Brain Res 987: 100-106
70. Deurveilher S, Semba K (2005) Indirect projections from the suprachiasmatic nucleus to major arousal-promoting cell groups in rat: implications for the circadian control of behavioural state. Neuroscience 130: 165-183
71. Leak RK, Moore RY (2001) Topographic organization of suprachiasmatic nucleus projection neurons. J Comp Neurol 433: 312-334
72. Watts AG, Swanson LW (1987) 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: 230-252
73. Thompson RH, Canteras NS, Swanson LW (1996) Organization of projections from the dorsomedial nucleus of the hypothalamus: A PHA-L study in the rat. J Comp Neurol 376: 143-173
74. Leak RK, Card JP, Moore RY (1999) Suprachiasmatic pacemaker organization analyzed by viral transynaptic transport. Brain Res 819: 23-32
75. Thompson RH, Swanson LW (1998) Organization of inputs to the dorsomedial nucleus of the hypothalamus: A reexamination with Fluorogold and PHA-L in the rat. Brain Res Rev 27: 89-118
76. Kriegsfeld LJ, Leak RK, Yackulic CB, LeSauter J, Silver R (2004) Organization of suprachiasmatic nucleus projections in Syrian hamsters (Mesocricetus auratus): an anterograde and retrograde analysis. J Comp Neurol 468: 361-379
77. Buijs RM, Markman M, Nunes-Cardoso B, Hou Y-X, Shinn S (1993) Projections of the suprachiasmatic nucleus to stress-related areas in the rat hypothalamus: A light and electron microscopic study. J Comp Neurol 335: 42-54
78. Watts AG, Swanson LW, Sanchez-Watts G (1987) Efferent projections of the suprachiasmatic nucleus: I. Studies using anterograde transport of Phaseolus vulgaris leucoagglutinin in the rat. J Comp Neurol 258: 204-229
79. Berk M, Finkelstein J (1981) An autoradiographic determination of the efferent projections of the suprachiasmatic nucleus of the hypothalamus. Brain Res 226: 1-13
80. Stephan FK, Berkley KJ, Moss RL (1981) Efferent connections of the rat suprachiasmatic nucleus. Neuroscience 6: 2625-2641
81. Kalsbeek A, Teclemariam-Mesbah R, Pevet P (1993) Efferent projections of the suprachiasmatic nucleus in the golden hamster (Mesocricetus auratus). J Comp Neurol 332: 293-314
82. Hoorneman EMD, Buijs RM (1982) Vasopressin fiber pathways in the rat brain following suprachiasmatic nucleus lesioning. Brain Res 243: 235-241
83. van der Beek EM, Wiegant VM, van der Donk HA, van der Hurk R, Buijs RM (1993) Lesions of the suprachiasmatic nucleus indicate the presence of a direct vasoactive intestinal polypeptide-containing projection to gonadotophin- releasing hormone neurons in the female rat. J Neuroendocrinol 5: 137-144
84. Abrahamson EE, Moore RY (2001) Suprachiasmatic nucleus in the mouse: retinal innervation, intrinsic organization and efferent projections. Brain Res 916: 172-191
85. van den Pol AN, Tsujimoto KL (1985) Neurotransmitters of the hypothalamic suprachiasmatic nucleus: immunocytochemical analysis of 25 neuronal antigens. Neuroscience 15: 1049-1086
86. Vrang N, Larsen PJ, Moller M, Mikkelsen JD (1995) Topographical organization of the rat suprachiasmatic-paraventricular projection. J Comp Neurol 353: 585-603
87. Moore RY, Speh JC (1993) GABA is the principal neurotransmitter of the circadian system. Neurosci Lett 150: 112-116
88. Morin LP, Blanchard JH (2001) Neuromodulator content of hamster intergeniculate leaflet neurons and their projection to the suprachiasmatic nucleus or visual midbrain. J Comp Neurol 437: 79-90
89. Buijs RM, Hou Y-X, Shinn S, Renaud LP (1994) Ultrastructural evidence for intraand extranuclear projections of GABAergic neurons of the suprachiasmatic nucleus. J Comp Neurol 340: 381-391
90. Hermes ML, Coderre EM, Buijs RM, Renaud LP (1996) GABA and glutamate mediate rapid neurotransmission from suprachiasmatic nucleus to hypothalamic paraventricular nucleus in rat. J Physiol 496: 749-757
91. Sun X, Whitefield S, Rusak B, Semba K (2001) Electrophysiological analysis of suprachiasmatic nucleus projections to the ventrolateral preoptic area in rat: implications for circadian control of behavioral state. Eur J Neurosci 14: 1257-1274
92. Saint-Mleux B, Bayer L, Eggermann E, Jones BE, Muhlethaler M, Serafin M (2007) Suprachiasmatic modulation of noradrenaline release in the ventrolateral preoptic nucleus. J Neurosci 27: 6412-6416
93. Buijs RM, Wortel J, Hou YX (1995) Colocalization of gamma-aminobutyric acid with vasopressin, vasoactive intestinal peptide, and somatostatin in the rat suprachiasmatic nucleus. J Comp Neurol 358: 343-352
94. ter Horst GJ, Luiten PG (1986) The projections of the dorsomedial hypothalamic nucleus in the rat. Brain Res Bull 16: 231-248
95. Swanson LW, Mogenson GJ, Simerly RB, Wu M (1987) Anatomical and electrophysiological evidence for a projection from the medial preoptic area to the "mesencephalic and subthalamic locomotor regions" in the rat. Brain Res 405: 108-122
96. Simerly RB, Swanson LW (1988) Projections of the medial preoptic nucleus: A phaseolus vulgaris leucoagglutinin anterograde tract-tracing study in the rat. J Comp Neurol 270: 209-242
97. Steininger TL, Gong H, McGinty D, Szymusiak R (2001) Subregional organization of preoptic area/anterior hypothalamic projections to arousal-related monoaminergic cell groups. J Comp Neurol 429: 638-653
98. Chiba T, Murata Y (1985) Afferent and efferent connections of the medial preoptic area in the rat: A WGA-HRP study. Brain Res Bull 14: 261-272
99. Kalen P, Karlson M, Wiklund L (1985) Possible excitatory amino acid afferents to nucleus raphe dorsalis of the rat investigated with retrograde wheat germ agglutinin and d-[3H]aspartate tracing. Brain Res 360: 285-297
100. Peschanski M, Besson J-M (1984) Diencephalic connections of the raphe nuclei of the rat brainstem: An anatomical study with reference to the somatosensory system. J Comp Neurol 224: 509-534
101. Aghajanian GK, Wang RY (1977) Habenular and other midbrain raphe afferents demonstrated by a modified retrograde tracing technique. Brain Res 122: 229-242
102. Semba K, Reiner PB, McGeer EG, Fibiger HC (1989) Brainstem projecting neurons in the rat basal forebrain: neurochemical, topographical, and physiological distinctions from cortically projecting cholinergic neurons. Brain Res Bull 22: 501-509
103. Peyron C, Petit J-M, Rampon C, Jouvet M, Luppi P-H (1998) Forebrain afferents to the rat dorsal raphe nucleus demonstrated by retrograde and anterograde tracing methods. Neuroscience 82: 443-468
104. Lee HS, Park SH, Song WC, Waterhouse BD (2005) Retrograde study of hypocretin-1 (orexin-A) projections to subdivisions of the dorsal raphe nucleus in the rat. Brain Res 1059: 35-45
105. Gervasoni D, Peyron C, Rampon C, Barbagli B, Chouvet G, Urbain N, Fort P, Luppi P-H (2000) Role and origin of the GABAergic innervation of dorsal raphe serotonergic neurons. J Neurosci 20: 4217-4225
106. Simerly RB, Gorski RA, Swanson LW (1986) Neurotransmitter specificity of cells and fibers in the medial preoptic nucleus: an immunohistochemical study in the rat. J Comp Neurol 246: 343-363
107. Skofitsch G, Jacobowitz DM (1985) Immunohistochemical mapping of galanin-like neurons in the rat central nervous system. Peptides 6: 509-546
108. Moga MM, Saper CB (1994) Neuropeptide-immunoreactive neurons projecting to the paraventricular hypothalamic nucleus in the rat. J Comp Neurol 346: 137-150
109. Chou TC, Scammell TE, Gooley JJ, Gaus SE, Saper C, Lu J (2003) Critical role of dorsomedial hypothalamic nucleus in a wide range of behavioral circadian rhythms. J Neurosci 23: 10691-10702
110. Valentino RJ, Commons KG (2005) Peptides that fine-tune the serotonin system. Neuropeptides 39: 1-8
111. Xu ZQ, Zhang X, Pieribone VA, Grillner S, Hokfelt T (1998) Galanin-5-hydroxytryptamine interactions: Electrophysiological, immunohistochemical and in situ hybridization studies on rat dorsal raphe neurons with a note on galanin R1 and R2 receptors. Neuroscience 87: 79-94
112. Brown RE, Sergeeva OA, Eriksson KS, Haas HL (2002) Convergent excitation of dorsal raphe serotonin neurons by multiple arousal systems (orexin/hypocretin, histamine and noradrenaline). J Neurosci 22: 8850-8859
113. Nanopoulos D, Belin MF, Maitre M, Vincendon G, Pujol JF (1982) Immunocytochemical evidence for the existence of GABAergic neurons in the nucleus raphe dorsalis. Possible existence of neurons containing serotonin and GABA. Brain Res 232: 375-389
114. Trulson ME, Cannon MS, Raese JD (1985) Identification of dopamine-containing cell bodies in the dorsal and median raphe nuclei of the rat brain using tyrosine hydroxylase immunochemistry. Brain Res Bull 15: 229-234
115. Clements JR, Madl JE, Johnson RL, Larson AA, Beitz AJ (1987) Localization of glutamate, glutaminase, aspartate and aspartate aminotransferase in the rat midbrain periaqueductal gray. Exp Brain Res 67: 594-602
116. Terkel J, Johnson JH, Whitmoyer DI, Sawyer CH (1974) Effect of adrenalectomy on a diurnal (circadian) rhythm in hypothalamic multiple unit activitiy in the female rat. Neuroendocrinology 14: 103-113
117. Inouye S-IT (1983) Does the ventromedial hypothalamic nucleus contain a self-sustained circadian oscillator associated with periodic feedings? Brain Res 279: 53-63
118. Yamazaki S, Kerbeshian MC, Hocker CG, Block GD, Menaker M (1998) Rhythmic properties of the hamster suprachiasmatic nucleus in vivo. J Neurosci 18: 10709-10723
119. Choi S, Wong LS, Yamat C, Dallman MF (1998) Hypothalamic ventromedial nuclei amplify circadian rhythms: do they contain a food-entrained endogenous oscillator? J Neurosci 18: 3843-3852
120. Gooley JJ, Schomer A, Saper CB (2006) The dorsomedial hypothalamic nucleus is critical for the expression of food-entrainable circadian rhythms. Nat Neurosci 9: 398-407
121. Lee Y, Arbogast LA, Voogt JL (1998) Semicircadian rhythms of c-Fos expression in several hypothalamic areas during pregnancy in the rat: relationship to prolactin secretion. Neuroendocrinology 67: 83-93
122. Nunez AA, Bult A, McElhinny TL, Smale L (1999) Daily rhythms of Fos expression in hypothalamic targets of the suprachiasmatic nucleus in diurnal and nocturnal rodents. J Biol Rhythms 14: 300-306
123. Schwartz MD, Nunez AA, Smale L (2004) Differences in the suprachiasmatic nucleus and lower subparaventricular zone of diurnal and nocturnal rodents. Neuroscience 127: 13-23
124. Smale L, Castleberry C, Nunez AA (2001) Fos rhythms in the hypothalamus of Rattus and Arvicanthis that exhibit nocturnal and diurnal patterns of rhythmicity. Brain Res 899: 101-105
125. Schwartz MD, Smale L (2005) Individual differences in rhythms of behavioral sleep and its neural substrates in Nile grass rats. J Biol Rhythms 20: 526-537
126. Asala SA, Okano Y, Honda K, Inoue S (1990) Effects of medial preoptic area lesions on sleep and wakefulness in unrestrained rats. Neurosci Lett 114: 300-304
127. Lu J, Greco MA, Shiromani P, Saper CB (2000) Effect of lesions of the ventrolateral preoptic nucleus on NREM and REM sleep. J Neurosci 20: 3830-3842
128. John J, Kumar VM (1998) Effect of NMDA lesion of the medial preoptic neurons on sleep and other functions. Sleep 21: 587-598
129. Srividya R, Mallick HN, Kumar VM (2006) Differences in the effects of medial and lateral preoptic lesions on thermoregulation and sleep in rats. Neuroscience 139: 853-864
130. Lu J, Zhang Y-H, Chou T, Gaus SE, Elmquist JK, Shiromani P, Saper CB (2001) Contrasting effects of ibotenate lesions of the paraventricular nucleus and subparaventricular zone on sleep-wake cycle and temperature regulation. J Neurosci 21: 4864-4874
131. Abrahamson EE, Moore RY (2006) Lesions of suprachiasmatic nucleus efferents selectively affect rest-activity rhythm. Mol Cell Endocrinol 252: 46-56
132. Moore RY, Danchenko RL (2002) Paraventricular-subparaventricular hypothalamic lesions selectively affect circadian function. Chronobiol Int 19: 345-360
133. Landry GJ, Simon MM, Webb IC, Mistlberger RE (2006) Persistence of a behavioral food-anticipatory circadian rhythm following dorsomedial hypothalamic ablation in rats. Am J Physiol Regul Integr Comp Physiol 290: R1527-R1534
134. Bellinger LL, Bernardis LL, Mendel VE (1976) Effect of ventromedial and dorsomedial hypothalamic lesions on circadian corticosterone rhythms. Neuroendocrinology 22: 216-225
135. Mistlberger RE (1994) Circadian food-anticipatory activity: formal models and physiological mechanisms. Neurosci Biobehav Rev 18: 171-195
136. Buijs RM, la Fleur SE, Wortel J, Van Heyningen C, Zuiddam L, Mettenleiter TC, Kalsbeek A, Nagai K, Niijima A (2003) The suprachiasmatic nucleus balances sympathetic and parasympathetic output to peripheral organs through separate preautonomic neurons. J Comp Neurol 464: 36-48
137. Alam MN, McGinty D, Szymusiak R (1995) Neuronal discharge of preoptic/anterior hypothalamic thermosensitive neurons: relation to NREM sleep. Am J Physiol 269: R1240-R1249
138. Methippara MM, Alam MN, Szymusiak R, McGinty D (2003) Preoptic area warming inhibits wake-active neurons in the perifornical lateral hypothalamus. Brain Res 960: 165-173
139. Alam MN, McGinty D, Szymusiak R (1995) Preoptic/anterior hypothalamic neurons: thermosensitivity in rapid eye movement sleep. Am J Physiol 269: R1250-R1257
140. Guzman-Marin R, Alam MN, Szymusiak R, Drucker-Colin R, Gong H, McGinty D (2000) Discharge modulation of rat dorsal raphe neurons during sleep and waking: effects of preoptic/basal forebrain warming. Brain Res 875: 23-34
141. Zaretskaia MV, Zaretsky DV, Shekhar A, DiMicco JA (2002) Chemical stimulation of the dorsomedial hypothalamus evokes non-shivering thermogenesis in anesthetized rats. Brain Res 928: 113-125
142. Saper CB, Lu J, Chou TC, Gooley J (2005) The hypothalamic integrator for circadian rhythms. Trends Neurosci 28: 152-157
143. Tischler RC, Morin LP (2003) Reciprocal serotonergic connections between the hamster median and dorsal raphe nuclei. Brain Res 981: 126-132
144. Mrosovsky N (1996) Locomotor activity and non-photic influences on circadian clocks. Biol Rev Camb Philos Soc 71: 343-372
145. Reebs SG, Mrosovsky N (1989) Effects of induced wheel running on the circadian activity rhythms of Syrian hamsters: entrainment and phase response curve. J Biol Rhythms 4: 39-48
146. Antle MC, Mistlberger RE (2000) Circadian clock resetting by sleep deprivation without exercise in the Syrian hamster. J Neurosci 20: 9326-9332
147. Mistlberger RE, Antle MC, Webb IC, Jones M, Weinberg J, Pollock MS (2003) Circadian clock resetting by arousal in Syrian hamsters: The role of stress and activity. Am J Physiol Regul Integr Comp Physiol 285: R917-R925
148. Medanic M, Gillette MU (1992) Serotonin regulates the phase of the rat suprachiasmatic circadian pacemaker in vitro only during the subjective day. J Physiol 450: 629-642
149. Ehlen JC, Grossman GH, Glass JD (2001) In vivo resetting of the hamster circadian clock by 5-HT7 receptors in the suprachiasmatic nucleus. J Neurosci 21: 5351-5357
150. Glass JD, DiNardo LA, Ehlen JC (2000) Dorsal raphe nuclear stimulation of SCN serotonin release and circadian phase-resetting. Brain Res 859: 224-232
151. Meyer-Bernstein EL, Morin LP (1999) Electrical stimulation of the median or dorsal raphe nuclei reduces light-induced FOS protein in the suprachiasmatic nucleus and causes circadian activity rhythm phase shifts. Neuroscience 92: 267-279
152. Dudley TE, Dinardo LA, Glass JD (1999) In vivo assessment of the midbrain raphe nuclear regulation of serotonin release in the hamster suprachiasmatic nucleus. J Neurophysiol 81: 1469-1477
153. Grossman GH, Mistlberger RE, Antle MC, Ehlen JC, Glass JD (2000) Sleep deprivation stimulates serotonin release in the suprachiasmatic nucleus. Neuroreport 11: 1929-1932
154. Edgar DM, Reid MS, Dement WC (1997) Serotonergic afferents mediate activity-dependent entrainment of the mouse circadian clock. Am J Physiol 273: R265-R269
155. Marchant EG, Watson NV, Mistlberger RE (1997) Both neuropeptide Y and serotonin are necessary for entrainment of circadian rhythms in mice by daily treadmill running schedules. J Neurosci 17: 7974-7987
156. Bobrzynska KJ, Vrang N, Mrosovsky N (1996) Persistence of nonphotic phase shifts in hamsters after serotonin depletion in the suprachiasmatic nucleus. Brain Res 741: 205-214
157. Antle MC, Marchant EG, Niel L, Mistlberger RE (1998) Serotonin antagonists do not attenuate activity-induced phase shifts of circadian rhythms in the Syrian hamster. Brain Res 813: 139-149
158. Biello SM, Janik D, Mrosovsky N (1994) Neuropeptide Y and behaviorally induced phase shifts. Neuroscience 62: 273-279
159. Glotzbach S, Cornett C, Heller H (1987) Activity of suprachiasmatic and hypothalamic neurons during sleep and wakefulness in the rat. Brain Res 419: 279-287
160. Deboer T, Vansteensel MJ, Detari L, Meijer JH (2003) Sleep states alter activity of suprachiasmatic nucleus neurons. Nat Neurosci 6: 1086-1090
161. Mason R (1986) Circadian variation in sensitivity of suprachiasmatic and lateral geniculate neurones to 5-hydroxytryptamine in the rat. J Physiol 377: 1-13
162. Ying S-W, Rusak B (1994) Effects of serotonergic agonists on firing rates of photically responsive cells in the hamster suprachiasmatic nucleus. Brain Res 651: 37-46
163. DeboerT, Detari L, Meijer JH (2007) Long term effects of sleep deprivation on the mammalian circadian pacemaker. Sleep 30: 257-262
164. Morin LP, Shivers KY, Blanchard JH, Muscat L (2006) Complex organization of mouse and rat suprachiasmatic nucleus. Neuroscience 137: 1285-1297
165. Glass JD, Selim M, Rea MA (1994) Modulation of light-induced c-Fos expression in the suprachiasmatic nuclei by 5-HT1A receptor agonists. Brain Res 638: 235-242
166. Rea MA, Glass JD, Colwell CS (1994) Serotonin modulates photic responses in the hamster suprachiasmatic nuclei. J Neurosci 14: 3635-3642
167. Pickard GE, Weber ET, Scott PA, Riberdy AF, Rea MA (1996) 5HT1B receptor agonists inhibit light-induced phase shifts of behavioral circadian rhythms and expression of the immediate-early gene c-fos in the suprachiasmatic nucleus. J Neurosci 16: 8208-8220
168. Pickard GE, Smith BN, Belenky M, Rea MA, Dudek FE, Sollars PJ (1999) 5-HT1B receptor-mediated presynaptic inhibition of retinal input to the suprachiasmatic nucleus. J Neurosci 19: 4034-4045
169. Aston-Jones G, Chen S, Zhu Y, Oshinsky ML (2001) A neural circuit for circadian regulation of arousal. Nature 4: 732-738