Cell and Tissue Research

, Volume 341, Issue 1, pp 1–11 | Cite as

Metabolic and reward feeding synchronises the rhythmic brain

Review

Abstract

Daily brain rhythmicity, which controls the sleep-wake cycle and neuroendocrine functions, is generated by an endogenous circadian timing system. Within the multi-oscillatory circadian network, a master clock is located in the suprachiasmatic nuclei of the hypothalamus, whose main synchroniser (Zeitgeber) is light. In contrast, imposed meal times and temporally restricted feeding are potent synchronisers for secondary clocks in peripheral organs such as the liver and in brain regions, although not for the suprachiasmatic nuclei. Even when animals are exposed to a light-dark cycle, timed calorie restriction (i.e. when only a hypocaloric diet is given every day) is a synchroniser powerful enough to modify the suprachiasmatic clockwork and increase the synchronising effects of light. A daily chocolate snack in animals fed ad libitum with chow diet entrains the suprachiasmatic clockwork only under the conditions of constant darkness and decreases the synchronising effects of light. Secondary clocks in the brain outside the suprachiasmatic nuclei are differentially influenced by meal timing. Circadian oscillations can either be highly sensitive to food-related metabolic or reward cues (i.e. their phase is shifted according to the timed meal schedule) in some structures or hardly affected by meal timing (palatable or not) in others. Furthermore, animals will manifest food-anticipatory activity prior to their expected meal time. Anticipation of a palatable or regular meal may rely on a network of brain clocks, involving metabolic and reward systems and the cerebellum.

Keywords

Circadian clock Suprachiasmatic nucleus Restricted feeding Hypocaloric feeding Reward Meal anticipation 

References

  1. Abe H, Rusak B (1992) Anticipatory activity and entrainment of circadian rhythms in Syrian hamsters exposed to restricted palatable diets. Am J Physiol Regul Integr Comp Physiol 263:R116–R124Google Scholar
  2. Abe H, Kida M, Tsuji K, Mano T (1989) Feeding cycles entrain circadian rhythms of locomotor activity in CS mice but not in C57BL/6 J mice. Physiol Behav 45:397–401PubMedGoogle Scholar
  3. Abe M, Herzog ED, Yamazaki S, Straume M, Tei H, Sakaki Y, Menaker M, Block GD (2002) Circadian rhythms in isolated brain regions. J Neurosci 22:350–356PubMedGoogle Scholar
  4. Andrade JP, Pereira PA, Silva SM, Sa SI, Lukoyanov NV (2004) Timed hypocaloric food restriction alters the synthesis and expression of vasopressin and vasoactive intestinal peptide in the suprachiasmatic nucleus. Brain Res 1022:226–233PubMedGoogle Scholar
  5. Angeles-Castellanos M, Aguilar-Roblero R, Escobar C (2004) c-Fos expression in hypothalamic nuclei of food-entrained rats. Am J Physiol Regul Integr Comp Physiol 286:R158–R165PubMedGoogle Scholar
  6. Angeles-Castellanos M, Salgado-Delgado R, Rodriguez K, Buijs RM, Escobar C (2008) Expectancy for food or expectancy for chocolate reveals timing systems for metabolism and reward. Neuroscience 155:297–307PubMedGoogle Scholar
  7. Asher G, Gatfield D, Stratmann M, Reinke H, Dibner C, Kreppel F, Mostoslavsky R, Alt FW, Schibler U (2008) SIRT1 regulates circadian clock gene expression through PER2 deacetylation. Cell 134:317–328PubMedGoogle Scholar
  8. Balsalobre A, Brown SA, Marcacci L, Tronche F, Kellendonk C, Reichardt HM, Schutz G, Schibler U (2000a) Resetting of circadian time in peripheral tissues by glucocorticoid signaling. Science 289:2344–2347PubMedGoogle Scholar
  9. Balsalobre A, Marcacci L, Schibler U (2000b) Multiple signaling pathways elicit circadian gene expression in cultured Rat-1 fibroblasts. Curr Biol 10:1291–1294PubMedGoogle Scholar
  10. Balsam P, Sanchez-Castillo H, Taylor K, Van Volkinburg H, Ward RD (2009) Timing and anticipation: conceptual and methodological approaches. Eur J Neurosci 30:1749–1755PubMedGoogle Scholar
  11. Bogdan A, Bouchareb B, Touitou Y (2005) Response of circulating leptin to Ramadan daytime fasting: a circadian study. Br J Nutr 93:515–518PubMedGoogle Scholar
  12. Borgland SL, Taha SA, Sarti F, Fields HL, Bonci A (2006) Orexin A in the VTA is critical for the induction of synaptic plasticity and behavioral sensitization to cocaine. Neuron 49:589–601PubMedGoogle Scholar
  13. Boudard DL, Mendoza J, Hicks D (2009) Loss of photic entrainment at low illuminances in rats with acute photoreceptor degeneration. Eur J Neurosci 30:1527–1536PubMedGoogle Scholar
  14. Brown TM, Coogan AN, Cutler DJ, Hughes AT, Piggins HD (2008) Electrophysiological actions of orexins on rat suprachiasmatic neurons in vitro. Neurosci Lett 448:273–278PubMedGoogle Scholar
  15. Bubser M, Fadel JR, Jackson LL, Meador-Woodruff JH, Jing D, Deutch AY (2005) Dopaminergic regulation of orexin neurons. Eur J Neurosci 21:2993–3001PubMedGoogle Scholar
  16. Caldelas I, Feillet CA, Dardente H, Eclancher F, Malan A, Gourmelen S, Pévet P, Challet E (2005) Timed hypocaloric feeding and melatonin synchronize the suprachiasmatic clockwork in rats, but with opposite timing of behavioral output. Eur J Neurosci 22:921–929PubMedGoogle Scholar
  17. Castillo MR, Hochstetler KJ, Tavernier RJ, Greene DM, Bult-Ito A (2004) Entrainment of the master circadian clock by scheduled feeding. Am J Physiol Regul Integr Comp Physiol 287:R551–R555PubMedGoogle Scholar
  18. Challet E, Pévet P, Malan A (1996) Intergeniculate leaflet lesion and daily rhythms in food-restricted rats fed during daytime. Neurosci Lett 216:214–218PubMedGoogle Scholar
  19. Challet E, Pévet P, Vivien-Roels B, Malan A (1997) Phase-advanced daily rhythms of melatonin, body temperature, locomotor activity in food-restricted rats fed during daytime. J Biol Rhythms 12:65–79PubMedGoogle Scholar
  20. Challet E, Bernard DJ, Turek FW (1998a) Lesions of glucose-responsive neurons impair synchronizing effects of calorie restriction in mice. Brain Res 801:244–250PubMedGoogle Scholar
  21. Challet E, Solberg LC, Turek FW (1998b) Entrainment in calorie-restricted mice: conflicting Zeitgebers and free-running conditions. Am J Physiol Regul Integr Comp Physiol 274:R1751–R1761Google Scholar
  22. Damiola F, Le Minh N, Preitner N, Kornmann B, Fleury-Olela F, Schibler U (2000) Restricted feeding uncouples circadian oscillators in peripheral tissues from the central pacemaker in the suprachiasmatic nucleus. Genes Dev 14:2950–2961PubMedGoogle Scholar
  23. Dardente H (2007) Does a melatonin-dependent circadian oscillator in the pars tuberalis drive prolactin seasonal rhythmicity? J Neuroendocrinol 19:657–666PubMedGoogle Scholar
  24. Davidson AJ (2009) Lesion studies targeting food-anticipatory activity. Eur J Neurosci 30:1658–1664PubMedGoogle Scholar
  25. Davidson AJ, Poole AS, Yamazaki S, Menaker M (2003) Is the food-entrainable circadian oscillator in the digestive system? Genes Brain Behav 2:32–39PubMedGoogle Scholar
  26. de Vasconcelos AP, Bartol-Munier I, Feillet CA, Gourmelen S, Pévet P, Challet E (2006) Modifications of local cerebral glucose utilization during circadian food-anticipatory activity. Neuroscience 139:741–748PubMedGoogle Scholar
  27. Dkhissi-Benyahya O, Gronfier C, De Vanssay W, Flamant F, Cooper HM (2007) Modeling the role of mid-wavelength cones in circadian responses to light. Neuron 53:677–687PubMedGoogle Scholar
  28. Escobar C, Cailotto C, Angeles-Castellanos M, Delgado RS, Buijs RM (2009) Peripheral oscillators: the driving force for food-anticipatory activity. Eur J Neurosci 30:1665–1675PubMedGoogle Scholar
  29. Feillet CA, Albrecht U, Challet E (2006a) "Feeding time" for the brain: a matter of clocks. J Physiol (Paris) 100:252–260Google Scholar
  30. Feillet CA, Ripperger JA, Magnone MC, Dulloo A, Albrecht U, Challet E (2006b) Lack of food anticipation in Per2 mutant mice. Curr Biol 16:2016–2022PubMedGoogle Scholar
  31. Feillet CA, Mendoza J, Albrecht U, Pévet P, Challet E (2008) Forebrain oscillators ticking with different clock hands. Mol Cell Neurosci 37:209–221PubMedGoogle Scholar
  32. Froy O, Chapnik N, Miskin R (2008) The suprachiasmatic nuclei are involved in determining circadian rhythms during restricted feeding. Neuroscience 155:1152–1159PubMedGoogle Scholar
  33. García-Cabezas MA, Martínez-Sánchez P, Sánchez-González MA, Garzón M, Cavada C (2009) Dopamine innervation in the thalamus: monkey versus rat. Cereb Cortex 19:424–434PubMedGoogle Scholar
  34. Guilding C, Hughes AT, Brown TM, Namvar S, Piggins HD (2009) A riot of rhythms: neuronal and glial circadian oscillators in the mediobasal hypothalamus. Mol Brain 2:28PubMedGoogle Scholar
  35. Guilding C, Piggins HD (2007) Challenging the omnipotence of the suprachiasmatic timekeeper: are circadian oscillators present throughout the mammalian brain? Eur J Neurosci 25:3195–3216PubMedGoogle Scholar
  36. Hall AC, Hoffmaster RM, Stern EL, Harrington ME, Bickar D (1997) Suprachiasmatic nucleus neurons are glucose sensitive. J Biol Rhythms 12:388–400PubMedGoogle Scholar
  37. Harrington ME (1997) The ventral lateral geniculate nucleus and the intergeniculate leaflet: interrelated structures in the visual and circadian systems. Neurosci Biobehav Rev 21:705–727PubMedGoogle Scholar
  38. Harris GC, Aston-Jones G (2006) Arousal and reward: a dichotomy in orexin function. Trends Neurosci 29:571–577PubMedGoogle Scholar
  39. Hayasaka N, Yaita T, Kuwaki T, Honma S, Honma K, Kudo T, Shibata S (2007) Optimization of dosing schedule of daily inhalant dexamethasone to minimize phase shifting of clock gene expression rhythm in the lungs of the asthma mouse model. Endocrinology 148:3316–3326PubMedGoogle Scholar
  40. Hiler DJ, Bhattacherjee A, Yamazaki S, Tei H, Geusz ME (2008) Circadian mPer1 gene expression in mesencephalic trigeminal nucleus cultures. Brain Res 1214:84–93PubMedGoogle Scholar
  41. Hirota T, Okano T, Kokame K, Shirotani-Ikejima H, Miyata T, Fukada Y (2002) Glucose down-regulates Per1 and Per2 mRNA levels and induces circadian gene expression in cultured Rat-1 fibroblasts. J Biol Chem 277:44244–44251PubMedGoogle Scholar
  42. Holmes MM, Mistlberger RE (2000) Food anticipatory activity and photic entrainment in food-restricted BALB/c mice. Physiol Behav 68:655–666PubMedGoogle Scholar
  43. Honma KI, Goetz C von, Aschoff J (1983) Effects of restricted daily feeding on freerunning circadian rhythms in rats. Physiol Behav 30:905–913PubMedGoogle Scholar
  44. Inouye ST (1982) Restricted daily feeding does not entrain circadian rhythms of the suprachiasmatic nucleus in the rat. Brain Res 232:194–199PubMedGoogle Scholar
  45. Iwanaga H, Yano M, Miki H, Okada K, Azama T, Takiguchi S, Fujiwara Y, Yasuda T, Nakayama M, Kobayashi M, Oishi K, Ishida N, Nagai K, Monden M (2005) Per2 gene expressions in the suprachiasmatic nucleus and liver differentially respond to nutrition factors in rats. J Parenter Enteral Nutr 29:157–161Google Scholar
  46. Jilg A, Moek J, Weaver DR, Korf HW, Stehle JH, Gall C von (2005) Rhythms in clock proteins in the mouse pars tuberalis depend on MT1 melatonin receptor signalling. Eur J Neurosci 22:2845–2854PubMedGoogle Scholar
  47. Kelley AE, Berridge KC (2002) The neuroscience of natural rewards: relevance to addictive drugs. J Neurosci 22:3306–3311PubMedGoogle Scholar
  48. Kennedy GA, Coleman GJ, Armstrong SM (1991) Restricted feeding entrains circadian wheel-running activity rhythms of the kowari. Am J Physiol Regul Integr Comp Physiol 261:R819–R827Google Scholar
  49. Kennedy GA, Coleman GJ, Armstrong SM (1996) Daily restricted feeding effects on the circadian activity rhythms of the stripe-faced dunnart, Sminthopsis macroura. J Biol Rhythms 11:188–195PubMedGoogle Scholar
  50. Klisch C, Inyushkin A, Mordel J, Karnas D, Pévet P, Meissl H (2009) Orexin A modulates neuronal activity of the rodent suprachiasmatic nucleus in vitro. Eur J Neurosci 30:65–75PubMedGoogle Scholar
  51. Lamia KA, Sachdeva UM, DiTacchio L, Williams EC, Alvarez JG, Egan DF, Vasquez DS, Juguilon H, Panda S, Shaw RJ, Thompson CB, Evans RM (2009) AMPK regulates the circadian clock by cryptochrome phosphorylation and degradation. Science 326:437–440PubMedGoogle Scholar
  52. Lamont EW, Diaz LR, Barry-Shaw J, Stewart J, Amir S (2005a) Daily restricted feeding rescues a rhythm of period2 expression in the arrhythmic suprachiasmatic nucleus. Neuroscience 132:245–248PubMedGoogle Scholar
  53. Lamont EW, Robinson B, Stewart J, Amir S (2005b) The central and basolateral nuclei of the amygdala exhibit opposite diurnal rhythms of expression of the clock protein Period2. Proc Natl Acad Sci USA 102:4180–4184PubMedGoogle Scholar
  54. Lavialle M, Champeil-Potokar G, Alessandri JM, Balasse L, Guesnet P, Papillon C, Pévet P, Vancassel S, Vivien-Roels B, Denis I (2008) An (n-3) polyunsaturated fatty acid-deficient diet disturbs daily locomotor activity, melatonin rhythm, and striatal dopamine in Syrian hamsters. J Nutr 138:1719–1724PubMedGoogle Scholar
  55. LeSauter J, Hoque N, Weintraub M, Pfaff DW, Silver R (2009) Stomach ghrelin-secreting cells as food-entrainable circadian clocks. Proc Natl Acad Sci USA 106:13582–13587PubMedGoogle Scholar
  56. Marchant EG, Mistlberger RE (1997) Anticipation and entrainment to feeding time in intact and SCN-ablated C57BL/6j mice. Brain Res 765:273–282PubMedGoogle Scholar
  57. McGranaghan PA, Piggins HD (2001) Orexin A-like immunoreactivity in the hypothalamus and thalamus of the Syrian hamster (Mesocricetus auratus) and Siberian hamster (Phodopus sungorus), with special reference to circadian structures. Brain Res 904:234–244PubMedGoogle Scholar
  58. Mendoza J, Angeles-Castellanos M, Escobar C (2005a) Differential role of the accumbens Shell and Core subterritories in food-entrained rhythms of rats. Behav Brain Res 158:133–142PubMedGoogle Scholar
  59. Mendoza J, Angeles-Castellanos M, Escobar C (2005b) Entrainment by a palatable meal induces food-anticipatory activity and c-Fos expression in reward-related areas of the brain. Neuroscience 133:293–303PubMedGoogle Scholar
  60. Mendoza J, Angeles-Castellanos M, Escobar C (2005c) A daily palatable meal without food deprivation entrains the suprachiasmatic nucleus of rats. Eur J Neurosci 22:2855–2862PubMedGoogle Scholar
  61. Mendoza J, Graff C, Dardente H, Pévet P, Challet E (2005d) Feeding cues alter clock gene oscillations and photic responses in the suprachiasmatic nuclei of mice exposed to a light-dark cycle. J Neurosci 25:1514–1522PubMedGoogle Scholar
  62. Mendoza J, Pévet P, Challet E (2007) Circadian and photic regulation of clock and clock-controlled proteins in the suprachiasmatic nuclei of calorie-restricted mice. Eur J Neurosci 25:3691–3701PubMedGoogle Scholar
  63. Mendoza J, Drevet K, Pévet P, Challet E (2008) Daily meal timing is not necessary for resetting the main circadian clock by calorie restriction. J Neuroendocrinol 20:251–260PubMedGoogle Scholar
  64. Mendoza J, Clesse D, Pévet P, Challet E (2010a) Food-reward signalling in the suprachiasmatic clock. J Neurochem 112:1489–1499PubMedGoogle Scholar
  65. Mendoza J, Pévet P, Felder-Schmittbuhl MP, Bailly Y, Challet E (2010b) The cerebellum harbors a circadian oscillator involved in food anticipation. J Neurosci 30:1894–1904PubMedGoogle Scholar
  66. Mistlberger RE (1993) Effects of scheduled food and water access on circadian rhythms of hamsters in constant light, dark, and light-dark. Physiol Behav 53:509–516PubMedGoogle Scholar
  67. Mistlberger RE (1994) Circadian food-anticipatory activity: formal models and physiological mechanisms. Neurosci Biobehav Rev 18:171–195PubMedGoogle Scholar
  68. Mistlberger R (2009) Food-anticipatory circadian rhythms: concepts and methods. Eur J Neurosci 30:1718–1729PubMedGoogle Scholar
  69. Mistlberger RE, Mumby DG (1992) The limbic system and food-anticipatory circadian rhythms in the rat: ablation and dopamine blocking studies. Behav Brain Res 47:159–168PubMedGoogle Scholar
  70. Mistlberger R, Rusak B (1987) Palatable daily meals entrain anticipatory activity rhythms in free-feeding rats: dependence on meal size and nutrient content. Physiol Behav 41:219–226PubMedGoogle Scholar
  71. Moga MM, Weis RP, Moore RY (1995) Efferent projections of the paraventricular thalamic nucleus in the rat. J Comp Neurol 359:221–238PubMedGoogle Scholar
  72. Mrosovsky N (1996) Locomotor activity and non-photic influences on circadian clocks. Biol Rev 71:343–372PubMedGoogle Scholar
  73. Nagai K, Nishio T, Nakagawa H, Nakamura S, Fukuda Y (1978) Effect of bilateral lesions of the suprachiasmatic nuclei on the circadian rhythm of food-intake. Brain Res 142:384–389PubMedGoogle Scholar
  74. Nakahata Y, Sahar S, Astarita G, Kaluzova M, Sassone-Corsi P (2009) Circadian control of the NAD + salvage pathway by CLOCK-SIRT1. Science 324:654–657PubMedGoogle Scholar
  75. Oishi K, Uchida D, Ohkura N, Doi R, Ishida N, Kadota K, Horie S (2009) Ketogenic diet disrupts the circadian clock and increases hypofibrinolytic risk by inducing expression of plasminogen activator inhibitor-1. Arterioscler Thromb Vasc Biol 29:1571–1577PubMedGoogle Scholar
  76. Pecoraro N, Gomez F, Laugero K, Dallman MF (2002) Brief access to sucrose engages food-entrainable rhythms in food-deprived rats. Behav Neurosci 116:757–776PubMedGoogle Scholar
  77. Peirson S, Foster RG (2006) Melanopsin: another way of signaling light. Neuron 49:331–339PubMedGoogle Scholar
  78. Perreau-Lenz S, Pévet P, Buijs RM, Kalsbeek A (2004) The biological clock: the bodyguard of temporal homeostasis. Chronobiol Int 21:1–25PubMedGoogle Scholar
  79. Pévet P, Agez L, Bothorel B, Saboureau M, Gauer F, Laurent V, Masson-Pévet M (2006) Melatonin in the multi-oscillatory mammalian circadian world. Chronobiol Int 23:39–51PubMedGoogle Scholar
  80. Platá-Salaman CR, Oomura Y (1987) Food intake dependence on acute changes in light schedule. Physiol Behav 41:135–140PubMedGoogle Scholar
  81. Poulin AM, Timofeeva E (2008) The dynamics of neuronal activation during food anticipation and feeding in the brain of food-entrained rats. Brain Res 1227:128–141PubMedGoogle Scholar
  82. Prosser RA, Bergeron HE (2003) Leptin phase-advances the rat suprachiasmatic circadian clock in vitro. Neurosci Lett 336:139-142PubMedGoogle Scholar
  83. Ramsey KM, Yoshino J, Brace CS, Abrassart D, Kobayashi Y, Marcheva B, Hong HK, Chong JL, Buhr ED, Lee C, Takahashi JS, Imai S, Bass J (2009) Circadian clock feedback cycle through NAMPT-mediated NAD + biosynthesis. Science 324:651–654PubMedGoogle Scholar
  84. Resuehr D, Olcese J (2005) Caloric restriction and melatonin substitution: effects on murine circadian parameters. Brain Res 1048:146–152PubMedGoogle Scholar
  85. Roky R, Chapotot F, Hakkou F, Benchekroun MT, Buguet A (2001) Sleep during Ramadan intermittent fasting. J Sleep Res 10:319–327PubMedGoogle Scholar
  86. Rutter J, Reick M, McKnight SL (2002) Metabolism and the control of circadian rhythms. Annu Rev Biochem 71:307–331PubMedGoogle Scholar
  87. Saito M, Ibuka N (1983) Decreased food intake of rats kept under adiurnal feeding cycles: effect of suprachiasmatic lesions. Physiol Behav 30:87–92PubMedGoogle Scholar
  88. Schibler U, Ripperger J, Brown SA (2003) Peripheral circadian oscillators in mammals: time and food. J Biol Rhythms 18:250–260PubMedGoogle Scholar
  89. Stephan FK (2001) Food-entrainable oscillators in mammals. In: Takahashi JS, Turek FW, Moore RY (eds) Handbook of behavioral neurobiology, vol 12. Circadian clocks. Kluwer, New York, pp 223–246Google Scholar
  90. Stephan FK, Zucker I (1972) Circadian rhythms in drinking behavior and locomotor activity of rats are eliminated by hypothalamic lesions. Proc Natl Acad Sci USA 69:1583–1586PubMedGoogle Scholar
  91. Stokkan KA, Yamazaki S, Tei H, Sakaki Y, Menaker M (2001) Entrainment of the circadian clock in the liver by feeding. Science 291:490–493PubMedGoogle Scholar
  92. Takahashi JS, Turek FW, Moore RY (2001) Handbook of behavioral neurobiology, vol 12. Circadian clocks. Kluwer, New YorkGoogle Scholar
  93. Tsujino N, Sakurai T (2009) Orexin/hypocretin: a neuropeptide at the interface of sleep, energy homeostasis, and reward system. Pharmacol Rev 61:162–176PubMedGoogle Scholar
  94. Verwey M, Khoja Z, Stewart J, Amir S (2007) Differential regulation of the expression of Period2 protein in the limbic forebrain and dorsomedial hypothalamus by daily limited access to highly palatable food in food-deprived and free-fed rats. Neuroscience 147:277–285PubMedGoogle Scholar
  95. Viswanathan N, Davis FC (1997) Single prenatal injections of melatonin or the D1-dopamine receptor agonist SKF 38393 to pregnant hamsters sets the offsprings' circadian rhythms to phases 180 degrees apart. J Comp Physiol [A] 180:339–346Google Scholar
  96. Waddington Lamont E, Harbour VL, Barry-Shaw J, Renteria Diaz L, Robinson B, Stewart J, Amir S (2007) Restricted access to food, but not sucrose, saccharine, or salt, synchronizes the expression of Period2 protein in the limbic forebrain. Neuroscience 144:402–411PubMedGoogle Scholar
  97. Wakamatsu H, Yoshinobu Y, Aida R, Moriya T, Akiyama M, Shibata S (2001) Restricted-feeding-induced anticipatory activity rhythm is associated with a phase-shift of the expression of mPer1 and mPer2 mRNA in the cerebral cortex and hippocampus but not in the suprachiasmatic nucleus of mice. Eur J Neurosci 13:1190–1196PubMedGoogle Scholar
  98. Weaver DR, Reppert SM (1995) Definition of the developmental transition from dopaminergic to photic regulation of c-fos gene expression in the rat suprachiasmatic nucleus. Brain Res Mol Brain Res 33:136–148PubMedGoogle Scholar
  99. Weaver DR, Rivkees SA, Reppert SM (1992) D1-dopamine receptors activate c-fos expression in the fetal suprachiasmatic nuclei. Proc Natl Acad Sci USA 89:9201–9204PubMedGoogle Scholar
  100. Yannielli PC, Molyneux PC, Harrington ME, Golombek DA (2007) Ghrelin effects on the circadian system of mice. J Neurosci 27:2890–2895PubMedGoogle Scholar
  101. Yi CX, Vliet J van der, Dai J, Yin G, Ru L, Buijs RM (2006) Ventromedial arcuate nucleus communicates peripheral metabolic information to the suprachiasmatic nucleus. Endocrinology 147:283–294PubMedGoogle Scholar
  102. Yi CX, Challet E, Pévet P, Kalsbeek A, Escobar C, Buijs RM (2008) A circulating ghrelin mimetic attenuates light-induced phase delay of mice and light-induced Fos expression in the suprachiasmatic nucleus of rats. Eur J Neurosci 27:1965–1972PubMedGoogle Scholar
  103. Zeitzer JM, Nishino S, Mignot E (2006) The neurobiology of hypocretins (orexins), narcolepsy and related therapeutic interventions. Trends Pharmacol Sci 27:368–374PubMedGoogle Scholar

Copyright information

© Springer-Verlag 2010

Authors and Affiliations

  1. 1.Centre National de la Recherche Scientifique (CNRS), Institut Fédératif en Neurosciences de Strasbourg (IFR37)Institut des Neurosciences Cellulaires et Intégratives (UPR3212), Associé à l’Université de StrasbourgStrasbourg cedexFrance

Personalised recommendations