Isolating neural correlates of the pacemaker for food anticipation

PLoS ONE

Volumn 7, Issue 4, 2012, Pages

  Blum, Ian David ^a,b   Lamont, Elaine Waddington ^a   Rodrigues, Trevor ^a   Abizaid, Alfonso ^a  

^a CARLETON UNIVERSITY   (Canada)

^b DOUGLAS MENTAL HEALTH UNIVERSITY INSTITUTE   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

GHRELIN; PROTEIN C FOS; CIRCADIAN RHYTHM SIGNALING PROTEIN; PER2 PROTEIN, MOUSE;

ANIMAL BEHAVIOR; ANIMAL EXPERIMENT; ANIMAL TISSUE; ANTICIPATION; ARTICLE; BRAIN REGION; BRAIN STEM; CIRCADIAN RHYTHM; CONTROLLED STUDY; ENZYME LINKED IMMUNOSORBENT ASSAY; FOOD ANTICIPATION; FOOD INTAKE; HYPOTHALAMUS; IMMUNOCYTOCHEMISTRY; LOCOMOTION; MALE; MOUSE; NONHUMAN; OSCILLATION; STOMACH; ANALYSIS OF VARIANCE; ANIMAL; BIOLOGICAL RHYTHM; BLOOD; BODY WEIGHT; CELL COUNT; CYTOLOGY; FEEDING BEHAVIOR; IMMUNOHISTOCHEMISTRY; METABOLISM; NERVE CELL; PHYSIOLOGY;

ANIMALIA; MUS;

ANALYSIS OF VARIANCE; ANIMALS; ANTICIPATION, PSYCHOLOGICAL; BIOLOGICAL CLOCKS; BODY WEIGHT; CELL COUNT; CIRCADIAN RHYTHM; FEEDING BEHAVIOR; GHRELIN; IMMUNOHISTOCHEMISTRY; MALE; MICE; NEURONS; PERIOD CIRCADIAN PROTEINS; PROTO-ONCOGENE PROTEINS C-FOS; STOMACH;

EID: 84860444284     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0036117     Document Type: Article

References (87)

1. Golombek DA, Rosenstein RE, (2010) Physiology of Circadian Entrainment. Physiol Rev 90: 1063-1102.
2. Mistlberger RE, (2011) Neurobiology of food anticipatory circadian rhythms. Physiology & behavior 104: 535-545.
3. Hirota T, Fukada Y, (2004) Resetting mechanism of central and peripheral circadian clocks in mammals. Zoolog Sci 21: 359-368.
4. Mistlberger RE, (1994) Circadian food-anticipatory activity: formal models and physiological mechanisms. Neurosci Biobehav Rev 18: 171-195.
5. Blum ID, Lamont EW, Abizaid A, (2012) Competing clocks: Metabolic status moderates signals from the master circadian pacemaker. Neuroscience and biobehavioral reviews 36: 254-270.
6. Bolles RC, Stokes LW, (1965) Rat's anticipation of diurnal and a-diurnal feeding. J Comp Physiol Psychol 60: 290-294.
7. Stephan FK, Swann JM, Sisk CL, (1979) Anticipation of 24-hr feeding schedules in rats with lesions of the suprachiasmatic nucleus. Behav Neural Biol 25: 346-363.
8. Stephan FK, Swann JM, Sisk CL, (1979) Entrainment of circadian rhythms by feeding schedules in rats with suprachiasmatic lesions. Behav Neural Biol 25: 545-554.
9. Rosenwasser AM, Pelchat RJ, Adler NT, (1984) Memory for feeding time: possible dependence on coupled circadian oscillators. Physiol Behav 32: 25-30.
10. Boulos Z, Rosenwasser AM, Terman M, (1980) Feeding schedules and the circadian organization of behavior in the rat. Behavioural Brain Research 1: 39-66.
11. Clarke JD, Coleman GJ, (1986) Persistent meal-associated rhythms in SCN-lesioned rats. Physiol Behav 36: 105-113.
12. Stephan FK, (1984) Phase shifts of circadian rhythms in activity entrained to food access. Physiol Behav 32: 663-671.
13. Verwey M, Amir S, (2009) Food-entrainable circadian oscillators in the brain. Eur J Neurosci 30: 1650-1657.
14. Carneiro BTS, Araujo JF, (2009) The Food-entrainable Oscillator: a network of interconnected brain structures entrained by humoral signals? Chronobiology International 26: 1273-1289.
15. 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: 1665-1675.
16. Provencio I, Jiang G, De Grip WJ, Hayes WP, Rollag MD, (1998) Melanopsin: An opsin in melanophores, brain, and eye. Proc Natl Acad Sci U S A 95: 340-345.
17. Hattar S, Lucas R, Mrosovsky N, Thompson S, Douglas R, et al. (2003) Melanopsin and rod-cone photoreceptive systems account for all major accessory visual functions in mice. Nature 424: 76-81.
18. Schmidt TM, Kofuji P, (2008) Novel insights into non-image forming visual processing in the retina. Cellscience 5: 77-83.
19. Dibner C, Schibler U, Albrecht U, (2010) The Mammalian Circadian Timing System: Organization and Coordination of Central and Peripheral Clocks. Annual Review of Physiology 72: 517-549.
20. Coleman GJ, Harper S, Clarke JD, Armstrong S, (1982) Evidence for a separate meal-associated oscillator in the rat. Physiology & behavior 29: 107-115.
21. Mistlberger RE, (2009) Food-anticipatory circadian rhythms: concepts and methods. Eur J Neurosci 30: 1718-1729.
22. Watson RE, Wiegand SJ, Clough RW, Hoffman GE, (1986) Use of cryoprotectant to maintain long-term peptide immunoreactivity and tissue morphology. Peptides 7: 155-159.
23. Abizaid A, Mezei G, Thanarajasingam G, Horvath TL, (2005) Estrogen enhances light-induced activation of dorsal raphe serotonergic neurons. European Journal of Neuroscience 21: 1536-1546.
24. Challet E, Jacob N, Vuillez P, Pevet P, Malan A, (1997) Fos-like immunoreactivity in the circadian timing system of calorie-restricted rats fed at dawn: daily rhythms and light pulse-induced changes. Brain Res 770: 228-236.
25. 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.
26. Ribeiro AC, Sawa E, Carren-LeSauter I, LeSauter J, Silver R, et al. (2007) Two forces for arousal: Pitting hunger versus circadian influences and identifying neurons responsible for changes in behavioral arousal. Proc Natl Acad Sci U S A 104: 20078-20083.
27. Takase LF, Nogueira MI, (2008) Patterns of fos activation in rat raphe nuclei during feeding behavior. Brain research 1200: 10-18.
28. Angeles-Castellanos M, Mendoza J, Diaz-Munoz M, Escobar C, (2005) Food entrainment modifies the c-Fos expression pattern in brain stem nuclei of rats. Am J Physiol Regul Integr Comp Physiol 288: R678-684.
29. 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: R158-165.
30. Gundersen HJ, Jensen EB, Kieu K, Nielsen J, (1999) The efficiency of systematic sampling in stereology-reconsidered. J Microsc 193: 199-211.
31. Gundersen HJ, Jensen EB, (1987) The efficiency of systematic sampling in stereology and its prediction. J Microsc 147: 229-263.
32. Paxinos G, Franklin KBJ, (2001) The Mouse Brain in Stereotaxic Coordinates New York, NY Academic Press.
33. Woods SC, (2004) Gastrointestinal satiety signals I. An overview of gastrointestinal signals that influence food intake. American journal of physiology Gastrointestinal and liver physiology 286: G7-13.
34. Mori T, Nagai K, Nakagawa H, (1983) Dependence of memory of meal time upon circadian biological clock in rats. Physiology & Behavior 30: 259-265.
35. Guido ME, de Guido LB, Goguen D, Robertson HA, Rusak B, (1999) Daily Rhythm of Spontaneous Immediate-Early Gene Expression in the Rat Suprachiasmatic Nucleus. Journal of Biological Rhythms 14: 275-280.
36. Davidson AJ, (2009) Lesion studies targeting food-anticipatory activity. Eur J Neurosci 30: 1658-1664.
37. Challet E, Mendoza J, Dardente H, Pevet P, (2009) Neurogenetics of food anticipation. Eur J Neurosci 30: 1676-1687.
38. Guilding C, Hughes A, Brown T, Namvar S, Piggins H, (2009) A riot of rhythms: neuronal and glial circadian oscillators in the mediobasal hypothalamus. Molecular Brain 2: 28.
39. Escobar C, Martínez-Merlos MT, Angeles-Castellanos M, Miñana MDC, Buijs RM, (2007) Unpredictable feeding schedules unmask a system for daily resetting of behavioural and metabolic food entrainment. European Journal of Neuroscience 26: 2804-2814.
40. Verwey M, Lam GY, Amir S, (2009) Circadian rhythms of PERIOD1 expression in the dorsomedial hypothalamic nucleus in the absence of entrained food-anticipatory activity rhythms in rats. Eur J Neurosci 29: 2217-2222.
41. Verwey M, Amir S, (2011) Nucleus-specific effects of meal duration on daily profiles of Period1 and Period2 protein expression in rats housed under restricted feeding. Neuroscience 192: 304-311.
42. Acosta-Galvan G, Yi C-X, van der Vliet J, Jhamandas JH, Panula P, et al. (2011) Interaction between hypothalamic dorsomedial nucleus and the suprachiasmatic nucleus determines intensity of food anticipatory behavior. Proceedings of the National Academy of Sciences 108: 5813-5818.
43. Landry GJ, Kent BA, Patton DF, Jaholkowski M, Marchant EG, et al. (2011) Evidence for Time-of-Day Dependent Effect of Neurotoxic Dorsomedial Hypothalamic Lesions on Food Anticipatory Circadian Rhythms in Rats. PLoS ONE 6: e24187.
44. Valassi E, Scacchi M, Cavagnini F, (2008) Neuroendocrine control of food intake. Nutr Metab Cardiovasc Dis 18: 158-168.
45. Ramos EJ, Meguid MM, Campos AC, Coelho JC, (2005) Neuropeptide Y, alpha-melanocyte-stimulating hormone, and monoamines in food intake regulation. Nutrition 21: 269-279.
46. Sutton GM, Begriche K, Kumar KG, Gimble JM, Perez-Tilve D, et al. (2010) Central nervous system melanocortin-3 receptors are required for synchronizing metabolism during entrainment to restricted feeding during the light cycle. FASEB J 24: 862-872.
47. Sutton GM, Perez-Tilve D, Nogueiras R, Fang J, Kim JK, et al. (2008) The melanocortin-3 receptor is required for entrainment to meal intake. J Neurosci 28: 12946-12955.
48. Hahn TM, Breininger JF, Baskin DG, Schwartz MW, (1998) Coexpression of Agrp and NPY in fasting-activated hypothalamic neurons. Nat Neurosci 1: 271-272.
49. Mistlberger RE, (2006) Circadian rhythms: PERturbing a food-entrained clock. Curr Biol 16: R968-969.
50. Moriya T, (2009) The dorsomedial hypothalamic nucleus is not necessary for food-anticipatory circadian rhythms of behavior, temperature or clock gene expression in mice. European Journal of Neuroscience 27: 1447-1460.
51. Acosta-Galvan G, Yi C-X, van der Vliet J, Jhamandas JH, Panula P, et al. (2011) Interaction between hypothalamic dorsomedial nucleus and the suprachiasmatic nucleus determines intensity of food anticipatory behavior. Proceedings of the National Academy of Sciences.
52. Sanchez E, Singru PS, Acharya R, Bodria M, Fekete C, et al. (2008) Differential Effects of Refeeding on Melanocortin-Responsive Neurons in the Hypothalamic Paraventricular Nucleus. Endocrinology 149: 4329-4335.
53. Herman JP, Tasker JG, Ziegler DR, Cullinan WE, (2002) Local circuit regulation of paraventricular nucleus stress integration: glutamate-GABA connections. Pharmacol Biochem Behav 71: 457-468.
54. Ziegler DR, Cullinan WE, Herman JP, (2002) Distribution of vesicular glutamate transporter mRNA in rat hypothalamus. J Comp Neurol 448: 217-229.
55. Bealer SL, (1986) Corticosteroids and plasma restitution after hemorrhage and hypothalamic lesions. Am J Physiol 250: R18-23.
56. Boudaba C, Szabo K, Tasker JG, (1996) Physiological mapping of local inhibitory inputs to the hypothalamic paraventricular nucleus. J Neurosci 16: 7151-7160.
57. Kalsbeek A, Fliers E, Hofman MA, Swaab DF, Buijs RM, (2010) Vasopressin and the output of the hypothalamic biological clock. J Neuroendocrinol 22: 362-372.
58. Dong H-W, Petrovich GD, Watts AG, Swanson LW, (2001) Basic organization of projections from the oval and fusiform nuclei of the bed nuclei of the stria terminalis in adult rat brain. The Journal of Comparative Neurology 436: 430-455.
59. Cullinan W, Ziegler D, Herman J, (2008) Functional role of local GABAergic influences on the HPA axis. Brain Structure and Function 213: 63-72.
60. Cullinan W, Helmreich DL, Watson SJ, (1996) Fos expression in forebrain afferents to the hypothalamic paraventricular nucleus following swim stress. The Journal of Comparative Neurology 368: 88-99.
61. Choi DC, Furay AR, Evanson NK, Ostrander MM, Ulrich-Lai YM, et al. (2006) Subnuclei of the bed nucleus of the stria terminalis differentially regulate PVN activation in response to restraint stress. Frontiers in Neuroendocrinology 27: 51-52.
62. Faulconbridge LF, Grill HJ, Kaplan JM, Daniels D, (2008) Caudal brainstem delivery of ghrelin induces fos expression in the nucleus of the solitary tract, but not in the arcuate or paraventricular nuclei of the hypothalamus. Brain Research 1218: 151-157.
63. Hayes MR, Bradley L, Grill HJ, (2009) Endogenous Hindbrain Glucagon-Like Peptide-1 Receptor Activation Contributes to the Control of Food Intake by Mediating Gastric Satiation Signaling. Endocrinology 150: 2654-2659.
64. Skibicka KP, Egecioglu E, Dickson SL, (2010) Parabrachial nucleus is a new target of orexigenic action of ghrelin. Endocrine Journal 57: S518-S518.
65. Davidson AJ, Cappendijk SL, Stephan FK, (2000) Feeding-entrained circadian rhythms are attenuated by lesions of the parabrachial region in rats. Am J Physiol Regul Integr Comp Physiol 278: R1296-1304.
66. Davidson AJ, Stephan FK, (1998) Circadian food anticipation persists in capsaicin deafferented rats. J Biol Rhythms 13: 422-429.
67. Williams DL, Baskin DG, Schwartz MW, (2009) Hindbrain leptin receptor stimulation enhances the anorexic response to cholecystokinin. American Journal of Physiology- Regulatory, Integrative and Comparative Physiology 297: R1238-R1246.
68. Johnstone LE, Fong TM, Leng G, (2006) Neuronal activation in the hypothalamus and brainstem during feeding in rats. Cell metabolism 4: 313-321.
69. LeSauter J, Hoque N, Weintraub M, Pfaff DW, Silver R, (2009) Stomach ghrelin-secreting cells as food-entrainable circadian clocks. Proceedings of the National Academy of Sciences of the United States of America 106: 13582-13587.
70. Davidson AJ, Poole AS, Yamazaki S, Menaker M, (2003) Is the food-entrainable circadian oscillator in the digestive system? Genes Brain Behav 2: 32-39.
71. Poulin A, Timofeeva E, (2008) The dynamics of neuronal activation during food anticipation and feeding in the brain of food-entrained rats. Brain Research 1227: 128-141.
72. Tsurumi C, Ishida N, Tamura T, Kakizuka A, Nishida E, et al. (1995) Degradation of c-Fos by the 26S proteasome is accelerated by c-Jun and multiple protein kinases. Molecular and Cellular Biology 15: 5682-5687.
73. Block M, Zucker I, (1976) Circadian rhythms of rat locomotor activity after lesions of the midbrain raphe nuclei. J Comp Physiol 109: 235-247.
74. Glass JD, Grossman GH, Farnbauch L, DiNardo L, (2003) Midbrain raphe modulation of nonphotic circadian clock resetting and 5-HT release in the mammalian suprachiasmatic nucleus. J Neurosci 23: 7451-7460.
75. Jacobs BL, Foote SL, Bloom FE, (1978) Differential Projections of Neurons within Dorsal Raphe Nucleus of Rat- a Horseradish-Peroxidase (Hrp) Study. Brain Research 147: 149-153.
76. Moga MM, Moore RY, (1997) Organization of neural inputs to the suprachiasmatic nucleus in the rat. J Comp Neurol 389: 508-534.
77. Varcoe TJ, Kennaway DJ, (2008) Activation of 5-HT2C receptors acutely induces Per1 gene expression in the rat SCN in vitro. Brain Res 1209: 19-28.
78. Webb IC, Patton DF, Landry GJ, Mistlberger RE, (2010) Circadian clock resetting by behavioral arousal: neural correlates in the midbrain raphe nuclei and locus coeruleus. Neuroscience 166: 739-751.
79. Verwey M, Amir S, (2012) Variable Restricted Feeding Disrupts the Daily Oscillations of Period2 Expression in the Limbic Forebrain and Dorsal Striatum in Rats. Journal of Molecular Neuroscience 46: 258-264.
80. Verwey M, Khoja Z, Stewart J, Amir S, (2008) Region-specific modulation of PER2 expression in the limbic forebrain and hypothalamus by nighttime restricted feeding in rats. Neurosci Lett 440: 54-58.
81. Waddington Lamont E, Harbour VL, Barry-Shaw J, Renteria Diaz L, Robinson B, et al. (2007) Restricted access to food, but not sucrose, saccharine, or salt, synchronizes the expression of Period2 protein in the limbic forebrain. Neuroscience 144: 402-411.
82. 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: 159-168.
83. Hood S, Cassidy P, Cossette M-P, Weigl Y, Verwey M, et al. (2010) Endogenous Dopamine Regulates the Rhythm of Expression of the Clock Protein PER2 in the Rat Dorsal Striatum via Daily Activation of D2 Dopamine Receptors. J Neurosci 30: 14046-14058.
84. Blum ID, Patterson Z, Khazall R, Lamont EW, Sleeman MW, et al. (2009) Reduced anticipatory locomotor responses to scheduled meals in ghrelin receptor deficient mice. Neuroscience 164: 351-359.
85. Escobar C, Diaz-Munoz M, Encinas F, Aguilar-Roblero R, (1998) Persistence of metabolic rhythmicity during fasting and its entrainment by restricted feeding schedules in rats. Am J Physiol 274: R1309-1316.
86. 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: R1527-1534.
87. Davidson AJ, (2006) Search for the feeding-entrainable circadian oscillator: a complex proposition. American Journal of Physiology- Regulatory, Integrative and Comparative Physiology 290: R1524-R1526.