Enhanced food anticipatory activity associated with enhanced activation of extrahypothalamic neural pathways in serotonin2C receptor null mutant mice

PLoS ONE

Volumn 5, Issue 7, 2010, Pages

  Hsu, Jennifer L ^a   Yu, Lisa ^b   Sullivan, Elinor ^c   Bowman, Melodi ^b   Mistlberger, Ralph E ^d   Tecott, Laurence H ^b  

^a GLADSTONE INSTITUTE OF NEUROLOGICAL DISEASE   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c OREGON HEALTH AND SCIENCE UNIVERSITY   (United States)

^d SIMON FRASER UNIVERSITY   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

PROTEIN C FOS; SEROTONIN 2C RECEPTOR;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARCUATE NUCLEUS; ARTICLE; BRAIN REGION; C57BL 6 MOUSE; CONTROLLED STUDY; DORSOMEDIAL HYPOTHALAMUS; FEEDING BEHAVIOR; FOOD DEPRIVATION; FOOD INTAKE; GENE EXPRESSION; GENOTYPE; GLUCOSE BLOOD LEVEL; HYPOTHALAMUS; HYPOTHALAMUS NUCLEUS; KNOCKOUT MOUSE; LATERAL HYPOTHALAMUS; LIGHT DARK CYCLE; LOCOMOTION; MALE; MOUSE; MUTANT; NONHUMAN; NUCLEUS ACCUMBENS; OSCILLATOR; PHENOTYPE; RED LIGHT; SENSORY CORTEX; SUPRACHIASMATIC NUCLEUS; THALAMUS; VENTRAL POSTERIOR THALAMUS; WEIGHT REDUCTION; WILD TYPE; ANALYSIS OF VARIANCE; ANIMAL; BODY WEIGHT; EATING; GENETICS; IN SITU HYBRIDIZATION; METABOLISM; MOTOR ACTIVITY; MOUSE MUTANT; NERVE TRACT; PHYSIOLOGY;

ANIMALIA; MUS;

ANALYSIS OF VARIANCE; ANIMALS; BLOOD GLUCOSE; BODY WEIGHT; EATING; FEEDING BEHAVIOR; FOOD DEPRIVATION; IN SITU HYBRIDIZATION; MALE; MICE; MICE, KNOCKOUT; MOTOR ACTIVITY; NEURAL PATHWAYS; PROTO-ONCOGENE PROTEINS C-FOS; RECEPTOR, SEROTONIN, 5-HT2C;

EID: 77955615935     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0011802     Document Type: Article

References (48)

1. Schibler U, Sassone-Corsi P (2002) A web of circadian pacemakers. Cell 111: 919-922.
2. Albrecht U (2006) Orchestration of gene expression and physiology by the circadian clock. Journal of Physiology-Paris 100: 243-251.
3. Mistlberger RE (1994) Circadian food-anticipatory activity: formal models and physiological mechanisms. Neurosci Biobehav Rev 18: 171-195.
4. Feillet CA, Albrecht U, Challet E (2006) ''Feeding time'' for the brain: a matter of clocks. J Physiol Paris 100: 252-260.
5. Stephan FK (2002) The ''other'' circadian system: food as a Zeitgeber. J Biol Rhythms 17: 284-292.
6. Stephan FK (1983) Circadian rhythm dissociation induced by periodic feeding in rats with suprachiasmatic lesions. Behav Brain Res 7: 81-98.
7. Marchant EG, Mistlberger RE (1997) Anticipation and entrainment to feeding time in intact and SCN-ablated C57BL/6j mice. Brain Res 765: 273-282.
8. Boulos Z, Rosenwasser AM, Terman M (1980) Feeding schedules and the circadian organization of behavior in the rat. Behav Brain Res 1: 39-65.
9. Abe H, Honma S, Honma K (2007) Daily restricted feeding resets the circadian clock in the suprachiasmatic nucleus of CS mice. Am J Physiol Regul Integr Comp Physiol 292: R607-615.
10. 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: 509-516.
11. Lax P, Zamora S, Madrid JA (1999) Food-entrained feeding and locomotor circadian rhythms in rats under different lighting conditions. Chronobiol Int 16: 281-291.
12. 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.
13. Angeles-Castellanos M, Mendoza J, Escobar C (2007) Restricted feeding schedules phase shift daily rhythms of c-Fos and protein Per1 immunoreactivity in corticolimbic regions in rats. Neuroscience 144: 344-355.
14. Mieda M, Williams SC, Sinton CM, Richardson JA, Sakurai T, et al. (2004) Orexin neurons function in an efferent pathway of a food-entrainable circadian oscillator in eliciting food-anticipatory activity and wakefulness. J Neurosci 24: 10493-10501.
15. Mieda M, Williams SC, Richardson JA, Tanaka K, Yanagisawa M (2006) The dorsomedial hypothalamic nucleus as a putative food-entrainable circadian pacemaker. Proc Natl Acad Sci U S A 103: 12150-12155.
16. Feillet CA, Mendoza J, Albrecht U, Pevet P, Challet E (2008) Forebrain oscillators ticking with different clock hands. Mol Cell Neurosci 37: 209-221.
17. Akiyama M, Yuasa T, Hayasaka N, Horikawa K, Sakurai T, et al. (2004) Reduced food anticipatory activity in genetically orexin (hypocretin) neuronablated mice. Eur J Neurosci 20: 3054-3062.
18. Mendoza J, Angeles-Castellanos M, Escobar C (2005) Differential role of the accumbens Shell and Core subterritories in food-entrained rhythms of rats. Behav Brain Res 158: 133-142.
19. 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.
20. 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: 219-226.
21. 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.
22. 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.
23. Landry GJ, Yamakawa GR, Webb IC, Mear RJ, Mistlberger RE (2007) The dorsomedial hypothalamic nucleus is not necessary for the expression of circadian food-anticipatory activity in rats. J Biol Rhythms 22: 467-478.
24. Moriya T, Aida R, Kudo T, Akiyama M, Doi M, et al. (2009) The dorsomedial hypothalamic nucleus is not necessary for food-anticipatory circadian rhythms of behavior, temperature or clock gene expression in mice. Eur J Neurosci 29: 1447-1460.
25. Davidson AJ (2009) Lesion studies targeting food-anticipatory activity. Eur J Neurosci 30: 1658-1664.
26. Shibata S, Ono M, Minamoto Y, Watanabe S (1995) Attenuating effect of serotonin receptor antagonists on impairment of mealtime-associated activity rhythm in old rats. Pharmacology Biochemistry and Behavior 51: 541-544.
27. Molineaux SM, Jessell TM, Axel R, Julius D (1989) 5-HT1c receptor is a prominent serotonin receptor subtype in the central nervous system. Proc Natl Acad Sci U S A 86: 6793-6797.
28. Wright DE, Seroogy KB, Lundgren KH, Davis BM, Jennes L (1995) Comparative localization of serotonin1A, 1C, and 2 receptor subtype mRNAs in rat brain. J Comp Neurol 351: 357-373.
29. Tecott LH, Sun LM, Akana SF, Strack AM, Lowenstein DH, et al. (1995) Eating disorder and epilepsy in mice lacking 5-HT2c serotonin receptors. Nature 374: 542-546.
30. Nonogaki K, Abdallah L, Goulding EH, Bonasera SJ, Tecott LH (2003) Hyperactivity and reduced energy cost of physical activity in serotonin 5-HT(2C) receptor mutant mice. Diabetes 52: 315-320.
31. Rocha BA, Goulding EH, O'Dell LE, Mead AN, Coufal NG, et al. (2002) Enhanced locomotor, reinforcing, and neurochemical effects of cocaine in serotonin 5-hydroxytryptamine 2C receptor mutant mice. Journal of Neuroscience 22: 10039-10045.
32. Paxinos G, Franklin KB (2001) The Mouse Brain in Stereotaxic Coordinates. San Diego: Academic Press.
33. Redlin U (2001) Neural basis and biological function of masking by light in mammals: suppression of melatonin and locomotor activity. Chronobiol Int 18: 737-758.
34. Saper CB, Lu J, Chou TC, Gooley J (2005) The hypothalamic integrator for circadian rhythms. Trends Neurosci 28: 152-157.
35. Goulding EH, Schenk AK, Juneja P, MacKay AW, Wade JM, et al. (2008) A robust automated system elucidates mouse home cage behavioral structure. Proc Natl Acad Sci U S A 105: 20575-20582.
36. Fuller PM, Lu J, Saper CB (2008) Differential rescue of light- and foodentrainable circadian rhythms. Science 320: 1074-1077.
37. Mistlberger RE, Buijs RM, Challet E, Escobar C, Landry GJ, et al. (2009) Standards of evidence in chronobiology: critical review of a report that restoration of Bmal1 expression in the dorsomedial hypothalamus is sufficient to restore circadian food anticipatory rhythms in Bmal1-/- mice. J Circadian Rhythms 7: 3.
38. Pendergast JS, Nakamura W, Friday RC, Hatanaka F, Takumi T, et al. (2009) Robust food anticipatory activity in BMAL1-deficient mice. PLoS One 4: e4860.
39. Storch KF, Weitz CJ (2009) Daily rhythms of food-anticipatory behavioral activity do not require the known circadian clock. Proc Natl Acad Sci U S A 106: 6808-6813.
40. Mistlberger RE, Antle MC, Kilduff TS, Jones M (2003) Food- and lightentrained circadian rhythms in rats with hypocretin-2-saporin ablations of the lateral hypothalamus. Brain Res 980: 161-168.
41. Mistlberger RE, Antle MC (1999) Neonatal monosodium glutamate alters circadian organization of feeding, food anticipatory activity and photic masking in the rat. Brain Res 842: 73-83.
42. 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.
43. Mogenson GJ, Jones DL, Yim CY (1980) From motivation to action: functional interface between the limbic system and the motor system. Prog Neurobiol 14: 69-97.
44. Berthoud HR (2004) Mind versus metabolism in the control of food intake and energy balance. Physiol Behav 81: 781-793.
45. Navailles S, Moison D, Ryczko D, Spampinato U (2006) Region-dependent regulation of mesoaccumbens dopamine neurons in vivo by the constitutive activity of central serotonin2C receptors. J Neurochem 99: 1311-1319.
46. De Deurwaerdere P, Navailles S, Berg KA, Clarke WP, Spampinato U (2004) Constitutive activity of the serotonin2C receptor inhibits in vivo dopamine release in the rat striatum and nucleus accumbens. J Neurosci 24: 3235-3241.
47. Abdallah L, Bonasera SJ, Hopf FW, O'Dell L, Giorgetti M, et al. (2009) Increased nigrostriatal dopaminergic neurotransmission in serotonin 2C receptor null mutant mice. Journal of Neuroscience.
48. Petersen CC (2007) The functional organization of the barrel cortex. Neuron 56: 339-355.