Enhanced phase resetting in the synchronized suprachiasmatic nucleus network

Journal of Biological Rhythms

Volumn 29, Issue 1, 2014, Pages 4-15

  Ramkisoensing, Ashna ^a   Gu, Changgui ^a   Van Engeldorp Gastelaars, Heleen M D ^a   Michel, Stephan ^a   Deboer, Tom ^a   Rohling, Jos H T ^a   Meijer, Johanna H ^a  

^a LEIDEN UNIVERSITY MEDICAL CENTER   (Netherlands)

Author keywords

activity; behavior; circadian; electrophysiology; entrainment; limit cycle oscillator; photoperiod

Indexed keywords

ACTION POTENTIAL; ACTIVITY; ALGORITHM; ANIMAL; ARTICLE; BEHAVIOR; BIOLOGICAL MODEL; C57BL MOUSE; CIRCADIAN; CIRCADIAN RHYTHM; DARKNESS; ELECTROPHYSIOLOGY; ELECTROSTIMULATION; ENTRAINMENT; IN VITRO STUDY; LIGHT; LIMIT CYCLE OSCILLATOR; MOTOR ACTIVITY; MOUSE; PHOTOPERIODICITY; PHYSIOLOGY; RADIATION EXPOSURE; SUPRACHIASMATIC NUCLEUS;

ACTIVITY; BEHAVIOR; CIRCADIAN; ELECTROPHYSIOLOGY; ENTRAINMENT; LIMIT CYCLE OSCILLATOR; PHOTOPERIOD;

ACTION POTENTIALS; ALGORITHMS; ANIMALS; CIRCADIAN RHYTHM; DARKNESS; ELECTRIC STIMULATION; LIGHT; MICE; MICE, INBRED C57BL; MODELS, NEUROLOGICAL; MOTOR ACTIVITY; PHOTOPERIOD; SUPRACHIASMATIC NUCLEUS;

EID: 84893588132     PISSN: 07487304     EISSN: 15524531     Source Type: Journal    
DOI: 10.1177/0748730413516750     Document Type: Article

References (57)

1. Abraham U, Granada AE, Westermark PO, Heine M, Kramer A, Herzel H. Coupling governs entrainment range of circadian clocks. Mol Syst Biol. 2010 ; 6: 438
2. Akiyama M, Kouzu Y, Takahashi S, Wakamatsu H, Moriya T, Maetani M, Watanabe S, Tei H, Sakaki Y, Shibata S. Inhibition of light- or glutamate-induced mPer1 expression represses the phase shifts into the mouse circadian locomotor and suprachiasmatic firing rhythms. J Neurosci. 1999 ; 19: 1115-1121 (Pubitemid 29066172)
3. Albrecht U, Sun ZS, Eichele G, Lee CC. A differential response of two putative mammalian circadian regulators, mper1 and mper2, to light. Cell. 1997 ; 91: 1055-1064 (Pubitemid 28027837)
4. Antle MC, Smith VM, Sterniczuk R, Yamakawa GR, Rakai BD. Physiological responses of the circadian clock to acute light exposure at night. Rev Endocr Metab Disord. 2009 ; 10: 279-291
5. Biello SM, Mrosovsky N. Phase response curves to neuropeptide Y in wildtype and tau mutant hamsters. J Biol Rhythms. 1996 ; 11: 27-34 (Pubitemid 126482591)
6. Brown TM, Hughes AT, Piggins HD. Gastrin-releasing peptide promotes suprachiasmatic nuclei cellular rhythmicity in the absence of vasoactive intestinal polypeptide-VPAC2 receptor signaling. J Neurosci. 2005 ; 25: 11155-11164 (Pubitemid 43089560)
7. Brown TM, Piggins HD. Spatiotemporal heterogeneity in the electrical activity of suprachiasmatic nuclei neurons and their response to photoperiod. J Biol Rhythms. 2009 ; 24: 44-54
8. Cao R, Robinson B, Xu H, Gkogkas C, Khoutorsky A, Alain T, Yanagiya A, Nevarko T, Liu AC, Amir S, Sonenberg N. Translational control of entrainment and synchrony of the suprachiasmatic circadian clock by mTOR/4E-BP1 signaling. Neuron. 2013 ; 79: 712-724
9. Daan S, Merrow M, Roenneberg T. External time: internal time. J Biol Rhythms. 2002 ; 17: 107-109
10. Deboer T, Tobler I. Running wheel size influences circadian rhythm period and its phase shift in mice. J Comp Physiol A. 2000 ; 186: 969-973
11. Ding JM, Buchanan GF, Tischkau SA, Chen D, Kuriashkina L, Faiman LE, Alster JM, McPherson PS, Campbell KP, Gillette MU. A neuronal ryanodine receptor mediates light-induced phase delays of the circadian clock. Nature. 1998 ; 394: 381-384 (Pubitemid 28373835)
12. Eilers PH. A perfect smoother. Anal Chem. 2003 ; 75: 3631-3636 (Pubitemid 36871257)
13. Field MD, Maywood ES, O'Brien JA, Weaver DR, Reppert SM, Hastings MH. Analysis of clock proteins in mouse SCN demonstrates phylogenetic divergence of the circadian clockwork and resetting mechanisms. Neuron. 2000 ; 25: 437-447
14. Forger DB, Peskin CS. A detailed predictive model of the mammalian circadian clock. Proc Natl Acad Sci U S A. 2003 ; 100: 14806-14811 (Pubitemid 37517972)
15. Gillette MU, Mitchell JW. Signaling in the suprachiasmatic nucleus: selectively responsive and integrative. Cell Tissue Res. 2002 ; 309: 99-107 (Pubitemid 34744032)
16. Goldbeter A. A model for circadian oscillations in the Drosophila period protein (PER). Proc Biol Sci. 1995 ; 261: 319-324
17. Guilding C, Scott F, Bechtold DA, Brown TM, Wegner S, Piggins HD. Suppressed cellular oscillations in after-hours mutant mice are associated with enhanced circadian phase-resetting. J Physiol. 2013 ; 591: 1063-1080
18. Hazlerigg DG, Ebling FJ, Johnston JD. Photoperiod differentially regulates gene expression rhythms in the rostral and caudal SCN. Curr Biol. 2005 ; 15: R449 - R450
19. Hosokawa N, Kushige H, Iwasaki H. Attenuation of the posttranslational oscillator via transcription-translation feedback enhances circadian-phase shifts in Synechococcus. Proc Natl Acad Sci U S A. 2013 ; 110: 14486-14491
20. Inagaki N, Honma S, Ono D, Tanahashi Y, Honma K. Separate oscillating cell groups in mouse suprachiasmatic nucleus couple photoperiodically to the onset and end of daily activity. Proc Natl Acad Sci U S A. 2007 ; 104: 7664-7669 (Pubitemid 47185963)
21. Janik D, Mrosovsky N. Nonphotically induced phase shifts of circadian rhythms in the golden hamster: activity-response curves at different ambient temperatures. Physiol Behav. 1993 ; 53: 431-436 (Pubitemid 23080563)
22. Johnson CH. Forty years of PRCs: what have we learned?. Chronobiol Int. 1999 ; 16: 711-743
23. Johnson CH, Hastings JW. Circadian phototransduction: phase resetting and frequency of the circadian clock of Gonyaulax cells in red light. J Biol Rhythms. 1989 ; 4: 417-437
24. Johnson EC, Voyles WF, Atterbom HA, Pathak D, Sutton MF, Greene ER. Effects of exercise training on common femoral artery blood flow in patients with intermittent claudication. Circulation. 1989 ; 80: III59 - III72
25. Johnston JD, Ebling FJ, Hazlerigg DG. Photoperiod regulates multiple gene expression in the suprachiasmatic nuclei and pars tuberalis of the Siberian hamster (Phodopus sungorus). Eur J Neurosci. 2005 ; 21: 2967-2974 (Pubitemid 40917061)
26. Kronauer RE, Czeisler CA, Pilato SF, Moore-Ede MC, Weitzman ED. Mathematical model of the human circadian system with two interacting oscillators. Am J Physiol. 1982 ; 242: R3 - R17
27. Malinowski JR, Laval-Martin DL, Edmunds LN. Circadian oscillators, cell cycles, and singularities: light perturbations of the free-running rhythm of cell division in Euglena. J Comp Physiol B. 1985 ; 155: 257-267
28. Meijer JH, Michel S, Vanderleest HT, Rohling JHT. Daily and seasonal adaptation of the circadian clock requires plasticity of the SCN neuronal network. Eur J Neurosci. 2010 ; 32: 2143-2151
29. Meijer JH, Colwell CS, Rohling JHT, Houben T, Michel S. Dynamic neuronal network organization of the circadian clock and possible deterioration in disease. Prog Brain Res. 2012 ; 199: 143-162
30. Mohawk JA, Pezuk P, Menaker M. Methamphetamine and dopamine receptor D1 regulate entrainment of murine circadian oscillators. PLoS One. 2013 ; 8: e62463
31. Morin LP, Allen CN. The circadian visual system, 2005. Brain Res Rev. 2006 ; 51: 1-60 (Pubitemid 44218910)
32. Myung J, Hong S, Hatanaka F, Nakajima Y, De Schutter E, Takumi T. Period coding of Bmal1 oscillators in the suprachiasmatic nucleus. J Neurosci. 2012 ; 32: 8900-8918
33. Naito E, Watanabe T, Tei H, Yoshimura T, Ebihara S. Reorganization of the suprachiasmatic nucleus coding for day length. J Biol Rhythms. 2008 ; 23: 140-149 (Pubitemid 351393176)
34. Obrietan K, Impey S, Storm DR. Light and circadian rhythmicity regulate MAP kinase activation in the suprachiasmatic nuclei. Nat Neurosci. 1998 ; 1: 693-700 (Pubitemid 128406380)
35. Paul MJ, Indic P, Schwartz WJ. A role for the habenula in the regulation of locomotor activity cycles. Eur J Neurosci. 2011 ; 34: 478-488
36. Phillips AJ, Fulcher BD, Robinson PA, Klerman EB. Mammalian rest/activity patterns explained by physiologically based modeling. PLoS Comput Biol. 2013 ; 9: e1003213
37. Pittendrigh CS, Elliott J, Takamura T Ciba Foundation Symposium 104: Photoperiodic Regulation of Insect and Molluscan Hormones. Porter R Collins GM, ed. Chichester, UK: John Wiley & Sons Ltd ; 2008: 26-47.
38. Pittendrigh CS, Kyner WT, Takamura T. The amplitude of circadian oscillations: temperature dependence, latitudinal clines, and the photoperiodic time measurement. J Biol Rhythms. 1991 ; 6: 299-313
39. Ralph MR, Foster RG, Davis FC, Menaker M. Transplanted suprachiasmatic nucleus determines circadian period. Science. 1990 ; 247: 975-978
40. Reebs SG, Mrosovsky N. Effects of induced wheel running on the circadian activity rhythms of Syrian hamsters: entrainment and phase response curve. J Biol Rhythms. 1989a ; 4: 39-48
41. Reebs SG, Mrosovsky N. Large phase-shifts of circadian rhythms caused by induced running in a re-entrainment paradigm: the role of pulse duration and light. J Comp Physiol A. 1989b ; 165: 819-825
42. Refinetti R. Compression and expansion of circadian rhythm in mice under long and short photoperiods. Integr Physiol Behav Sci. 2002 ; 37: 114-127
43. Refinetti R. Effects of prolonged exposure to darkness on circadian photic responsiveness in the mouse. Chronobiol Int. 2003 ; 20: 417-440 (Pubitemid 36828476)
44. Rohling J, Wolters L, Meijer JH. Simulation of day-length encoding in the SCN: from single-cell to tissue-level organization. J Biol Rhythms. 2006 ; 21: 301-313 (Pubitemid 44078723)
45. Schaap J, Albus H, VanderLeest HT, Eilers PH, Detari L, Meijer JH. Heterogeneity of rhythmic suprachiasmatic nucleus neurons: implications for circadian waveform and photoperiodic encoding. Proc Natl Acad Sci U S A. 2003 ; 100: 15994-15999 (Pubitemid 38021103)
46. Schwartz WJ, Tavakoli-Nezhad M, Lambert CM, Weaver DR, de la Iglesia HO. Distinct patterns of Period gene expression in the suprachiasmatic nucleus underlie circadian clock photoentrainment by advances or delays. Proc Natl Acad Sci U S A. 2011 ; 108: 17219-17224
47. Sellix MT, Evans JA, Leise TL, Castanon-Cervantes O, Hill DD, DeLisser P, Block GD, Menaker M, Davidson AJ. Aging differentially affects the re-entrainment response of central and peripheral circadian oscillators. J Neurosci. 2012 ; 32: 16193-16202
48. VanderLeest HT, Houben T, Michel S, Deboer T, Albus H, Vansteensel MJ, Block GD, Meijer JH. Seasonal encoding by the circadian pacemaker of the SCN. Curr Biol. 2007 ; 17: 468-473
49. vanderLeest HT, Rohling JH, Michel S, Meijer JH. Phase shifting capacity of the circadian pacemaker determined by the SCN neuronal network organization. PLoS One. 2009 ; 4: e4976
50. van Oosterhout F, Lucassen EA, Houben T, vanderLeest HT, Antle MC, Meijer JH. Amplitude of the SCN clock enhanced by the behavioral activity rhythm. PLoS One. 2012 ; 7: e39693
51. Vansteensel MJ, Yamazaki S, Albus H, Deboer T, Block GD, Meijer JH. Dissociation between circadian Per1 and neuronal and behavioral rhythms following a shifted environmental cycle. Curr Biol. 2003 ; 13: 1538-1542 (Pubitemid 37078411)
52. Vitaterna MH, Ko CH, Chang AM, Buhr ED, Fruechte EM, Schook A, Antoch MP, Turek FW, Takahashi JS. The mouse Clock mutation reduces circadian pacemaker amplitude and enhances efficacy of resetting stimuli and phase-response curve amplitude. Proc Natl Acad Sci U S A. 2006 ; 103: 9327-9332 (Pubitemid 43902576)
53. Welsh DK, Takahashi JS, Kay SA. Suprachiasmatic nucleus: cell autonomy and network properties. Annu Rev Physiol. 2010 ; 72: 551-577
54. Winfree AT The Geometry of Biological Time. New York: Springer-Verlag ; 2001 :
55. Yamanaka Y, Honma S, Honma K. Scheduled exposures to a novel environment with a running-wheel differentially accelerate re-entrainment of mice peripheral clocks to new light-dark cycles. Genes Cells. 2008 ; 13: 497-507 (Pubitemid 351567050)
56. 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 (Pubitemid 35334990)
57. Zylka MJ, Shearman LP, Weaver DR, Reppert SM. Three period homologs in mammals: differential light responses in the suprachiasmatic circadian clock and oscillating transcripts outside of brain. Neuron. 1998 ; 20: 1103-1110 (Pubitemid 28293128)