A multiscale model to investigate circadian rhythmicity of pacemaker neurons in the suprachiasmatic nucleus

PLoS Computational Biology

Volumn 6, Issue 3, 2010, Pages

  Vasalou, Christina ^a   Henson, Michael A ^a  

^a University of Massachusetts   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CALCIUM; DIGITAL STORAGE; MAMMALS; TRANSCRIPTION;

DAILY RHYTHM; FIRING FREQUENCY; FIRING RATES; GENE REGULATORY NETWORKS; GENES EXPRESSION; MULTICELLULAR SYSTEMS; MULTISCALE MODELING; PACEMAKER NEURONS; RATE CODES; SUPRACHIASMATIC NUCLEUS;

ELECTROPHYSIOLOGY;

4 AMINOBUTYRIC ACID; CALCIUM; NEUROTRANSMITTER; PROTEIN; PROTEIN PER; UNCLASSIFIED DRUG; VASOACTIVE INTESTINAL POLYPEPTIDE;

ARTICLE; CALCIUM CELL LEVEL; CALCIUM METABOLISM; CALCIUM SIGNALING; CELL FUNCTION; CIRCADIAN RHYTHM; CONTROLLED STUDY; GABAERGIC TRANSMISSION; GENE EXPRESSION; GENETIC REGULATION; GENETIC TRANSCRIPTION; ION CONDUCTANCE; MATHEMATICAL MODEL; MEMBRANE DEPOLARIZATION; MOLECULAR DYNAMICS; NERVE CELL MEMBRANE POTENTIAL; NERVOUS SYSTEM ELECTROPHYSIOLOGY; OSCILLATORY POTENTIAL; PACEMAKER NERVE CELL; SUPRACHIASMATIC NUCLEUS; SYNAPTIC TRANSMISSION; ANIMAL; BIOLOGICAL MODEL; BIOLOGICAL RHYTHM; COMPUTER SIMULATION; HUMAN; NERVE CELL; NERVE CELL NETWORK; PHYSIOLOGY;

MAMMALIA;

ANIMALS; BIOLOGICAL CLOCKS; CIRCADIAN RHYTHM; COMPUTER SIMULATION; HUMANS; MODELS, NEUROLOGICAL; NERVE NET; NEURONS; SUPRACHIASMATIC NUCLEUS;

EID: 77950793989     PISSN: 1553734X     EISSN: 15537358     Source Type: Journal    
DOI: 10.1371/journal.pcbi.1000706     Document Type: Article

References (49)

1. Welsh DK, Logothetis DE, Meister M, Reppert SM (1995) Individual neurons dissociated from rat suprachiasmatic nucleus express independently phased circadian firing rhythms. Neuron 14: 697-706.
2. Reppert SM, Weaver DR (2002) Coordination of circadian timing in mammals. Nature 418: 935-941.
3. Brown TM, Piggins HD (2007) Electrophysiology of the suprachiasmatic circadian clock. Prog Neurobiol 82: 229-255.
4. Ikeda M, Sugiyama T, Wallace CS, Gompf HS, Yoshioka T, et al. (2003) Circadian dynamics of cytosolic and nuclear Ca2+ in single suprachiasmatic nucleus neurons. Neuron 38: 253-263.
5. Kuhlman SJ, McMahon DG (2004) Rhythmic regulation of membrane potential and potassium current persists in SCN neurons in the absence of environmental input. Euro J Neurosci 20: 1113-1117.
6. Pennartz CMA, de Jeu MTG, Bos NPA, Schaap J, Geurtsen AMS (2002) Diurnal modulation of pacemaker potentials and calcium current in the mammalian circadian clock. Nature 416: 286-290.
7. Itri JN, Michel S, Vansteensel MJ, Meijer JH, Colwell CS (2005) Fast delayed rectifier potassium current is required for circadian neural activity. Nat Neurosci 8: 650-656.
8. Meredith AL, Wiler SW, Miller BH, Takahashi JS, Fodor AA, et al. (2006) BK calcium-activated potassium channels regulate circadian behavioral rhythms and pacemaker output. Nat Neurosci 9: 1041-1049.
9. Pitts GR, Ohta H, McMahon DG (2006) Daily rhythmicity of large-conductance Ca2+-activated K+ currents in suprachiasmatic nucleus neurons. Brain Res 1071: 54-62.
10. Nitabach MN, Blau J, Holmes TC (2002) Electrical silencing of Drosophila pacemaker neurons stops the free-running circadian clock. Cell 109: 485-495.
11. Quintero JE, Kuhlman SJ, McMahon DG (2003) The biological clock nucleus: A multiphasic oscillator network regulated by light. J Neurosci 23: 8070-8076.
12. Ehlen JC, Novak CM, Karom MC, Gamble KL, Paul KN, et al. (2006) GABA(A) receptor activation suppresses Period 1 mRNA and Period 2 mRNA in the suprachiasmatic nucleus during the mid-subjective day. Euro J Neurosci 23: 3328-3336.
13. Ehlen JC, Novak CM, Karom MC, Gamble KL, Albers HE (2008) Interactions of GABA(A) receptor activation and light on Period mRNA expression in the suprachiasmatic nucleus. J Biol Rhythm 23: 16-25.
14. Gribkoff VK, Pieschl RL, Dudek FE (2003) GABA receptor-mediated inhibition of neuronal activity in rat SCN in vitro: Pharmacology and influence of circadian phase. J Neurophysiol 90: 1438-1448.
15. Shirakawa T, Honma S, Katsuno Y, Oguchi H, Honma K (2000) Synchronization of circadian firing rhythms in cultured rat suprachiasmatic neurons. Euro J Neurosci 12: 2833-2838.
16. Maywood ES, Reddy AB, Wong GKY, O'Neill JS, O'Brien JA, et al. (2006) Synchronization and maintenance of timekeeping in suprachiasmatic circadian clock cells by neuropeptidergic signaling. Curr Biol 16: 599-605.
17. Brown TM, Colwell CS, Waschek JA, Piggins HD (2007) Disrupted neuronal activity rhythms in the suprachiasmatic nuclei of vasoactive intestinal polypeptide-deficient mice. J Neurophysiol 97: 2553-2558.
18. Honma S, Honma K (2003) The biological clock: Ca2+ links the pendulum to the hands. Trends Neurosci 26: 650-653.
19. Tischkau SA, Mitchell JW, Tyan SH, Buchanan GF, Gillette MU (2003) Ca2+/cAMP response element-binding protein (CREB)-dependent activation of Per1 is required for light-induced signaling in the Suprachiasmatic nucleus circadian clock. J Biol Chem 278: 718-723.
20. Lundkvist GB, Kwak Y, Davis EK, Tei H, Block GD (2005) A calcium flux is required for circadian rhythm generation in mammalian pacemaker neurons. J Neurosci 25: 7682-7686.
21. Goldbeter A, Dupont G, Berridge MJ (1990) Minimal model for signal-induced Ca2+ oscillations and for their frequency encoding through protein-phosphorylation. P Natl Acad Sci USA 87: 1461-1465.
22. Jackson AC, Yao GL, Bean BP (2004) Mechanism of spontaneous firing in dorsomedial suprachiasmatic nucleus neurons. J Neurosci 24: 7985-7998.
23. Cloues RK, Sather WA (2003) Afterhyperpolarization regulates firing rate in neurons of the suprachiasmatic nucleus. J Neurosci 23: 1593-1604.
24. Itri J, Michel S, Waschek JA, Colwell CS (2004) Circadian rhythm in inhibitory synaptic transmission in the mouse suprachiasmatic nucleus. J Neurophysi 92: 311-319.
25. Obrietan K, Impey S, Smith D, Athos J, Storm DR (1999) Circadian regulation of cAMP response element-mediated gene expression in the Suprachiasmatic nuclei. J Biol Chem 274: 17748-17756.
26. Itri J, Colwell CS (2003) Regulation of inhibitory synaptic transmission by vasoactive intestinal peptide (VIP) in the mouse suprachiasmatic nucleus. J Neurophysi 90: 1589-1597.
27. Albus H, Vansteensel MJ, Michel S, Block GD, Meijer JH, et al. (2005) A GABAergic mechanism is necessary for coupling dissociable ventral and dorsal regional oscillators within the circadian clock. Curr Biol 15: 886-893.
28. Choi HJ, Lee CJ, Schroeder A, Kim YS, Jung SH, et al. (2008) Excitatory actions of GABA in the suprachiasmatic nucleus. J Neurosci 28: 5450-5459.
29. Leloup JC, Goldbeter A (2003) Toward a detailed computational model for the mammalian circadian clock. P Natl Acad Sci USA 100: 7051-7056.
30. Gerstner W, Kistler WM (2002) Spiking Neuron Models: Single Neurons, Populations, Plasticity. Cambridge University Press. pp. 93-97.
31. Liu YH, Wang XJ (2001) Spike-frequency adaptation of a generalized leaky integrate-and-fire model neuron. J Comput Neurosci 10: 25-45.
32. Hodgkin AL, Huxley AF (1952) A quantitative description of membrane current and its application to conduction and excitation in nerve. J Physiol-London 117: 500-544.
33. French DA, Gruenstein EI (2006) An integrate-and-fire model for synchronized bursting in a network of cultured cortical neurons. J Comput Neurosci 21: 227-241.
34. Burkitt AN (2006) A review of the integrate-and-fire neuron model: II. Inhomogeneous synaptic input and network properties. Biol Cybern 95: 97-112.
35. Bouskila Y, Dudek FE (1995) A rapidly activating type of outward rectifier K+ current and A-current in rat suprachiasmatic nucleus neurons. J Physiol-London 488: 339-350.
36. Hille B (1992) Ionic channels of excitable membranes. 2nd ed. Sunderland, Mass: Sinauer Associates.
37. Sim CK, Forger DB (2007) Modeling the electrophysiology of Suprachiasmatic nucleus neurons. J Biol Rhythm 22: 445-453.
38. Wagner S, Castel M, Gainer H, Yarom Y (1997) GABA in the mammalian suprachiasmatic nucleus and its role in diurnal rhythmicity. Nature 387: 598-603.
39. Purves D, Augustine GJ, Fitzpatrick D, Hall WC, LaMantia A, et al. (2008) Neuroscience. Fourth ed 25-39.
40. Wagner S, Sagiv N, Yarom Y (2001) GABA-induced current and circadian regulation of chloride in neurones of the rat suprachiasmatic nucleus. J Physiol-London 537: 853-869.
41. Shimura M, Akaike N, Harata N (2002) Circadian rhythm in intracellular Cl- activity of acutely dissociated neurons of suprachiasmatic nucleus. Am J Physiol-Cell Ph 282: C366-C373.
42. Lundkvist GB, Kristensson K, Hill RH (2002) The Suprachiasmatic nucleus exhibits diurnal variations in spontaneous excitatory postsynaptic activity. J Biol Rhythm 17: 40-51.
43. Michel S, Itri J, Colwell CS (2002) Excitatory mechanisms in the suprachiasmatic nucleus: The role of AMPA/KA glutamate receptors. J Neurophysi 88: 817-828.
44. Colwell CS (2001) NMDA-evoked calcium transients and currents in the suprachiasmatic nucleus: gating by the circadian system. Euro J Neurosci 13: 1420-1428.
45. Irwin RP, Allen CN (2007) Calcium response to retinohypothalamic tract synaptic transmission in Suprachiasmatic nucleus neurons. J Neurosci 27: 11748-11757.
46. Piek TP.N.R U, editor (1975) Ionic and electrical properties. Insect Muscle. London: New York and San Francisco: Academic Press. pp. 281-336.
47. Kandel ER, Schwartz JH, Jessel TM (2000) Principles of Neural Science. Fourth ed 125-139.
48. To TL, Henson MA, Herzog ED, Doyle FJ (2007) A molecular model for intercellular synchronization in the mammalian circadian clock. Biophys J 92: 3792-3803.
49. Dunlap JC (1999) Molecular bases for circadian clocks. Cell 96: 271-290.