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Computational modeling of synchronization process of the circadian timing system of mammals

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Abstract

This paper presents a model for the circadian temporization system of mammals which associates the synchronization dynamics of coupling oscillators to a set of equations able to reproduce the synaptic characteristics of somatodendritic membrane of neurons. The circadian timing system is organized in a way to receive information from the external and internal environments, and its function is the timing organization of physiological and behavioral processes in a circadian pattern. Circadian timing system in mammals is constituted by a group of structures which includes the suprachiasmatic nucleus, the intergeniculate leaflet and the pineal gland. In suprachiasmatic nucleus are found neuron groups working as a biological pacemaker—the so-called biological master clock. By means of numerical simulations using the Kuramoto model, we simulated the dynamics behavior of the biological pacemaker. For this we used a set of 1,000 coupled oscillators with long-range coupling, which were distributed on a 10 × 10 × 10 spherical lattice, and a new method to estimate the order parameter, which characterizes the degree of synchronization of oscillator system. Our model has been able to produce frequency responses in accordance with physiological patterns, and to reproduce two fundamental characteristics of biological rhythms: the endogenous generation and synchronization to the light–dark cycle.

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References

  • Aschoff J (1979) Circadian rhythms: general features and endocrinological aspects. In: Krieger DT (eds) Endocrine rhythms. Raven, New York, pp 1–61

    Google Scholar 

  • Aujard F, Herzog ED, Block GD (2001) Circadian rhythms in firing rate of individual suprachiasmatic nucleus neurons from adult and middle-aged mice. Neuroscience 106: 255–261

    Article  PubMed  CAS  Google Scholar 

  • Baker SN, Olivier E, Lemon RN (1997) Coherent oscillations in monkey motor cortex and hand muscle EMG show task-dependent modulation. J Physiol 501: 225–229

    Article  PubMed  CAS  Google Scholar 

  • Barrett EF, Barrett JN, Crill E (1980) Voltage-sensitive outward currents in cat motoneurones. J Physiol 304: 251–276

    PubMed  CAS  Google Scholar 

  • Carp JS (1992) Physiological properties of primate lumbar motoneurons. J Neurophysiol 68: 1121–1132

    PubMed  CAS  Google Scholar 

  • Cipolla-Neto J, Afeche SC, Menna-Barreto L, Marques N, Benedito-Silva AA, Fortunato G, Recine EG, Schott C (1998) Lack of similarity between the effect of lesions of the suprachiasmatic nucleus and subparaventricular hypothalamic zone on behavioral circadian rhythms. Braz J Med Biol Res 21: 653–654

    Google Scholar 

  • Cruz FAO, Cortez CM (2005) Computer simulation of a central pattern generator via Kuramoto model. Physica A 353: 258–270

    Article  Google Scholar 

  • Dalcin BL, Cruz FAO, Cortez CM, Passos EP (2005) Computer modeling of a spinal reflex circuit. Braz J Phys 35: 987–994

    Article  Google Scholar 

  • Glotzbach SF, Cornett CM, Heller HC (1987) Activity of suprachiasmatic and hypothalamic neurons during sleep and wakefulness in the rat. Brain Res 419: 279–286

    Article  PubMed  CAS  Google Scholar 

  • Groos G, Hendriks J (1982) Circadian rhythms in electrical discharge of rat suprachiasmatic nucleus neurones recorded in vitro. Neurosci Lett 34: 283–288

    Article  PubMed  CAS  Google Scholar 

  • Hendrickson AE, Wagoner N, Cowan WM (1972) An autoradiographic and electron microscopic study of retinohypothalamic connections. Z Zellforsch 135: 1–26

    Article  PubMed  CAS  Google Scholar 

  • Honma S, Ikeda M, Abe H, Tanahashi Y, Namihira M, Honma K, Nomura M (1998) Circadian oscillation of BMAL1, a partner of a mammalian clock gene Clock, in rat suprachiasmatic nucleus. Biochem Biophys Res Commun 250: 83–87

    Article  PubMed  CAS  Google Scholar 

  • Ichikawa T (2001) Mutual coupling among insect neurosecretory cells with an ultradian firing rhythm. Neuroscience 299: 73–76

    CAS  Google Scholar 

  • Inouye ST, Kawamura H (1979) Persistence of circadian rhythmicity in a mammalian hypothalamic “island” containing the suprachiasmatic nucleus. Proc Natl Acad Sci USA 76: 5962–5966

    Article  PubMed  CAS  Google Scholar 

  • Irwin RP, Allen CN (2007) Calcium response to retinohypothalamic tract synaptic transmission in suprachiasmatic nucleus neurons. J Neurosci 27: 11748–11757

    Article  PubMed  CAS  Google Scholar 

  • Jezzini SH, Hill AA, Kuzyk P, Calabrese RL (2004) Detailed model of intersegmental coordination in the timing network of the leech heartbeat central pattern generator. J Neurophysiol 91: 958–977

    Article  PubMed  Google Scholar 

  • Joly S, Pernet V, Dorfman AL, Chemtob S, Lachapelle P (2006) Light-induced retinopathy: comparing adult and juvenile rats. Invest Ophthalmol Vis Sci 47: 3202–3212

    Article  PubMed  Google Scholar 

  • Kim YI, Dudek FE (1992) Intracellular electrophysiological study of suprachiasmatic nucleus neurons in rodents: inhibitory synaptic mechanisms. J Physiol 458: 247–260

    PubMed  CAS  Google Scholar 

  • Kim YI, Dudek FE (1993) Membrane properties of rat suprachiasmatic nucleus neurons receiving optic nerve input. J Physiol 464: 229–243

    PubMed  CAS  Google Scholar 

  • Kononenko NI, Dudek FE (2004) Mechanism of irregular firing of suprachiasmatic nucleus neurons in rat hypothalamic slices. J Neurophysiol 91: 267–273

    Article  PubMed  Google Scholar 

  • Kudela P, Franaszczuk PJ, Bergey GK (1997) A simple computer model of excitable synaptically connected neurons. Biol Cybern 77: 71–77

    Article  PubMed  CAS  Google Scholar 

  • Kuramoto Y (1984) Chemical oscillation, waves and turbulence. Springer, Berlin

    Google Scholar 

  • Lockley SW, Arend Jt, Skene DJ (2007) Visual impairment and circadian rhythm disorders. Dialogues Clin Neurosci 9: 301–314

    PubMed  Google Scholar 

  • Marques MD, Waterhouse JM (1994) Masking and the evolution of circadian rhythmicity. Cronobiol Int 11: 146–155

    Article  CAS  Google Scholar 

  • Meijer JH, Rietveld WJ (1989) Neurophysiology of the suprachiasmatic circadian pacemaker in rodents. Physiol Rev 69: 671–707

    PubMed  CAS  Google Scholar 

  • Mendell LM, Henneman E (1971) Terminals of single Ia fibers: location, density, and distribution within a pool of 300 homonymous motoneurons. J Neurophysiol 34: 171–187

    PubMed  CAS  Google Scholar 

  • Moga MM, Weis RP, Moore RY (1995) Efferent projections of the paraventricular thalamic nucleus in the rat. J Comp Neurol 359: 221–238

    Article  PubMed  CAS  Google Scholar 

  • Moore RY (1991) The suprachiasmatic nucleus and the circadian timing system. In: Klein DC, Moore RY, Reppert SM (eds) Suprachiasmatic nucleus: the mind’s clock. Oxford University Press, New York, pp 13–15

    Google Scholar 

  • Moore RY (1992) The organization of the human circadian timing system. Prog Brain Res 93: 101–117

    Article  Google Scholar 

  • Moore RY, Lenn NJ (1972) A retinohypothalamic projection in the rat. J Comp Neurol 180: 1–14

    Article  Google Scholar 

  • Moore-Ede MC (1986) Physiology of the circadian timing system: predictive versus reactive homeostasis. Am J Physiol 250: 735–752

    Google Scholar 

  • Morin LP (1994) The circadian visual system. Brain Res Rev 19: 102–127

    Article  PubMed  CAS  Google Scholar 

  • Murthy VN, Fetz EE (1996) Coherent 25-Hz to 35-Hz oscillations in the sensorimotor cortex of awake behaving monkeys. Proc Natl Acad Sci USA 89: 5670–5677

    Article  Google Scholar 

  • Nakamura W, Honma S, Shirakawa T, Honma K (2001) Regional pacemakers composed of multiple oscillator neurons in the rat suprachiasmatic nucleus. Eur J Neurosci 14: 666–674

    Article  PubMed  CAS  Google Scholar 

  • Negroni J, Nevo E, Cooper HM (1997) Neuropeptidergic organization of the suprachiasmatic nucleus in the blind mole rat (Spalax ehrenbergi). Brain Res Bull 44: 633–639

    Article  PubMed  CAS  Google Scholar 

  • Nishino H (1976) Activity of neurons of the hypothalamic suprachiasmatic nuclei and circadian rhythms: the role of the suprachiasmatic nuclei. Nippon Yakurigaku Zasshi 72: 941–954

    PubMed  CAS  Google Scholar 

  • Pennart CM, Bos NP, Jeu MT, Geurtsen AM, Mirmiran M, Sluiter AA, Buijs RM (1998) Membrane properties and morphology of vasopressin neurons in slices of rat suprachiasmatic nucleus. J Neurophysiol 80: 2710–2717

    Google Scholar 

  • Proakis JG, Manolakis DG (1992) Digital signal processing: principles, algorithms, and applications, 2nd edn. Macmillan Publishing Company, New York

    Google Scholar 

  • Reinberg A, Smolensky MH (1982) Circadian changes of drug disposition in man. Clin Pharmacokinet 7: 401–420

    Article  PubMed  CAS  Google Scholar 

  • Reuss S (1996) Components and connections of the circadian timing system in mammals. Cell Tissue Res 285: 353–378

    Article  PubMed  CAS  Google Scholar 

  • Rusak B, Zucker I (1979) Neural regulation of circadian rhythms. Physiol Rev 59: 449–526

    PubMed  CAS  Google Scholar 

  • Sawaki Y (1979) Suprachiasmatic nucleus neurones: excitation and inhibition mediated by the direct retino-hypothalamic projection in female rats. Exp Brain Res 37: 127–138

    Article  PubMed  CAS  Google Scholar 

  • Schaap J, Bos NP, de Jeu MT, Geurtsen AM, Meijer JH, Pennartz CM (1999) Neurons of the rat suprachiasmatic nucleus show a circadian rhythm in membrane properties that is lost during prolonged whole-cell recording. Brain Res 815: 154–166

    Article  PubMed  CAS  Google Scholar 

  • Shibata S, Moore RY (1988) Electrical and metabolic activity of suprachiasmatic nucleus neurons in hamster hypothalamic slices. Brain Res 438: 374–378

    Article  PubMed  CAS  Google Scholar 

  • Turek FW (1994) Circadian rhythms. Recent Prog Horm Res 49: 43–90

    PubMed  CAS  Google Scholar 

  • Van Den Pol AN (1980) The hypothalamic suprachiasmatic nucleus of rat: intrinsic anatomy. J Comp Neurol 191: 661–702

    Article  PubMed  CAS  Google Scholar 

  • Van Den Pol AN, Tsujimoto JL (1985) Neurotransmitters of the hypothalamic suprachiasmatic nucleus: immunocytochemical analysis of 25 neuronal antigens. Neuroscience 15: 1049–1086

    Article  PubMed  CAS  Google Scholar 

  • Walsh IB, van den Berg RJ, Marani E, Rietveld WJ (1992) Spontaneous and stimulated firing in cultured rat suprachiasmatic neurons. Brain Res 588: 120–131

    Article  PubMed  CAS  Google Scholar 

  • Wickland C, Turek TW (1994) Lesion of the thalamic intergeniculate leaflet block activity-induced phase shifts in the circadian activity rhythm of the golfem hamster. Brain Res 660: 293–300

    Article  PubMed  CAS  Google Scholar 

  • Zlomanczuk P, Margraf RR, Lynch GR (1991) In vitro electrical activity in the suprachiasmatic nucleus following splitting and masking of wheel-running behavior. Brain Res 559: 94–99

    Article  PubMed  CAS  Google Scholar 

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Correspondence to Célia Martins Cortez.

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Cardoso, F.R.G., de Oliveira Cruz, F.A., Silva, D. et al. Computational modeling of synchronization process of the circadian timing system of mammals. Biol Cybern 100, 385–393 (2009). https://doi.org/10.1007/s00422-009-0309-6

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  • DOI: https://doi.org/10.1007/s00422-009-0309-6

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