Skip to main content

Coupling-induced synchronization in multicellular circadian oscillators of mammals

Cognitive Neurodynamics volume 7, pages 59–65 (2013)Cite this article

Abstract

In mammals, circadian rhythms are controlled by the neurons located in the suprachiasmatic nucleus (SCN) of the hypothalamus. Each neuron in the SCN contains an autonomous molecular clock. The fundamental question is how the individual cellular oscillators, expressing a wide range of periods, interact and assemble to achieve phase synchronization. Most of the studies carried out so far emphasize the crucial role of the periodicity imposed by the light-dark cycle in neuronal synchronization. However, in natural conditions, the interaction between the SCN neurons is non-negligible and coupling between cells in the SCN is achieved partly by neurotransmitters. In this paper, we use a model of nonidentical, globally coupled cellular clocks considered as Goodwin oscillators. We mainly study the synchronization induced by coupling from an analytical way. Our results show that the role of the coupling is to enhance the synchronization to the external forcing. The conclusion of this paper can help us better understand the mechanism of circadian rhythm.

This is a preview of subscription content, access via your institution.

Access options

Buy single article

Instant access to the full article PDF.

43,34 €

Price includes VAT (Finland)
Tax calculation will be finalised during checkout.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8

References

  • Antle MC, Foley DK, Foley NC, Silver R (2003) Gates and oscillators: a network model of the brain clock. J Biol Rhythms 18(4):339–350

    PubMed  Article  Google Scholar 

  • Antle MC, Foley NC, Foley DK, Silver R (2007) Gates and oscillators II: zeitgebers and the network model of the brain clock. J Biol Rhythms 22(1):14–25

    PubMed  Article  Google Scholar 

  • Aton S, Colwell C, Harmar A, Waschek J, Herzog E (2005) Vasoactive intestinal polypeptide mediates circadian rhythmicity and synchrony in mammalian clock neurons. Nat Neurosci 8:476–483

    PubMed  CAS  Google Scholar 

  • Benuskova L, Kasabov N (2008) Modeling brain dynamics using computational neurogenetic approach. Cogn Neurodyn 2(4):319–334

    PubMed  Article  Google Scholar 

  • Bush W, Siegelman HT (2006) Circadian synchrony in networks of protein rhythm driven neurons. Complexity 12:67–72

    Article  Google Scholar 

  • Gonze D, Bernard S, Waltermann C, Kramer A, Herzel H (2005) Spontaneous synchronization of coupled circadian oscillators. Biophys J 89:120–129

    PubMed  Article  CAS  Google Scholar 

  • Goodwin B (1965) Oscillatory behavior in enzymatic control processes. Adv Enzyme Regul 3:524–438

    Article  Google Scholar 

  • Hamada T, LeSauter J, Venuti JM, Silver R (2001) Expression of Period genes: rhythmic and nonrhythmic compartments of the suprachiasmatic nucleus pacemaker. J Neurosci 21(19):7742–7750

    CAS  Google Scholar 

  • Hastings M, Herzog E (2004) Clock genes, oscillators, and cellular networks in the suprachiasmatic nuclei. J Biol Rhythms 19:400–413

    PubMed  Article  CAS  Google Scholar 

  • Honma S, Nakamura W, Shirakawa T, Honma K (2004) Diversity in the circadian periods of single neurons of the rat suprachiasmatic nucleus on nuclear structure and intrinsic period. Neurosci Lett 358:173–176

    PubMed  Article  CAS  Google Scholar 

  • Indic P, Schwartz WJ, Herzog ED, Foley NC, Antle MC (2007) Modeling the behavior of coupled cellular circadian oscillators in the suprachiasmatic nucleus. J Biol Rhythms 22(3):211–219

    PubMed  Article  Google Scholar 

  • Jiao XF, Wang RB (2006) Synchronization in neuronal population with the variable coupling strength in the presence of external stimulus. Appl Phys Lett 88:203901

    Article  Google Scholar 

  • Jordi GO, Michael BE, Steven HS (2004) Modeling a synthetic multicellular clock: repressilators coupled by quorum sensing. PNAS 101(30):10955–10960

    Article  Google Scholar 

  • Katriel G (2008) Synchronization of oscillators coupled through an environment. Phys D 237:2933–2944

    Article  Google Scholar 

  • Komin N, Murza AC, Hernandez-Garcia E, Toral R (2011) Synchronization and entrainment of coupled circadian oscillators. Biol Phys 1:167–176

    CAS  Google Scholar 

  • Kori H, Kawamura Y, Masuda N (2012) Structure of cell networks critically determines oscillation regularity. J Theor Biol 297:61–72

    Google Scholar 

  • Li Y, Zhang J, Liu Z (2006) Circadian oscillators and phase synchronization under a light-dark cycle. Int J Nonlinear Sci 1(3):131–138

    Google Scholar 

  • Liu C, Reppert SM (2000) GABA synchronizes clock cells within the suprachiasmatic circadian clock. Neuron 25:123–128

    PubMed  Article  CAS  Google Scholar 

  • Liu Y, Wang RB, Zhang ZK, Jiao XF (2010) Analysis on stability of neural network in the presence of inhibitory neurons. Cogn Neurodyn 4(1):61–68

    PubMed  Article  Google Scholar 

  • Matsuura H, Tateno K, Aou S (2008) Dynamical properties of the two-process model for sleep-wake cycles in infantile autism. Cogn Neurodyn 2(3):221–228

    PubMed  Article  Google Scholar 

  • Maywood ES, Reddy AB, Wong GKY, ONeill JS, OBrien JA, McMahon DG, Harmar AJ, Okamura H, Hastings MH (2006) Synchronization and maintenance of timekeeping in suprachiasmatic circadian clock cells by neuropeptidergic signaling. Curr Biol 16:599–605

    PubMed  Article  CAS  Google Scholar 

  • Moore RY, Speh JC, Leak RK (2002) Suprachiasmatic nucleus organization. Cell Tissue Res 309:89–98

    PubMed  Article  CAS  Google Scholar 

  • Reppert S, Weaver D (2001) Molecular analysis of mammalian circadian rhythms. Annu Rev Physiol 63:647–676

    Google Scholar 

  • Reppert S, Weaver D (2002) Coordination of circadian timing in mammals. Nature 418:935–941

    PubMed  Article  CAS  Google Scholar 

  • Rougemont J, Naef F (2006) Collective synchronization in populations of globally coupled phase oscillators with drifting frequencies. Phys Rev E 73:011104(5)

    Article  Google Scholar 

  • Shirakawa T, Honma S, Katsuno Y, Oguchi H, Honma K (2001) Multiple oscillators in the suprachiasmatic nucleus. Chronobiol Int 18:371–387

    PubMed  Article  CAS  Google Scholar 

  • To TL, Henson MA, Herzog ED, Doyle FJ III (2007) A molecular model for intercellular synchronization in the mammalian circadian clock. Biophys J 92:3792–3803

    PubMed  Article  CAS  Google Scholar 

  • Ullner E, Buceta J, Díez-Noguera A, García-Ojalvo J (2009) Noise-Induced coherence in multicellular circadian clocks. Biophys J 96:3573–3581

    PubMed  Article  CAS  Google Scholar 

  • Vasalou C, Herzog ED, Henson MA (2009) Small-world network models of intercellular coupling predict enhanced synchronization in the suprachiasmatic nucleus. J Biol Rhythms 24(3):243–54

    PubMed  Article  Google Scholar 

  • Vasalou C, Henson MA (2011) A multicellular model for differential regulation of circadian signals in the core and shell regions of the suprachiasmatic nucleus. J Theor Biol 7(288):44–56

    Article  Google Scholar 

  • Wang RB, Zhang ZK, Qu JY, Cao JT (2011) Phase synchronization motion and neural coding in dynamic transmission of neural information. IEEE Trans Neural Netw 22(7):1097–1106

    Article  Google Scholar 

  • Wang RB, Zhang ZK, Tseb CK, Qu JY, Cao JT (2011b) Neuralcoding in networks of multi-populations of neuraloscillators. Math Comput Simul doi:10.1016/j.matcom.2010.10.029

  • 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

    PubMed  Article  CAS  Google Scholar 

  • Yamaguchi S, Isejima H, Matsuo T, Okura R, Yagita K, Kobayashi M, Okamura H (2003) Synchronization of cellular clocks in the suprachiasmatic nucleus. Science 302:1408–1412

    PubMed  Article  CAS  Google Scholar 

Download references

Acknowledgments

This research is supported by the NNSF of China (Grant No: 11102106 and 11172158).

Author information

Affiliations

  1. College of Information Technology, Shanghai Ocean University, Shanghai, 201306, China

    Ying Li & Jinhuo Luo

  2. Institute of Systems Biology, Shanghai University, Shanghai, 200444, China

    Zengrong Liu

  3. College of Science and Information, Qingdao Agricultural University, Qingdao, 266109, Shandong, China

    Hui Wu

Authors
  1. Ying Li
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Zengrong Liu
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Jinhuo Luo
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Hui Wu
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Ying Li.

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Li, Y., Liu, Z., Luo, J. et al. Coupling-induced synchronization in multicellular circadian oscillators of mammals. Cogn Neurodyn 7, 59–65 (2013). https://doi.org/10.1007/s11571-012-9218-9

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11571-012-9218-9

Keywords

  • Circadian rhythm
  • Clock
  • Synchronization
  • Self-sustained oscillator