Abstract

A simple model for synchronous firing of biological oscillators based on Peskin’s model of the cardiac pacemaker [Mathematical aspects of heart physiology, Courant Institute of Mathematical Sciences, New York University, New York, 1975, pp. 268–278] is studied. The model consists of a population of identical integrate-and-fire oscillators. The coupling between oscillators is pulsatile: when a given oscillator fires, it pulls the others up by a fixed amount, or brings them to the firing threshold, whichever is less.
The main result is that for almost all initial conditions, the population evolves to a state in which all the oscillators are firing synchronously. The relationship between the model and real communities of biological oscillators is discussed; examples include populations of synchronously flashing fireflies, crickets that chirp in unison, electrically synchronous pacemaker cells, and groups of women whose menstrual cycles become mutually synchronized.

MSC codes

  1. 92A09
  2. 34C15
  3. 58F40

Keywords

  1. synchronization
  2. biological oscillators
  3. pacemaker
  4. integrate-and-fire

Get full access to this article

View all available purchase options and get full access to this article.

References

1.
J. C. Alexander, Patterns at primary Hopf bifurcations of a plexus of identical oscillators, SIAM J. Appl. Math., 46 (1986), 199–221
2.
Preben Alstrøm, Bo Christiansen, Mogens T. Levinsen, Nonchaotic transition from quasiperiodicity to complete phase locking, Phys. Rev. Lett., 61 (1988), 1679–1682
3.
Anonymous, Olfactory synchrony of menstrual cycles, Science News, 112 (1977), 5–
4.
Jacques Bélair, Periodic pulsatile stimulation of a nonlinear oscillator, J. Math. Biol., 24 (1986), 217–232
5.
J. Buck, Synchronous rhythmic flashing of fireflies. II, Quart. Rev. Biol., 63 (1988), 265–289
6.
J. Buck, E. Buck, Synchronous fireflies, Scientific American, 234 (1976), 74–85
7.
Avis H. Cohen, Philip J. Holmes, Richard H. Rand, The nature of the coupling between segmental oscillators of the lamprey spinal generator for locomotion: a mathematical model, J. Math. Biol., 13 (1981/82), 345–369
8.
H. Daido, Lower critical dimension for populations of oscillators with randomly distributed frequencies: A renormalization-group analysis, Phys. Rev. Lett., 61 (1988), 231–234
9.
J. T. Enright, Temporal precision in circadian systems: a reliable neuronal clock from unreliable components?, Science, 209 (1980), 1542–1545
10.
G. Bard Ermentrout, Synchronization in a pool of mutually coupled oscillators with random frequencies, J. Math. Biol., 22 (1985), 1–9
11.
G. B. Ermentrout, The behavior of rings of coupled oscillators, J. Math. Biol., 23 (1985), 55–74
12.
George Bard Ermentrout, Nancy Kopell, Frequency plateaus in a chain of weakly coupled oscillators. I, SIAM J. Math. Anal., 15 (1984), 215–237
13.
G. B. Ermentrout, N. Kopell, Oscillator death in systems of coupled neural oscillators, SIAM J. Appl. Math., 50 (1990), 125–146
14.
G. Bard Ermentrout, John Rinzel, Waves in a simple, excitable or oscillatory, reaction-diffusion model, J. Math. Biol., 11 (1981), 269–294
15.
G. B. Ermentrout, J. Rinzel, Beyond a pacemaker's entrainment limit: phase walk-through, Amer. J. Physiol., 246 (1984), R102–R106
16.
G. B. Ermentrout, W. C. Troy, Phaselocking in a reaction-diffusion system with a linear frequency gradient, SIAM J. Appl. Math., 46 (1986), 359–367
17.
Leon Glass, Michael C. Mackey, A simple model for phase locking of biological oscillators, J. Math. Biol., 7 (1979), 339–352
18.
Leon Glass, Michael C. Mackey, From clocks to chaos, Princeton University Press, Princeton, NJ, 1988xviii+248
19.
J. Grasman, M. J. W. Jansen, Mutually synchronized relation oscillators as prototypes of oscillating systems in biology, J. Math. Biol., 7 (1979), 171–197
20.
F. E. Hanson, Comparative studies of firefly pacemakers, Fed. Proc., 37 (1978), 2158–2164
21.
J. Honerkamp, The heart as a system of coupled nonlinear oscillators, J. Math. Biol., 18 (1983), 69–88
22.
N. Ikeda, S. Yoshizawa, T. Sato, Difference equation model of ventricular parasystole as an interaction between cardiac pacemakers based on the phase reponse curve, J. Theoret. Biol., 103 (1983), 439–465
23.
J. Jalife, Mutual entrainment and electrical coupling as mechanisms for synchronous firing of rabbit sinoatrial pacemaker cells, J. Physiol., 356 (1984), 221–243
24.
J. P. Keener, F. C. Hoppensteadt, J. Rinzel, Integrate-and-fire models of nerve membrane response to oscillatory input, SIAM J. Appl. Math., 41 (1981), 503–517
25.
B. W. Knight, Dynamics of encoding in a population of neurons, J. Gen. Physiol., 59 (1972), 734–766
26.
N. Kopell, A. H. Cohen, S. Rossignol, S. Grillner, Toward a theory of modelling central pattern generatorsNeural Control of Rhythmic Movement in Vertebrates, John Wiley, New York, 1988, 369–413
27.
N. Kopell, G. B. Ermentrout, Symmetry and phaselocking in chains of weakly coupled oscillators, Comm. Pure Appl. Math., 39 (1986), 623–660
28.
N. Kopell, L. N. Howard, Plane wave solutions to reaction-diffusion equations, Studies in Appl. Mat., 52 (1973), 291–328
29.
Yoshiki Kuramoto, Ikuko Nishikawa, Statistical macrodynamics of large dynamical systems. Case of a phase transition in oscillator communities, J. Statist. Phys., 49 (1987), 569–605
30.
M. K. McClintock, Menstrual synchrony and suppression, Nature, 229 (1971), 244–245
31.
D. C. Michaels, E. P. Matyas, J. Jalife, Mechanisms of sinoatrial pacemaker synchronization: a new hypothesis, Circulation Res., 61 (1987), 704–714
32.
Hans G. Othmer, I. Rensing, N. I. Jaeger, Synchronization, phase-locking and other phenomena in coupled cellsTemporal order (Bremen, 1984), Springer Ser. Synergetics, Vol. 29, Springer, Berlin, 1985, 130–143
33.
T. Pavlidis, Biological Oscillators: Their Mathematical Analysis, Academic Press, New York, 1973
34.
Charles S. Peskin, Mathematical aspects of heart physiology, Courant Institute of Mathematical Sciences New York University, New York, 1975, 268–278
35.
M. J. Russell, G. M. Switz, K. Thompson, Olfactory influences on the human menstrual cycle, Pharmacol. Biochem. Behav., 13 (1980), 737–738
36.
H. Sakaguchi, S. Shinomoto, Y. Kuramoto, Local and global self entrainments in oscillator lattices, Progr. Theoret. Phys., 77 (1987), 1005–1010
37.
H. Sakaguchi, S. Shinomoto, Y. Kuramoto, Mutual entrainment in oscillator lattices with nonvariational type interaction, Progr. Theoret. Phys., 79 (1988), 1069–1079
38.
A. Sherman, J. Rinzel, Collective properties of insulin secreting cells, preprint
39.
A. Sherman, J. Rinzel, J. Keizer, Emergence of organized bursting in clusters of pancreatic beta-cells by channel sharing, Biophys. J., 54 (1988), 411–425
40.
H. M. Smith, Synchronous flashing of fireflies, Science, 82 (1935), 151–
41.
Steven H. Strogatz, Charles M. Marcus, Robert M. Westervelt, Renato E. Mirollo, Collective dynamics of coupled oscillators with random pinning, Phys. D, 36 (1989), 23–50
42.
Steven H. Strogatz, Renato E. Mirollo, Phase-locking and critical phenomena in lattices of coupled nonlinear oscillators with random intrinsic frequencies, Phys. D, 31 (1988), 143–168
43.
Steven H. Strogatz, Renato E. Mirollo, Collective synchronisation in lattices of nonlinear oscillators with randomness, J. Phys. A, 21 (1988), L699–L705
44.
Vincent Torre, A theory of synchronization of heart pace-maker cells, J. Theoret. Biol., 61 (1976), 55–71
45.
R. D. Traub, R. Miles, R. K. S. Wong, Model of the origin of rhythmic population oscillations in the hippocampal slice, Science, 243 (1989), 1319–1325
46.
T. J. Walker, Acoustic synchrony: two mechanisms in the snowy tree cricket, Science, 166 (1969), 891–894
47.
A. T. Winfree, Biological rhythms and the behavior of populations of coupled oscillators, J. Theoret. Biol., 16 (1967), 15–42
48.
Arthur T. Winfree, The geometry of biological time, Biomathematics, Vol. 8, Springer-Verlag, Berlin, 1980xiv+530
49.
A. T. Winfree, The Timing of Biological Clocks, Scientific American Press, New York, 1987
50.
Arthur T. Winfree, When time breaks down, Princeton University Press, Princeton, NJ, 1987xiv+340, The Three-Dimensional Dynamics of Electrochemical Waves and Cardiac Arrhythmias
51.
A. T. Winfree, S. H. Strogatz, Organizing centers for three-dimensional chemical waves, Nature, 311 (1984), 611–615

Information & Authors

Information

Published In

cover image SIAM Journal on Applied Mathematics
SIAM Journal on Applied Mathematics
Pages: 1645 - 1662
ISSN (online): 1095-712X

History

Submitted: 3 August 1989
Accepted: 15 December 1989
Published online: 10 July 2006

MSC codes

  1. 92A09
  2. 34C15
  3. 58F40

Keywords

  1. synchronization
  2. biological oscillators
  3. pacemaker
  4. integrate-and-fire

Authors

Affiliations

Metrics & Citations

Metrics

Citations

If you have the appropriate software installed, you can download article citation data to the citation manager of your choice. Simply select your manager software from the list below and click Download.

Cited By

Media

Figures

Other

Tables

Share

Share

Copy the content Link

Share with email

Email a colleague

Share on social media

The SIAM Publications Library now uses SIAM Single Sign-On for individuals. If you do not have existing SIAM credentials, create your SIAM account https://my.siam.org.