Skip to main content

The Phase Oscillator Approximation in Neuroscience: An Analytical Framework to Study Coherent Activity in Neural Networks

  • Chapter
  • First Online:

Part of the book series: Springer Series in Computational Neuroscience ((NEUROSCI,volume 2))

Abstract

One of the major challenges in neuroscience today is to understand how coherent activity emerges in neural networks from the interactions between their neurons, as well as its role in normal and pathological brain function. Probably the two most relevant examples of coherent activity in the brain are synchronization and phase-locking. The phase oscillator approximation used in physics and the mathematical models based thereon provide a powerful tool to investigate the biophysical mechanisms underlying these phenomena. In particular, the experimental or numerical determination of the phase–response curve, which derives from the intrinsic properties of a real or a simulated neuron, allows one to greatly simplify the analytical treatment of their dynamics, as well as their computational modeling. In this way, it is possible to predict the existence and stability of phase-locked states and of synchronized assemblies in real and simulated neural networks with electrical or chemical synapses. The phase–response curve also determines the stability of repetitive neuronal firing thereby affecting spike-time reliability and noise-induced synchronization. Moreover, for neurons that fire repetitively, the phase–response curve is directly related to the waveform of the input that most likely precedes an action potential, i.e., to the spike-triggered average, or optimal stimulus. Here, we discuss these phenomena with special emphasis on the implications for neural function.

This is a preview of subscription content, log in via an institution.

Buying options

Chapter
USD   29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD   89.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD   119.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD   169.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Learn about institutional subscriptions

References

  • Brody CD, Hopfield JJ (2003) Simple networks for spike-timing-based computation, with application to olfactory processing. Neuron 37:843–852.

    Article  PubMed  CAS  Google Scholar 

  • Brown E, Moehlis J, Holmes P (2004) On the phase reduction and response dynamics of neural oscillator populations. Neural Comput 16:673–715.

    Article  PubMed  Google Scholar 

  • Bryant HL, Segundo JP (1976) Spike initiation by transmembrane current: a white-noise analysis. J Physiol 260:279–314.

    PubMed  CAS  Google Scholar 

  • Canavier CC, Butera RJ, Dror RO, Baxter DA, Clark JW, Byrne JH (1997) Phase response characteristics of model neurons determine which patterns are expressed in a ring circuit model of gait generation. Biol Cybern 77:367–380.

    Article  PubMed  CAS  Google Scholar 

  • Engel AK, Singer W (2001) Temporal binding and the neural correlates of sensory awareness. Trends Cogn Sci 5:16–25.

    Article  PubMed  Google Scholar 

  • Ermentrout B (1996) Type I membranes, phase resetting curves, and synchrony. Neural Comput 8:979–1001.

    Article  PubMed  CAS  Google Scholar 

  • Ermentrout B (2002) Simulating, Analyzing, and Animating Dynamical Systems: A Guide to XPPAUT for Researchers and Students. Philadelphia: SIAM.

    Google Scholar 

  • Ermentrout GB, Galan RF, Urban NN (2007) Relating neural dynamics to neural coding. Phys Rev Lett 99:248103.

    Article  PubMed  Google Scholar 

  • Foffani G, Uzcategui YG, Gal B, Menendez de la PL (2007) Reduced spike-timing reliability correlates with the emergence of fast ripples in the rat epileptic hippocampus. Neuron 55: 930–941.

    Article  PubMed  CAS  Google Scholar 

  • Galán RF, Ermentrout GB, Urban NN (2005) Efficient estimation of phase-resetting curves in real neurons and its significance for neural-network modeling. Phys Rev Lett 94:158101.

    Article  PubMed  Google Scholar 

  • Galán RF, Ermentrout GB, Urban NN (2006) Predicting synchronized neural assemblies from experimentally estimated phase-resetting curves. Neurocomputing 69:1112–1115.

    Article  Google Scholar 

  • Galán RF, Ermentrout GB, Urban NN (2007a) Reliability and stochastic synchronization in type I vs. type II neural oscillators. Neurocomputing 70:2102–2106.

    Article  Google Scholar 

  • Galán RF, Ermentrout GB, Urban NN (2007b) Stochastic dynamics of uncoupled neural oscillators: Fokker-Planck studies with the finite element method. Phys Rev E Stat Nonlin Soft Matter Phys 76:056110.

    Article  PubMed  Google Scholar 

  • Galán RF, Ermentrout GB, Urban NN (2008) Optimal time scale for spike-time reliability: theory, simulations, and experiments. J Neurophysiol 99:277–283.

    Article  Google Scholar 

  • Galán RF, Sachse S, Galizia CG, Herz AVM (2004) Odor-driven attractor dynamics in the antennal lobe allow for simple and rapid olfactory pattern classification. Neural Comput 16:999–1012.

    Article  Google Scholar 

  • Goldobin DS, Pikovsky AS (2005) Synchronization of self-sustained oscillators by common white noise. Phys A – Stat Mech Appl 351:126–132.

    Article  Google Scholar 

  • Goldobin DS, Pikovsky A (2006) Antireliability of noise-driven neurons. Phys Rev E Stat Nonlin Soft Matter Phys 73:061906.

    Article  PubMed  Google Scholar 

  • Hodgkin AL, Huxley AF (1952) A quantitative description of membrane current and its application to conduction and excitation in nerve. J Physiol 117:500–544.

    PubMed  CAS  Google Scholar 

  • Hopfield JJ, Brody CD (2001) What is a moment? Transient synchrony as a collective mechanism for spatiotemporal integration. Proc Natl Acad Sci U S A 98:1282–1287.

    Article  PubMed  CAS  Google Scholar 

  • Hoppensteadt FC, Izhikevich EM (1997) Weakly Connected Neural Networks. New York: Springer-Verlag.

    Google Scholar 

  • Kupper R, Gewaltig MO, Korner U, Korner E (2005) Spike-latency codes and the effect of saccades. Neurocomputing 65:189–194.

    Article  Google Scholar 

  • Kuramoto Y (1984) Chemical Oscillations, Waves, and Turbulence. Berlin: Springer Verlag.

    Google Scholar 

  • Mainen ZF, Sejnowski TJ (1995) Reliability of spike timing in neocortical neurons. Science 268:1503–1506.

    Article  PubMed  CAS  Google Scholar 

  • Mancilla JG, Lewis TJ, Pinto DJ, Rinzel J, Connors BW (2007) Synchronization of electrically coupled pairs of inhibitory interneurons in neocortex. J Neurosci 27:2058–2073.

    Article  PubMed  CAS  Google Scholar 

  • Morison RS, Dempsey EW (1943) Mechanism of thalamocortical augmentation and repetition. Am J Physiol 138:0297–0308.

    Google Scholar 

  • Movshon JA (2000) Reliability of neuronal responses. Neuron 27:412–414.

    Article  PubMed  CAS  Google Scholar 

  • Netoff TI, Banks MI, Dorval AD, Acker CD, Haas JS, Kopell N, White JA (2005) Synchronization in hybrid neuronal networks of the hippocampal formation. J Neurophysiol 93:1197–1208.

    Article  PubMed  Google Scholar 

  • Oprisan SA, Canavier CC (2002) The influence of limit cycle topology on the phase resetting curve. Neural Comput 14:1027–1057.

    Article  PubMed  Google Scholar 

  • Oprisan SA, Prinz AA, Canavier CC (2004) Phase resetting and phase locking in hybrid circuits of one model and one biological neuron. Biophys J 87:2283–2298.

    Article  PubMed  CAS  Google Scholar 

  • Pérez Velázquez JL, Galán RF, Domínguez LG, Leshchenko Y, Lo S, Belkas J, Guevara Erra R (2007) Phase response curves in the characterization of epileptiform activity. Phys Rev E Stat Nonlin Soft Matter Phys 76:061912.

    Article  PubMed  Google Scholar 

  • Preyer AJ, Butera RJ (2005) Neuronal oscillators in aplysia californica that demonstrate weak coupling in vitro. Phys Rev Lett 95:138103.

    Article  PubMed  Google Scholar 

  • Rieke F, Warland D, de Ryuter van Stevenick R, Bialek W (1997) Spikes. Exploring the neural code. Cambridge, Mass: MIT Press.

    Google Scholar 

  • Rinzel J, Ermentrout B (1998) Analysis of neural excitability. In: Methods in Neuronal Modeling (Koch C, Segev I, eds), pp. 251–291. Cambridge, Mass: MIT Press.

    Google Scholar 

  • Schafer C, Rosenblum MG, Abel HH, Kurths J (1999) Synchronization in the human cardiorespiratory system. Phys Rev e 60:857–870.

    Article  CAS  Google Scholar 

  • Shadlen MN, Movshon JA (1999) Synchrony unbound: a critical evaluation of the temporal binding hypothesis. Neuron 24:67–25.

    Article  PubMed  CAS  Google Scholar 

  • Singer W, Gray CM (1995) Visual feature integration and the temporal correlation hypothesis. Annu Rev Neurosci 18:555–586.

    Article  PubMed  CAS  Google Scholar 

  • Spors H, Wachowiak M, Cohen LB, Friedrich RW (2006) Temporal dynamics and latency patterns of receptor neuron input to the olfactory bulb. J Neurosci 26:1247–1259.

    Article  PubMed  CAS  Google Scholar 

  • Tateno T, Robinson HP (2007) Phase resetting curves and oscillatory stability in interneurons of rat somatosensory cortex. Biophys J 92:683–695.

    Article  PubMed  CAS  Google Scholar 

  • Teramae J, Tanaka D (2004) Robustness of the noise-induced phase synchronization in a general class of limit cycle oscillators. Phys Rev Lett 93:204103.

    Article  PubMed  Google Scholar 

  • Tsubo Y, Takada M, Reyes AD, Fukai T (2007) Layer and frequency dependencies of phase response properties of pyramidal neurons in rat motor cortex. Euro J Neurosci 25:3429–3441.

    Article  Google Scholar 

  • Uhlhaas PJ, Singer W (2006) Neural synchrony in brain disorders: relevance for cognitive dysfunctions and pathophysiology. Neuron 52:155–168.

    Article  PubMed  CAS  Google Scholar 

  • Vida I, Bartos M, Jonas P (2006) Shunting inhibition improves robustness of gamma oscillations in hippocampal interneuron networks by homogenizing firing rates. Neuron 49:107–117.

    Article  PubMed  CAS  Google Scholar 

  • Winfree AT (2001) The Geometry of Biological Time. New York: Springer.

    Book  Google Scholar 

Download references

Acknowledgments

The author thanks Dr. Christopher G. Wilson for helpful comments. This work has been supported by the Mount Sinai Health Care Foundation and the Alfred P. Sloan Foundation.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Roberto F. Galán .

Editor information

Editors and Affiliations

Rights and permissions

Reprints and permissions

Copyright information

© 2009 Springer Science+Business Media, LLC

About this chapter

Cite this chapter

Galán, R.F. (2009). The Phase Oscillator Approximation in Neuroscience: An Analytical Framework to Study Coherent Activity in Neural Networks. In: Velazquez, J., Wennberg, R. (eds) Coordinated Activity in the Brain. Springer Series in Computational Neuroscience, vol 2. Springer, New York, NY. https://doi.org/10.1007/978-0-387-93797-7_4

Download citation

Publish with us

Policies and ethics