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Stable propagation of synchronous spiking in cortical neural networks

Abstract

The classical view of neural coding has emphasized the importance of information carried by the rate at which neurons discharge action potentials. More recent proposals that information may be carried by precise spike timing1,2,3,4,5 have been challenged by the assumption that these neurons operate in a noisy fashion—presumably reflecting fluctuations in synaptic input6—and, thus, incapable of transmitting signals with millisecond fidelity. Here we show that precisely synchronized action potentials can propagate within a model of cortical network activity that recapitulates many of the features of biological systems. An attractor, yielding a stable spiking precision in the (sub)millisecond range, governs the dynamics of synchronization. Our results indicate that a combinatorial neural code, based on rapid associations of groups of neurons co-ordinating their activity at the single spike level, is possible within a cortical-like network.

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Figure 1: Propagation of synchronous spiking in cortical networks.
Figure 2: Neural transmission function for pulse-packet input.
Figure 3: State-space analysis of propagating spike synchrony.
Figure 4: Dependence of the spike synchrony state space on the size of the neuron groups.

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References

  1. Abeles,M., Bergman,H., Margalit,E. & Vaadia,E. Spatiotemporal firing patterns in the frontal cortex of behaving monkeys. J. Neurophysiol. 70, 1629–1638 (1993).

    Article  CAS  Google Scholar 

  2. Prut,Y. et al. Spatiotemporal structure of cortical activity: Properties and behavioral relevance. J. Neurophysiol. 79, 2857–2874 (1998).

    Article  CAS  Google Scholar 

  3. Riehle,A., Grün,S., Diesmann,M. & Aertsen,A. Spike synchronization and rate modulation differentially involved in motor cortical function. Science 278, 1950–1953 (1997).

    Article  ADS  CAS  Google Scholar 

  4. Mainen,Z. F. & Sejnowski,T. J. Reliability of spike timing in neocortical neurons. Science 268, 1503–1506 (1995).

    Article  ADS  CAS  Google Scholar 

  5. Nowak,L. G., Sanchez-Vives,M. V. & McCormick,D. A. Influence of low and high frequency inputs on spike timing in visual cortical neurons. Cereb. Cortex 7, 487–501 (1997).

    Article  CAS  Google Scholar 

  6. Calvin,W. H. & Stevens,C. F. Synaptic noise and other sources of randomness in motoneuron interspike intervals. J. Neurophysiol. 31, 574–587 (1968).

    Article  CAS  Google Scholar 

  7. Shadlen,M. N. & Newsome,W. T. Noise, neural codes and cortical organization. Curr. Opin. Neurobiol. 4, 569–579 (1994).

    Article  CAS  Google Scholar 

  8. Shadlen,M. N. & Newsome,W. T. The variable discharge of cortical neurons: Implications for connectivity, computation, and information coding. J. Neurosci. 18, 3870–3896 (1998).

    Article  CAS  Google Scholar 

  9. König,P., Engel,A. K. & Singer,W. Integrator or coincidence detector? The role of the cortical neuron revisited. Trends Neurosci. 19, 130–137 (1996).

    Article  Google Scholar 

  10. Marsalek,P., Koch,C. & Maunsell,J. On the relationship between synaptic input and spike output jitter in individual neurons. Proc. Natl Acad. Sci. USA 94, 735–740 (1997).

    Article  ADS  CAS  Google Scholar 

  11. Diesmann,M., Gewaltig,M.-O. & Aertsen,A. in Computational Neuroscience—Trends in Research 1995 (ed. Bower, J.) 59–64 (Academic, San Diego, 1996).

    Google Scholar 

  12. Diesmann,M., Gewaltig,M.-O. & Aertsen,A. in From Membrane to Mind (eds Elsner, N. & Wässle, H.) 62 (Thieme, Stuttgart, 1997).

    Google Scholar 

  13. Gerstein,G. L. & Mandelbrot,B. Random walk models for the spike activity of a single neuron. Biophys. J. 4, 41–68 (1964).

    Article  CAS  Google Scholar 

  14. Tuckwell,H. C. Introduction to Theoretical Neurobiology (Cambridge Univ. Press, Cambridge, 1988).

    Book  Google Scholar 

  15. Perkel,D. H., Gerstein,G. L. & Moore,G. P. Neuronal spike trains and stochastic point processes. II. Simultaneous spike trains. Biophys. J. 7, 419–440 (1967).

    Article  CAS  Google Scholar 

  16. Griffith,J. S. On the stability of brain-like structures. Biophys. J. 3, 299–308 (1963).

    Article  ADS  MathSciNet  CAS  Google Scholar 

  17. Abeles,M. Corticonics (Cambridge Univ. Press, Cambridge, 1991).

    Book  Google Scholar 

  18. Abeles,M. Role of cortical neuron: integrator or coincidence detector? Isr. J. Med. Sci. 18, 83–92 (1982).

    CAS  PubMed  Google Scholar 

  19. Bernander,O., Koch,C. & Usher,M. The effect of synchronized inputs at the single neuron level. Neural Comp. 6, 622–641 (1994).

    Article  Google Scholar 

  20. Murthy,V. N. & Fetz,E. E. Effects of input synchrony on the firing rate of a three-conductance cortical neuron model. Neural Comp. 6, 1111–1126 (1994).

    Article  Google Scholar 

  21. Arieli,A., Sterkin,A., Grinvald,A. & Aertsen,A. Dynamics of ongoing activity: explanation of the large variability in evoked cortical responses. Science 273, 1868–1871 (1996).

    Article  ADS  CAS  Google Scholar 

  22. Hopfield,J. J. Neural networks and physical systems with emergent collective computational abilities. Proc. Natl Acad. Sci. USA 79, 2554–2558 (1982).

    Article  ADS  MathSciNet  CAS  Google Scholar 

  23. Bienenstock,E. A model of neocortex. Network 6, 179–224 (1995).

    Article  Google Scholar 

  24. Herrmann,M., Hertz,J. A. & Prügel-Bennett,A. Analysis of synfire chains. Network 6, 403–414 (1995).

    Article  Google Scholar 

  25. Arnoldi,H.-M. R. & Brauer,W. Synchronization without oscillatory neurons. Biol. Cybern. 74, 209–223 (1996).

    Article  CAS  Google Scholar 

  26. Braitenberg,V. & Schüz,A. Anatomy of the Cortex (Springer, Berlin, 1991).

    Book  Google Scholar 

  27. Fetz,E., Toyama,K. & Smith,W. in Cerebral Cortex Vol. 9 (eds Peters, A. & Jones, E. G.) 1–47 (Plenum, New York, 1991).

    Google Scholar 

  28. van Vreeswijk,C. & Sompolinsky,H. Chaos in neuronal networks with balanced excitatory and inhibitory activity. Science 274, 1724–1726 (1996).

    Article  ADS  CAS  Google Scholar 

  29. Diesmann,M., Gewaltig,M.-O. & Aertsen,A. SYNOD: An Environment for Neural Systems Simulations Technical report GC-AA/95-3 (The Weizmann Institute of Science, Rohovot, Israel, 1995). (http://www.synod.uni-freiburg.de).

    Google Scholar 

  30. Arieli,A., Shoham,D., Hildesheim,R. & Grinvald,A. Coherent spatiotemporal patterns of ongoing activity revealed by real-time optical imaging coupled with single-unit recording in the cat visual cortex. J. Neurophysiol. 73, 2072–2093 (1995).

    Article  CAS  Google Scholar 

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Acknowledgements

We thank M. Abeles, E. Bienenstock, S. Grün, I. Nelken, A. Riehle, S. Rotter and C. von der Malsburg for their constructive comments. Supported in part by grants for the Deutsche Forschungsgemeinschaft, the German–Israeli Foundation for Scientific Research and Development, and Human Frontier Science Program..

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Correspondence to Ad Aertsen.

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Diesmann, M., Gewaltig, MO. & Aertsen, A. Stable propagation of synchronous spiking in cortical neural networks. Nature 402, 529–533 (1999). https://doi.org/10.1038/990101

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