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 fashionâpresumably reflecting fluctuations in synaptic input6âand, 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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References
Abeles,M., Bergman,H., Margalit,E. & Vaadia,E. Spatiotemporal firing patterns in the frontal cortex of behaving monkeys. J. Neurophysiol. 70, 1629â1638 (1993).
Prut,Y. et al. Spatiotemporal structure of cortical activity: Properties and behavioral relevance. J. Neurophysiol. 79, 2857â2874 (1998).
Riehle,A., Grün,S., Diesmann,M. & Aertsen,A. Spike synchronization and rate modulation differentially involved in motor cortical function. Science 278, 1950â1953 (1997).
Mainen,Z. F. & Sejnowski,T. J. Reliability of spike timing in neocortical neurons. Science 268, 1503â1506 (1995).
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, 487â501 (1997).
Calvin,W. H. & Stevens,C. F. Synaptic noise and other sources of randomness in motoneuron interspike intervals. J. Neurophysiol. 31, 574â587 (1968).
Shadlen,M. N. & Newsome,W. T. Noise, neural codes and cortical organization. Curr. Opin. Neurobiol. 4, 569â579 (1994).
Shadlen,M. N. & Newsome,W. T. The variable discharge of cortical neurons: Implications for connectivity, computation, and information coding. J. Neurosci. 18, 3870â3896 (1998).
König,P., Engel,A. K. & Singer,W. Integrator or coincidence detector? The role of the cortical neuron revisited. Trends Neurosci. 19, 130â137 (1996).
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, 735â740 (1997).
Diesmann,M., Gewaltig,M.-O. & Aertsen,A. in Computational NeuroscienceâTrends in Research 1995 (ed. Bower, J.) 59â64 (Academic, San Diego, 1996).
Diesmann,M., Gewaltig,M.-O. & Aertsen,A. in From Membrane to Mind (eds Elsner, N. & Wässle, H.) 62 (Thieme, Stuttgart, 1997).
Gerstein,G. L. & Mandelbrot,B. Random walk models for the spike activity of a single neuron. Biophys. J. 4, 41â68 (1964).
Tuckwell,H. C. Introduction to Theoretical Neurobiology (Cambridge Univ. Press, Cambridge, 1988).
Perkel,D. H., Gerstein,G. L. & Moore,G. P. Neuronal spike trains and stochastic point processes. II. Simultaneous spike trains. Biophys. J. 7, 419â440 (1967).
Griffith,J. S. On the stability of brain-like structures. Biophys. J. 3, 299â308 (1963).
Abeles,M. Corticonics (Cambridge Univ. Press, Cambridge, 1991).
Abeles,M. Role of cortical neuron: integrator or coincidence detector? Isr. J. Med. Sci. 18, 83â92 (1982).
Bernander,O., Koch,C. & Usher,M. The effect of synchronized inputs at the single neuron level. Neural Comp. 6, 622â641 (1994).
Murthy,V. N. & Fetz,E. E. Effects of input synchrony on the firing rate of a three-conductance cortical neuron model. Neural Comp. 6, 1111â1126 (1994).
Arieli,A., Sterkin,A., Grinvald,A. & Aertsen,A. Dynamics of ongoing activity: explanation of the large variability in evoked cortical responses. Science 273, 1868â1871 (1996).
Hopfield,J. J. Neural networks and physical systems with emergent collective computational abilities. Proc. Natl Acad. Sci. USA 79, 2554â2558 (1982).
Bienenstock,E. A model of neocortex. Network 6, 179â224 (1995).
Herrmann,M., Hertz,J. A. & Prügel-Bennett,A. Analysis of synfire chains. Network 6, 403â414 (1995).
Arnoldi,H.-M. R. & Brauer,W. Synchronization without oscillatory neurons. Biol. Cybern. 74, 209â223 (1996).
Braitenberg,V. & Schüz,A. Anatomy of the Cortex (Springer, Berlin, 1991).
Fetz,E., Toyama,K. & Smith,W. in Cerebral Cortex Vol. 9 (eds Peters, A. & Jones, E. G.) 1â47 (Plenum, New York, 1991).
van Vreeswijk,C. & Sompolinsky,H. Chaos in neuronal networks with balanced excitatory and inhibitory activity. Science 274, 1724â1726 (1996).
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).
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, 2072â2093 (1995).
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 GermanâIsraeli Foundation for Scientific Research and Development, and Human Frontier Science Program..
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Diesmann, M., Gewaltig, MO. & Aertsen, A. Stable propagation of synchronous spiking in cortical neural networks. Nature 402, 529â533 (1999). https://doi.org/10.1038/990101
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DOI: https://doi.org/10.1038/990101
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