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The evidence for neural information processing with precise spike-times: A survey

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Abstract

This paper surveys recent findings in neuroscience regarding the behavioral relevancy of the precise timing with which real spiking neurons emit spikes. The literature suggests that in almost any system where the processing-speed of a neural (sub)-system is required to be high, the timing of single spikes can be very precise and reliable. Additionally, new, more refined methods are finding precisely timed spikes where previously none where found. This line of evidence thus provides additional motivation for researching the computational properties of networks of artificial spiking neurons that compute with more precisely timed spikes.

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References

  • AgmonSnir H, Carr C and Rinzel J (1998) The role of dendrites in auditory coincidence detection. Nature 393: 268–272

    Article  Google Scholar 

  • Bair W and Koch C (1996) Temporal precision of spike trains in extrastriate cortex of the behaving macaque monkey. Neural Computation 8(6): 1185–1202

    Google Scholar 

  • Beierholm U, Nielsen C, Ryge J, Alstrom P and Kiehn O (2001) Characterization of reliability of spike timing in spinal interneurons during oscillating inputs. J. Neurophysiol. 86: 1858–1868

    Google Scholar 

  • Bell C, Han V, Sugawara Y and Grant K (1997) Synaptic plasticity in a cerebellum-like structure depends on temporal order. Nature 387: 278–281

    Article  Google Scholar 

  • Bi B-q and Poo M-m (1999) Distributed synaptic modification in neural networks induced by patterned stimulation. Nature 401: 792–716

    Article  Google Scholar 

  • Bi G-q and Poo M-m (1998) Synaptic modifications in cultured hippocampal neurons: Dependence on spike timing, synaptic strength, and postsynaptic cell type. J. Neurosci. 18(24): 10464–10472

    Google Scholar 

  • Bi G-q and Poo M-m (2001) Synaptic modification by correlated activity: Hebb's postulate revisited. Annu. Rev. Neurosci. 24: 139–166

    Article  Google Scholar 

  • Bialek W, Rieke F, Steveninck R de Ruyter van and Warland D (1991) Reading a neural code. Science 252: 1854–1857

    Google Scholar 

  • Bohte SM, Kok JN and La Poutré H (2002a) Spike-prop: error-backpropagation in multi-layer networks of spiking neurons. Neurocomputing 48(1–4): 17–37

    Article  MATH  Google Scholar 

  • Bohte SM, Kok JN and La Poutré H (2002b) Unsupervised classification in a layered RBF network of spiking neurons. IEEE Trans. Neural Networks: 426–435

  • Brenner N, Strong SP, Koberle R, Bialek W and de Ruyter van Steveninck RR (2000) Synergy in a neural code. Neural Computation 12(7): 1531–1552

    Article  Google Scholar 

  • Buracas G, Zador A, DeWeese M and Albright T (1998) Efficient discrimination of temporal patterns by motion-sensitive neurons in primate visual cortex. Neuron 20: 959–969

    Article  Google Scholar 

  • Carr C and Konishi M (1990) A circuit for detection of interaural time differences in the brain stem of the barn owl. J. Neurosci. 10: 3227–3246

    Google Scholar 

  • Chechik G (2003) Spike-timing-dependent-plasticity and relevant mutual information maximization. Neural Computation 15: 1481–1510

    Article  MATH  Google Scholar 

  • Dayan P, Hausser M and London M (2003) Plasticity kernels and temporal statistics. In: Nips 2002 (Vol. 15). The MIT Press (to appear)

  • de Ruyter van Steveninck R, Borst A and Bialek W (2001) Real-time encoding of motion: answerable questions and questionable answers from the fly's visual system. In: Zanker J and Zeil J (eds) Motion Vision — Computational, Neural, and Ecological Constraints. Springer Verlag, Berlin Heidelberg New York

    Google Scholar 

  • de Ryter van Steveninck R, Lewen G, Strong S, Koberle R and Bialek W (1997) Reproducibility and variability in neural spike trains. Science 275: 1805–1808

    Article  Google Scholar 

  • deCharms R and Merzenich M (1996) Primary cortical representation of sounds by the coordination of action-potential timing. Nature 381: 610–613

    Article  Google Scholar 

  • Delorme A, Gautrais J, VanRullen R and Thorpe S (1999) Spikenet: A simulator for modeling large networks of integrate and fire neurons. Neurocomputing: 989–996

  • DeWeese M and Zador A (2002) Binary coding in auditory cortex. In: Advances in Neural Information Processing Systems (Vol. 15). The MIT Press

  • Eisele M and Miller K (2003) Hidden markov model of cortical synaptic plasticity: Derivation of the learning rule. In: Nips 2002 (Vol. 15). The MIT Press (to appear)

  • Fairhall A, Lewen G, Bialek W and de Ruyter van Steveninck R (2001) Efficiency and ambiguity in an adaptive neural code. Nature 412: 787–792

    Article  Google Scholar 

  • Feldman D, Nicoll R, Malenka R and Isaac J (1998) Long-term depression at thalamocortical synapses in developing somatosensory cortex. Neuron 21: 347–357

    Article  Google Scholar 

  • Fellous J-M, Houweling A, Modi R, Rao R, Tiesinga P and Sejnowski T (2001) Frequency dependence of spike timing reliability in cortical pyramidal cells and interneurons. J. Neurophysiol. 85: 1782–1787

    Google Scholar 

  • Gerstner W (1998) Spiking neurons. In: Maass W and Bishop CM (eds) Pulsed Neural Networks, pp. 3–55. The MIT Press.

  • Gerstner W (2000) Population dynamics of spiking neurons: Fast transients, asynchronous states, and locking. Neural Computation 12(1): 43–89

    Article  Google Scholar 

  • Gerstner W, Kempter R, Hemmen J van and Wagner H (1996) A neuronal learning rule for sub-millisecond temporal coding. Nature 383: 76–78

    Article  Google Scholar 

  • Gray C (1999) The temporal correlation hypothesis of visual feature integration: Still alive and well. Neuron 24: 31–47

    Article  Google Scholar 

  • Gray C, König P, Engel A and Singer W (1989) Oscillatory responses in cat visual cortex exhibit inter-columnar synchronization which reflects global stimulus properties. Nature 338: 334–337

    Article  Google Scholar 

  • Harris K, Henze D, Hirase H, Leinekugel X, Dragoi G, Czurkó A and Buzsáki (2002) Spike train dynamics predicts theta-related phase precession in hippocampel pyramidal cells. Nature 417: 738–741

    Article  Google Scholar 

  • Heiligenberg W (1991) Neural Nets in Electric Fish. MIT Press.

  • Hopfield J (1995) Pattern recognition computation using action potential timing for stimulus representation. Nature 376: 33–36

    Article  Google Scholar 

  • Hopfield J and Brody C (2000) What is a moment? transient synchrony as a collective mechanism for spatiotemporal integration. Proc. Natl. Acad. Sci. USA 97: 13919–13924

    Article  Google Scholar 

  • Izhikevich E, Deai N, Walcott E and Hoppensteadt F (2003) Bursts as a unit of neural information: selective communication via resonance. Trends Neurosci. 26(3): 161–167

    Article  Google Scholar 

  • Johansson R and Birznieks I (2004) Fist spikes in ensembles of human tactile afferents code complex spatial fingertip events. Nature Neurosci. 7(2): 170–177

    Article  Google Scholar 

  • Kandel E, Schwartz J and Jessell T (eds) (1991) Principles of Neural Science (third ed.). Elsevier/North-Holland, Amsterdam, London, New York

    Google Scholar 

  • Kepecs A, van Rossum M, Song S and Tegner J (2002) Spike-timing plasticity: common themes and divergent vistas. Biol. Cybern. 87: 446–458

    Article  MATH  Google Scholar 

  • Kuwabara N and Suga N (1993) Delay lines and amplitude selectivity are created in subthalamic auditory nuclei: the branchium of the inferior colliculus of the mustached bat. J. Neurophysiol. 69: 1713–1724

    Google Scholar 

  • Laurent G (1999) A systems perspective on early olfactory coding. Science 286: 723–728

    Article  Google Scholar 

  • Laurent G, Wehr M and Davidowitz H (1996) Temporal representations of odors in an olfactory network. J. Neurosci. 16(12): 3837–3847

    Google Scholar 

  • Lewen G, Bialek W. and de Ruyter van Steveninck R (2001) Neural coding of naturalistic motion stimuli. Network: Comput. Neural Syst. 12: 317–329

    Article  Google Scholar 

  • Liu R, Tzonev S, Rebrik S and Miller K (1997) The structure and precision of retinal spike trains. Proc. Nat. Acad. Sc. USA 94: 5411–5416

    Article  Google Scholar 

  • Liu R, Tzonev S, Rebrik S and Miller K (2001) Variability and information in a neural code of the cat lateral geniculate nucleus. J. Neurophys. 86: 2789–2806

    Google Scholar 

  • Maass W (1997a) Fast sigmoidal networks via spiking neurons. Neural Computation 9(2): 275–304

    Google Scholar 

  • Maass W (1997b) Networks of spiking neurons: The third generation of neural network models. Neural Networks 10(9): 1659–1671

    Article  Google Scholar 

  • Mainen Z and Sejnowski T (1995) Reliability of spike timing in neocortical neurons. Science 268(5216): 1503–1506

    Google Scholar 

  • Markram H, Lübke J, Frotscher M and Sakmann B (1997) Regulation of synaptic efficacy by coincidence of postsynaptic aps and epsps. Nature 375: 213–215

    Google Scholar 

  • Mehta M, Lee A and Wilson M (2002) Role of experience and oscillations in transforming a rate code into a temporal code. Nature 417: 741–746

    Article  Google Scholar 

  • O'Keefe J and Recce M (1993) Phase relationship between hippocampal place units and the EEG theta rhythm. Hippocampus 3: 317–330

    Article  Google Scholar 

  • Oram M, Xiao D, Dritschel B and Payne K (2002) The temporal resolution of neural codes: does response latency have a unique role? Phil. Trans. R. Soc. Lond. B 357: 987–1001

    Article  Google Scholar 

  • Reich D, Mechler F and Victor J (2001) Independent and redundant information in nearby cortical neurons. Science 294: 2566–2568

    Article  Google Scholar 

  • Reinagel P and Reid R (2000) Temporal coding of visual information in the thalamus. J. Neurosci. 20(14): 5392–5400

    Google Scholar 

  • Shadlen M. and Movshon J (1999) Synchrony unbound: A critical evaluation of the temporal binding hypothesis. Neuron 24: 67–77

    Article  Google Scholar 

  • Shadlen M and Newsome W (1994) Noise, neural codes and cortical organization. Curr. Opin. Neurobiol. 4: 569–579

    Article  Google Scholar 

  • Shadlen M and Newsome W (1995) Is there a signal in the noise? Curr. Opin. Neurobiol. 5: 248–250

    Article  Google Scholar 

  • Shadlen M and Newsome W (1998) The variable discharge of cortical neurons: implications for connectivity, computation and information coding. J. Neuronsci 18: 3870–3896

    Google Scholar 

  • Singer W (1999) Neuronal synchrony: A versatile code for the definition of relations. Neuron 24: 49–65

    Article  Google Scholar 

  • Softky W (1995) Simple codes versus efficient codes. Curr. Opin. Neurobiol. 5: 239–247

    Article  Google Scholar 

  • Softky W and Koch C (1993) The highly irregular firing of cortical cells is inconsistent with temporal integration of random epsp's. J. Neurosci. 13: 334–350

    Google Scholar 

  • Stopfer M and Laurent G (1999) Short-term memory in olfactory network dynamics. Nature 402: 610–614

    Article  Google Scholar 

  • Stratford K, Tarczy-Hornoch K, Martin K, Bannister N and Jack J (1996) Excitatory synaptic inputs to spiny stellate cells in cat visual cortex. Nature 382: 258–261

    Article  Google Scholar 

  • Thorpe S, Fize F and Marlot C (1996) Speed of processing in the human visual system. Nature 381: 520–522

    Article  Google Scholar 

  • von der Malsburg C (1981) The correlation theory of brain function. Internal Report 81-2, Max-Planck-Institute for Biophysical Chemistry, Göttingen, Germany

    Google Scholar 

  • Williams S and Stuart G (2002) Dependence of epsp efficacy on synapse location in neocortical pyramidal neurons. Science 295: 1907–1910

    Article  Google Scholar 

  • Zhang L, Tao H, Holt C, Harris W, Poo M (1998) A critical window for cooperation and competition among developing retinotectal synapses. Nature 395(3): 37–44

    Google Scholar 

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Bohte, S.M. The evidence for neural information processing with precise spike-times: A survey. Natural Computing 3, 195–206 (2004). https://doi.org/10.1023/B:NACO.0000027755.02868.60

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  • DOI: https://doi.org/10.1023/B:NACO.0000027755.02868.60

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