Finding the event structure of neuronal spike trains

Neurons in sensory systems convey information about physical stimuli in their spike trains. In vitro, single neurons respond precisely and reliably to the repeated injection of the same fluctuating current, producing regions of elevated firing rate, termed events. Analysis of these spike trains reveals that multiple distinct spike patterns can be identified as trial-to-trial correlations between spike times [1]. Finding events in data with realistic spiking statistics is challenging because events belonging to different spike patterns may overlap. We propose a method for finding spiking events that uses contextual information to disambiguate which pattern a trial belongs to. The procedure can be applied to spike trains of the same neuron across multiple trials to detect and separate responses obtained during different brain states. The procedure can also be applied to spike trains from multiple simultaneously recorded neurons in order to identify volleys of near synchronous activity or to distinguish between excitatory and inhibitory neurons. The procedure was tested using artificial data as well as recordings in vitro in response to fluctuating current waveforms.

[1]  R. Reid,et al.  Precise Firing Events Are Conserved across Neurons , 2002, The Journal of Neuroscience.

[2]  David G. Stork,et al.  Pattern Classification (2nd ed.) , 1999 .

[3]  James Steele,et al.  The Salk Institute. , 1968, The Journal of practical nursing.

[4]  W. Singer,et al.  Modulation of Neuronal Interactions Through Neuronal Synchronization , 2007, Science.

[5]  D. M. Green,et al.  Signal detection theory and psychophysics , 1966 .

[6]  D. Hubel,et al.  Receptive fields, binocular interaction and functional architecture in the cat's visual cortex , 1962, The Journal of physiology.

[7]  R. Larsen,et al.  An introduction to mathematical statistics and its applications (2nd edition) , by R. J. Larsen and M. L. Marx. Pp 630. £17·95. 1987. ISBN 13-487166-9 (Prentice-Hall) , 1987, The Mathematical Gazette.

[8]  Paul H. E. Tiesinga,et al.  The Possible Role of Spike Patterns in Cortical Information Processing , 2005, Journal of Computational Neuroscience.

[9]  Wulfram Gerstner,et al.  Predicting spike timing of neocortical pyramidal neurons by simple threshold models , 2006, Journal of Computational Neuroscience.

[10]  Noureddine Zahid,et al.  A new cluster-validity for fuzzy clustering , 1999, Pattern Recognit..

[11]  C. Koch,et al.  Encoding of visual information by LGN bursts. , 1999, Journal of neurophysiology.

[12]  T. Sejnowski,et al.  Synchrony of Thalamocortical Inputs Maximizes Cortical Reliability , 2010, Science.

[13]  T. Sejnowski,et al.  Reliability of spike timing in neocortical neurons. , 1995, Science.

[14]  Thomas M. Cover,et al.  Elements of Information Theory , 2005 .

[15]  G. Ermentrout,et al.  Reliability, synchrony and noise , 2008, Trends in Neurosciences.

[16]  R. Reid,et al.  Temporal Coding of Visual Information in the Thalamus , 2000, The Journal of Neuroscience.

[17]  Wulfram Gerstner,et al.  Generalized integrate-and-fire models of neuronal activity approximate spike trains of a detailed model to a high degree of accuracy. , 2004, Journal of neurophysiology.

[18]  David A Markowitz,et al.  Rate-specific synchrony: Using noisy oscillations to detect equally active neurons , 2008, Proceedings of the National Academy of Sciences.

[19]  G. Clark,et al.  Reference , 2008 .

[20]  Rajesh P. N. Rao,et al.  Frequency dependence of spike timing reliability in cortical pyramidal cells and interneurons. , 2001, Journal of neurophysiology.

[21]  Heng Tao Shen,et al.  Principal Component Analysis , 2009, Encyclopedia of Biometrics.

[22]  Shengrui Wang,et al.  An objective approach to cluster validation , 2006, Pattern Recognit. Lett..

[23]  D. McCormick,et al.  Rapid Neocortical Dynamics: Cellular and Network Mechanisms , 2009, Neuron.

[24]  Paul H. E. Tiesinga,et al.  Attractor Reliability Reveals Deterministic Structure in Neuronal Spike Trains , 2002, Neural Computation.

[25]  Boudewijn P. F. Lelieveldt,et al.  A new cluster validity index for the fuzzy c-mean , 1998, Pattern Recognit. Lett..

[26]  T. Albright,et al.  Efficient Discrimination of Temporal Patterns by Motion-Sensitive Neurons in Primate Visual Cortex , 1998, Neuron.

[27]  Christof Koch,et al.  Temporal Precision of Spike Trains in Extrastriate Cortex of the Behaving Macaque Monkey , 1999, Neural Computation.

[28]  Robert Tibshirani,et al.  Estimating the number of clusters in a data set via the gap statistic , 2000 .

[29]  Paul H. E. Tiesinga,et al.  Finding the event structure of neuronal spike trains , 2011, Neural Computation.

[30]  T. Sejnowski,et al.  Regulation of spike timing in visual cortical circuits , 2008, Nature Reviews Neuroscience.

[31]  James C. Bezdek,et al.  On cluster validity for the fuzzy c-means model , 1995, IEEE Trans. Fuzzy Syst..

[32]  Paul H. E. Tiesinga,et al.  Attentional modulation of firing rate and synchrony in a model cortical network , 2005, Journal of Computational Neuroscience.

[33]  T. Sejnowski,et al.  Discovering Spike Patterns in Neuronal Responses , 2004, The Journal of Neuroscience.

[34]  Shigeo Abe DrEng Pattern Classification , 2001, Springer London.

[35]  R. Reid,et al.  Predicting Every Spike A Model for the Responses of Visual Neurons , 2001, Neuron.

[36]  James C. Bezdek,et al.  Pattern Recognition with Fuzzy Objective Function Algorithms , 1981, Advanced Applications in Pattern Recognition.

[37]  R. Larsen An introduction to mathematical statistics and its applications / Richard J. Larsen, Morris L. Marx , 1986 .

[38]  M. Steriade Neocortical cell classes are flexible entities , 2004, Nature Reviews Neuroscience.

[39]  Jaime de la Rocha,et al.  Supplementary Information for the article ‘ Correlation between neural spike trains increases with firing rate ’ , 2007 .

[40]  Paul H. E. Tiesinga,et al.  Multiple Spike Time Patterns Occur at Bifurcation Points of Membrane Potential Dynamics , 2012, PLoS Comput. Biol..

[41]  Keying Ye,et al.  Determining the Number of Clusters Using the Weighted Gap Statistic , 2007, Biometrics.

[42]  T. Sejnowski,et al.  Correlated neuronal activity and the flow of neural information , 2001, Nature Reviews Neuroscience.

[43]  J. Victor,et al.  Nature and precision of temporal coding in visual cortex: a metric-space analysis. , 1996, Journal of neurophysiology.

[44]  Stefano Panzeri,et al.  Analytical estimates of limited sampling biases in different information measures. , 1996, Network.

[45]  Terrence J. Sejnowski,et al.  Selective attention through phase relationship of excitatory and inhibitory input synchrony in a model cortical neuron , 2006, Neural Networks.

[46]  William Bialek,et al.  Spikes: Exploring the Neural Code , 1996 .

[47]  William Bialek,et al.  Entropy and Information in Neural Spike Trains , 1996, cond-mat/9603127.

[48]  R K Powers,et al.  Contributions of the input signal and prior activation history to the discharge behaviour of rat motoneurones , 2005, The Journal of physiology.

[49]  D. McCormick,et al.  Comparative electrophysiology of pyramidal and sparsely spiny stellate neurons of the neocortex. , 1985, Journal of neurophysiology.

[50]  E J Chichilnisky,et al.  Prediction and Decoding of Retinal Ganglion Cell Responses with a Probabilistic Spiking Model , 2005, The Journal of Neuroscience.