A generative spike train model with time-structured higher order correlations

Emerging technologies are revealing the spiking activity in ever larger neural ensembles. Frequently, this spiking is far from independent, with correlations in the spike times of different cells. Understanding how such correlations impact the dynamics and function of neural ensembles remains an important open problem. Here we describe a new, generative model for correlated spike trains that can exhibit many of the features observed in data. Extending prior work in mathematical finance, this generalized thinning and shift (GTaS) model creates marginally Poisson spike trains with diverse temporal correlation structures. We give several examples which highlight the model's flexibility and utility. For instance, we use it to examine how a neural network responds to highly structured patterns of inputs. We then show that the GTaS model is analytically tractable, and derive cumulant densities of all orders in terms of model parameters. The GTaS framework can therefore be an important tool in the experimental and theoretical exploration of neural dynamics.

[1]  Eero P. Simoncelli,et al.  Spatio-temporal correlations and visual signalling in a complete neuronal population , 2008, Nature.

[2]  Haim Sompolinsky,et al.  Nonlinear Population Codes , 2004, Neural Computation.

[3]  Mark T. Harnett,et al.  Nonlinear dendritic integration of sensory and motor input during an active sensing task , 2012, Nature.

[4]  M. Häusser,et al.  Dendritic Discrimination of Temporal Input Sequences in Cortical Neurons , 2010, Science.

[5]  M. Häusser,et al.  Synaptic Integration Gradients in Single Cortical Pyramidal Cell Dendrites , 2011, Neuron.

[6]  Jonathon Shlens,et al.  The Structure of Multi-Neuron Firing Patterns in Primate Retina , 2006, The Journal of Neuroscience.

[7]  C. Gray,et al.  Higher Order Correlations within Cortical Layers Dominate Functional Connectivity in Microcolumns , 2012, 1301.0050.

[8]  L A JEFFRESS,et al.  A place theory of sound localization. , 1948, Journal of comparative and physiological psychology.

[9]  R. Cowan An introduction to the theory of point processes , 1978 .

[10]  A Aertsen,et al.  Propagation of synchronous spiking activity in feedforward neural networks , 1996, Journal of Physiology-Paris.

[11]  Sonja Grün,et al.  CuBIC: cumulant based inference of higher-order correlations in massively parallel spike trains , 2009, Journal of Computational Neuroscience.

[12]  Eugene M. Izhikevich,et al.  Polychronization: Computation with Spikes , 2006, Neural Computation.

[13]  S. Swain Handbook of Stochastic Methods for Physics, Chemistry and the Natural Sciences , 1984 .

[14]  Daryl J. Daley,et al.  An Introduction to the Theory of Point Processes , 2013 .

[15]  J. R. Rosenberg,et al.  An extended difference of coherence test for comparing and combining several independent coherence estimates: theory and application to the study of motor units and physiological tremor , 1997, Journal of Neuroscience Methods.

[16]  Shan Yu,et al.  Higher-Order Interactions Characterized in Cortical Activity , 2011, The Journal of Neuroscience.

[17]  Eric Shea-Brown,et al.  When are feedforward microcircuits well-modeled by maximum entropy methods? , 2010, ArXiv.

[18]  D. H. Johnson,et al.  Jointly Poisson processes , 2009, 0911.2524.

[19]  Shy Shoham,et al.  Generation of Spike Trains with Controlled Auto- and Cross-Correlation Functions , 2009, Neural Computation.

[20]  Markus Diesmann,et al.  The spread of rate and correlation in stationary cortical networks , 2003, Neurocomputing.

[21]  Jerry M. Mendel,et al.  Tutorial on higher-order statistics (spectra) in signal processing and system theory: theoretical results and some applications , 1991, Proc. IEEE.

[22]  J. J. Hopfield,et al.  Pattern recognition computation using action potential timing for stimulus representation , 1995, Nature.

[23]  Philip H Smith,et al.  Coincidence Detection in the Auditory System 50 Years after Jeffress , 1998, Neuron.

[24]  Stefan Rotter,et al.  Higher-Order Statistics of Input Ensembles and the Response of Simple Model Neurons , 2003, Neural Computation.

[25]  H. Sompolinsky,et al.  The tempotron: a neuron that learns spike timing–based decisions , 2006, Nature Neuroscience.

[26]  Robert Rosenbaum,et al.  Frontiers in Computational Neuroscience Computational Neuroscience , 2022 .

[27]  Romain Brette,et al.  Generation of Correlated Spike Trains , 2009, Neural Computation.

[28]  C. W. Gardiner,et al.  Handbook of stochastic methods - for physics, chemistry and the natural sciences, Second Edition , 1986, Springer series in synergetics.

[29]  W. Newsome,et al.  The Variable Discharge of Cortical Neurons: Implications for Connectivity, Computation, and Information Coding , 1998, The Journal of Neuroscience.

[30]  Maurice G. Kendall,et al.  The Advanced Theory of Statistics, Vol. I. , 1945 .

[31]  Arnaud Delorme,et al.  Spike-based strategies for rapid processing , 2001, Neural Networks.

[32]  József Fiser,et al.  Suppression of cortical neural variability is stimulus- and state-dependent. , 2012, Journal of neurophysiology.

[33]  Eric Shea-Brown,et al.  Time scales of spike-train correlation for neural oscillators with common drive. , 2009, Physical review. E, Statistical, nonlinear, and soft matter physics.

[34]  Jeffrey D. Scargle,et al.  An Introduction to the Theory of Point Processes, Vol. I: Elementary Theory and Methods , 2004, Technometrics.

[35]  Sonja Grün,et al.  Analysis of Parallel Spike Trains , 2010 .

[36]  Yuji Ikegaya,et al.  Synfire Chains and Cortical Songs: Temporal Modules of Cortical Activity , 2004, Science.

[37]  U. Knoblich,et al.  Optogenetic drive of neocortical pyramidal neurons generates fMRI signals that are correlated with spiking activity , 2013, Brain Research.

[38]  Stefan Rotter,et al.  Dependence of Neuronal Correlations on Filter Characteristics and Marginal Spike Train Statistics , 2008, Neural Computation.

[39]  D. Wilkin,et al.  Neuron , 2001, Brain Research.

[40]  R. G. Medhurst,et al.  Topics in the Theory of Random Noise , 1969 .

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

[42]  Peter E. Latham,et al.  Pairwise Maximum Entropy Models for Studying Large Biological Systems: When They Can Work and When They Can't , 2008, PLoS Comput. Biol..

[43]  Alexander S. Ecker,et al.  Generating Spike Trains with Specified Correlation Coefficients , 2009, Neural Computation.

[44]  Nicole Bäuerle,et al.  Multivariate Counting Processes: Copulas and Beyond , 2005, ASTIN Bulletin.

[45]  Moshe Abeles,et al.  Corticonics: Neural Circuits of Cerebral Cortex , 1991 .

[46]  Moshe Abeles,et al.  Synfire chain in a balanced network , 2002, Neurocomputing.

[47]  Keith J. Kelleher,et al.  Three-dimensional random access multiphoton microscopy for functional imaging of neuronal activity , 2008, Nature Neuroscience.

[48]  Michael J. Berry,et al.  Weak pairwise correlations imply strongly correlated network states in a neural population , 2005, Nature.

[49]  M. Bethge,et al.  Common input explains higher-order correlations and entropy in a simple model of neural population activity. , 2011, Physical review letters.

[50]  Valentin Dragoi,et al.  Correlated Variability in Laminar Cortical Circuits , 2012, Neuron.

[51]  Emery N. Brown,et al.  State-Space Analysis of Time-Varying Higher-Order Spike Correlation for Multiple Neural Spike Train Data , 2012, PLoS Comput. Biol..

[52]  A. Pouget,et al.  Neural correlations, population coding and computation , 2006, Nature Reviews Neuroscience.

[53]  J. Pfister,et al.  A triplet spike-timing–dependent plasticity model generalizes the Bienenstock–Cooper–Munro rule to higher-order spatiotemporal correlations , 2011, Proceedings of the National Academy of Sciences.

[54]  宁北芳,et al.  疟原虫var基因转换速率变化导致抗原变异[英]/Paul H, Robert P, Christodoulou Z, et al//Proc Natl Acad Sci U S A , 2005 .

[55]  K. Harris Neural signatures of cell assembly organization , 2005, Nature Reviews Neuroscience.

[56]  Sami El Boustani,et al.  Prediction of spatiotemporal patterns of neural activity from pairwise correlations. , 2009, Physical review letters.

[57]  William R. Softky,et al.  Comparison of discharge variability in vitro and in vivo in cat visual cortex neurons. , 1996, Journal of neurophysiology.

[58]  W. Bair,et al.  Correlated Firing in Macaque Visual Area MT: Time Scales and Relationship to Behavior , 2001, The Journal of Neuroscience.

[59]  G. Buzsáki,et al.  Sequential structure of neocortical spontaneous activity in vivo , 2007, Proceedings of the National Academy of Sciences.

[60]  Michael A. Henninger,et al.  High-Performance Genetically Targetable Optical Neural Silencing via Light-Driven Proton Pumps , 2010 .

[61]  CainNicholas,et al.  Impact of correlated neural activity on decision-making performance , 2013 .

[62]  Yutaka Sakai,et al.  Synchronous Firing and Higher-Order Interactions in Neuron Pool , 2003, Neural Computation.

[63]  Jonathon Shlens,et al.  The Structure of Large-Scale Synchronized Firing in Primate Retina , 2009, The Journal of Neuroscience.

[64]  Michael J. Berry,et al.  Gibbs distribution analysis of temporal correlations structure in retina ganglion cells , 2011, Journal of Physiology - Paris.

[65]  J. Knott The organization of behavior: A neuropsychological theory , 1951 .

[66]  E. Boyden,et al.  Multiple-Color Optical Activation, Silencing, and Desynchronization of Neural Activity, with Single-Spike Temporal Resolution , 2007, PloS one.

[67]  David Vere-Jones,et al.  Point Processes , 2011, International Encyclopedia of Statistical Science.

[68]  K. Harris,et al.  Gating of Sensory Input by Spontaneous Cortical Activity , 2013, The Journal of Neuroscience.

[69]  D. Brillinger An Introduction to Polyspectra , 1965 .

[70]  G. Buzsáki,et al.  Spike train dynamics predicts theta-related phase precession in hippocampal pyramidal cells , 2002, Nature.

[71]  R. Fisher The Advanced Theory of Statistics , 1943, Nature.

[72]  R. L. Stratonovich,et al.  Topics in the theory of random noise , 1967 .

[73]  Ifije E. Ohiorhenuan,et al.  Sparse coding and high-order correlations in fine-scale cortical networks , 2010, Nature.

[74]  J. Magee,et al.  State-Dependent Dendritic Computation in Hippocampal CA1 Pyramidal Neurons , 2006, The Journal of Neuroscience.

[75]  György Buzsáki,et al.  Neural Syntax: Cell Assemblies, Synapsembles, and Readers , 2010, Neuron.

[76]  W. Gerstner,et al.  Triplets of Spikes in a Model of Spike Timing-Dependent Plasticity , 2006, The Journal of Neuroscience.

[77]  Robert Rosenbaum,et al.  The Effects of Pooling on Spike Train Correlations , 2011, Front. Neurosci..

[78]  Eric Shea-Brown,et al.  Impact of Correlated Neural Activity on Decision-Making Performance , 2012, Neural Computation.

[79]  Andrew M. Clark,et al.  Stimulus onset quenches neural variability: a widespread cortical phenomenon , 2010, Nature Neuroscience.

[80]  John M. Beggs,et al.  A Maximum Entropy Model Applied to Spatial and Temporal Correlations from Cortical Networks In Vitro , 2008, The Journal of Neuroscience.

[81]  A. Litwin-Kumar,et al.  Slow dynamics and high variability in balanced cortical networks with clustered connections , 2012, Nature Neuroscience.

[82]  Simon R. Schultz,et al.  Statistical modelling of higher-order correlations in pools of neural activity , 2012, 1211.6348.

[83]  M Abeles,et al.  Spatio-temporal firing patterns in the frontal cortex of behaving monkeys , 1996, Journal of Physiology-Paris.

[84]  B. A. Conway,et al.  The effects of laforin, malin, Stbd1, and Ptg deficiencies on heart glycogen levels in Pompe disease mouse models , 2015 .

[85]  J. Rinzel,et al.  The role of dendrites in auditory coincidence detection , 1998, Nature.

[86]  Sheldon M. Ross,et al.  Stochastic Processes , 2018, Gauge Integral Structures for Stochastic Calculus and Quantum Electrodynamics.

[87]  Michael J. Berry,et al.  The Neural Code of the Retina , 1999, Neuron.

[88]  R. Segev,et al.  Sparse low-order interaction network underlies a highly correlated and learnable neural population code , 2011, Proceedings of the National Academy of Sciences.

[89]  Diego A Gutnisky,et al.  Generation of spatiotemporally correlated spike trains and local field potentials using a multivariate autoregressive process. , 2010, Journal of neurophysiology.

[90]  M. Kendall,et al.  The advanced theory of statistics , 1945 .

[91]  S. Rumpel,et al.  Discrete Neocortical Dynamics Predict Behavioral Categorization of Sounds , 2012, Neuron.