Higher-Order Correlations in Non-Stationary Parallel Spike Trains: Statistical Modeling and Inference

The extent to which groups of neurons exhibit higher-order correlations in their spiking activity is a controversial issue in current brain research. A major difficulty is that currently available tools for the analysis of massively parallel spike trains (N >10) for higher-order correlations typically require vast sample sizes. While multiple single-cell recordings become increasingly available, experimental approaches to investigate the role of higher-order correlations suffer from the limitations of available analysis techniques. We have recently presented a novel method for cumulant-based inference of higher-order correlations (CuBIC) that detects correlations of higher order even from relatively short data stretches of length T = 10–100 s. CuBIC employs the compound Poisson process (CPP) as a statistical model for the population spike counts, and assumes spike trains to be stationary in the analyzed data stretch. In the present study, we describe a non-stationary version of the CPP by decoupling the correlation structure from the spiking intensity of the population. This allows us to adapt CuBIC to time-varying firing rates. Numerical simulations reveal that the adaptation corrects for false positive inference of correlations in data with pure rate co-variation, while allowing for temporal variations of the firing rates has a surprisingly small effect on CuBICs sensitivity for correlations.

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

[2]  Y. Sakurai,et al.  Dynamic Synchrony of Firing in the Monkey Prefrontal Cortex during Working-Memory Tasks , 2006, The Journal of Neuroscience.

[3]  A. Villa,et al.  Detection of syntonies between multiple spike trains using a coarse-grain binarization of spike count distributions , 2004, Network.

[4]  A. Aertsen,et al.  Spike synchronization and rate modulation differentially involved in motor cortical function. , 1997, Science.

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

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

[7]  G. P. Moore,et al.  Neuronal spike trains and stochastic point processes. II. Simultaneous spike trains. , 1967, Biophysical journal.

[8]  Shun-ichi Amari,et al.  Information-Geometric Measure for Neural Spikes , 2002, Neural Computation.

[9]  Kathryn B. Laskey,et al.  Neural Coding: Higher-Order Temporal Patterns in the Neurostatistics of Cell Assemblies , 2000, Neural Computation.

[10]  Daeyeol Lee,et al.  Effects of noise correlations on information encoding and decoding. , 2006, Journal of neurophysiology.

[11]  S. Grün,et al.  Higher-Order Correlations and Cumulants , 2010 .

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

[13]  Sonja Grün,et al.  Unitary Events in Multiple Single-Neuron Spiking Activity: I. Detection and Significance , 2002, Neural Computation.

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

[15]  W. Singer,et al.  Stimulus-specific neuronal oscillations in orientation columns of cat visual cortex. , 1989, Proceedings of the National Academy of Sciences of the United States of America.

[16]  G. P. Moore,et al.  Neuronal spike trains and stochastic point processes. I. The single spike train. , 1967, Biophysical journal.

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

[18]  M K Habib,et al.  Dynamics of neuronal firing correlation: modulation of "effective connectivity". , 1989, Journal of neurophysiology.

[19]  R. Kass,et al.  Multiple neural spike train data analysis: state-of-the-art and future challenges , 2004, Nature Neuroscience.

[20]  T. Speed,et al.  Additive and Multiplicative Models and Interactions , 1983 .

[21]  Günther Palm,et al.  Detecting higher-order interactions among the spiking events in a group of neurons , 1995, Biological Cybernetics.

[22]  Pieter R. Roelfsema,et al.  The Effects of Pair-wise and Higher-order Correlations on the Firing Rate of a Postsynaptic Neuron , 1998, Neural Computation.

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

[24]  Ad Aertsen,et al.  Stable propagation of synchronous spiking in cortical neural networks , 1999, Nature.

[25]  Robert E Kass,et al.  Trial-to-trial variability and its effect on time-varying dependency between two neurons. , 2005, Journal of neurophysiology.

[26]  Donald L. Snyder,et al.  Random Point Processes in Time and Space , 1991 .

[27]  Emery N. Brown,et al.  State-space analysis on time-varying correlations in parallel spike sequences , 2009, 2009 IEEE International Conference on Acoustics, Speech and Signal Processing.

[28]  S. Rotter,et al.  Decomposition of neuronal assembly activity via empirical de-Poissonization , 2007, 0711.1965.

[29]  A. Aertsen,et al.  Neuronal assemblies , 1989, IEEE Transactions on Biomedical Engineering.

[30]  William H. Press,et al.  Numerical recipes in C , 2002 .

[31]  Elvira Di Nardo,et al.  A unifying framework for $k$-statistics, polykays and their multivariate generalizations , 2006, math/0607623.

[32]  W. Singer,et al.  Stimulus-dependent synchronization of neuronal responses in the visual cortex of the awake macaque monkey , 1996, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[33]  Pranesh Kumar MOMENTS INEQUALITIES OF A RANDOM VARIABLE DEFINED OVER A FINITE INTERVAL , 2002 .

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

[35]  William R. Softky,et al.  Simple codes versus efficient codes , 1995, Current Opinion in Neurobiology.

[36]  A Aertsen,et al.  ‘Dynamics of neuronal interactions’ cannot be explained by ‘neuronal transients’ , 1995, Proceedings of the Royal Society of London. Series B: Biological Sciences.

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

[38]  Jos J. Eggermont The Correlative Brain , 1990 .

[39]  Eric Shea-Brown,et al.  Stimulus-Dependent Correlations and Population Codes , 2008, Neural Computation.

[40]  M. A. Smith,et al.  Stimulus Dependence of Neuronal Correlation in Primary Visual Cortex of the Macaque , 2005, The Journal of Neuroscience.

[41]  B. Streitberg Lancaster Interactions Revisited , 1990 .

[42]  Stefano Panzeri,et al.  The impact of high-order interactions on the rate of synchronous discharge and information transmission in somatosensory cortex , 2009, Philosophical Transactions of the Royal Society A: Mathematical, Physical and Engineering Sciences.

[43]  Sonja Grün,et al.  Data-driven significance estimation for precise spike correlation. , 2009, Journal of neurophysiology.

[44]  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..

[45]  F. Attneave,et al.  The Organization of Behavior: A Neuropsychological Theory , 1949 .

[46]  Sonja Grün,et al.  Can Spike Coordination Be Differentiated from Rate Covariation? , 2008, Neural Computation.

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

[48]  Sonja Grün,et al.  Unitary Events in Multiple Single-Neuron Spiking Activity: II. Nonstationary Data , 2002, Neural Computation.

[49]  G. Buzsáki,et al.  Behavior-dependent short-term assembly dynamics in the medial prefrontal cortex , 2008, Nature Neuroscience.

[50]  A. Grinvald,et al.  Linking spontaneous activity of single cortical neurons and the underlying functional architecture. , 1999, Science.

[51]  A. Aertsen,et al.  Dynamics of neuronal interactions in monkey cortex in relation to behavioural events , 1995, Nature.