Motif statistics and spike correlations in neuronal networks

Motifs are patterns of subgraphs that are the building blocks of complex networks. Recent experiments have characterized the frequencies with which different motifs occur in biological neural networks, and found remarkable deviations from what we would expect if the networks were randomly connected [1]. Here, we study the impact of such patterns of connectivity on the level of correlated, or synchronized, spiking activity among pairs of cells. Correlations in spiking activity have been shown to strongly impact the neural coding of information. We use a linear, stochastic model of recurrent networks. A cell’s time-dependent firing rate is perturbed from its baseline level by convolution of a response kernel and the input signal from presynaptic neurons. Each neuron generates spikes as an inhomogeneous Poisson process. Previous studies have shown that such models can capture pairwise correlations in integrate and fire networks [2,3], and they are closely related to spike response and Hawkes models [4,6]. For this model, there is an explicit expression for pairwise correlation in terms of the connectivity matrix. By expanding this expression in a series, one can relate each term to a different motif (with a different number of connections). Through a resumming technique, we show that the average correlation across the network can be closely approximated using the frequencies of only first and second order motifs. These are the diverging motif—two cells both receiving projections from another cell, its counterpart the converging motif—two cells projecting to a common cell, and the chain motif—three cells linked by two consecutive projections. Specifically, we show that the prevalence of diverging and chain motifs tends to increase correlation, while the converging motif makes no contribution to the average correlation. Moreover, we numerically show that variance of correlations across the network is largely determined by the frequency of the chain motif (see Figure ​Figure1)1) alone. Finally, we demonstrate potential effect of motif statistics on neural coding by showing how motif frequencies impact linear Fisher information. In particular, we find that the linear Fisher information is only affected by converging motif frequency (more information with given more converging motifs). Figure 1 Each dot represent one network sample plotted against its chain and diverging motif frequencies. Color shows the standard deviation of correlations in the network. Inset is the same plot with respect to diverging and converging motifs.

[1]  Brent Doiron,et al.  Theory of oscillatory firing induced by spatially correlated noise and delayed inhibitory feedback. , 2005, Physical review. E, Statistical, nonlinear, and soft matter physics.

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

[3]  Ehud Zohary,et al.  Correlated neuronal discharge rate and its implications for psychophysical performance , 1994, Nature.

[4]  E T Rolls,et al.  Correlations and the encoding of information in the nervous system , 1999, Proceedings of the Royal Society of London. Series B: Biological Sciences.

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

[6]  M. J. Richardson,et al.  Dynamics of populations and networks of neurons with voltage-activated and calcium-activated currents. , 2009, Physical review. E, Statistical, nonlinear, and soft matter physics.

[7]  Alexander S. Ecker,et al.  Decorrelated Neuronal Firing in Cortical Microcircuits , 2010, Science.

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

[9]  Duncan J. Watts,et al.  Collective dynamics of ‘small-world’ networks , 1998, Nature.

[10]  Eric Shea-Brown,et al.  Correlation and synchrony transfer in integrate-and-fire neurons: basic properties and consequences for coding. , 2008, Physical review letters.

[11]  Nicolas Brunel,et al.  How Connectivity, Background Activity, and Synaptic Properties Shape the Cross-Correlation between Spike Trains , 2009, The Journal of Neuroscience.

[12]  M. Diamond,et al.  The Role of Spike Timing in the Coding of Stimulus Location in Rat Somatosensory Cortex , 2001, Neuron.

[13]  M. Newman,et al.  Random graphs with arbitrary degree distributions and their applications. , 2000, Physical review. E, Statistical, nonlinear, and soft matter physics.

[14]  J. White,et al.  Channel noise in neurons , 2000, Trends in Neurosciences.

[15]  H. Sompolinsky,et al.  Chaos in Neuronal Networks with Balanced Excitatory and Inhibitory Activity , 1996, Science.

[16]  Nicolas Brunel,et al.  From Spiking Neuron Models to Linear-Nonlinear Models , 2011, PLoS Comput. Biol..

[17]  J. Elgin The Fokker-Planck Equation: Methods of Solution and Applications , 1984 .

[18]  Wolfgang Maass,et al.  Motif distribution, dynamical properties, and computational performance of two data-based cortical microcircuit templates , 2009, Journal of Physiology-Paris.

[19]  T. Sejnowski On the stochastic dynamics of neuronal interaction , 1976, Biological Cybernetics.

[20]  P. Dayan,et al.  Supporting Online Material Materials and Methods Som Text Figs. S1 to S9 References the Asynchronous State in Cortical Circuits , 2022 .

[21]  D. Hansel,et al.  How Spike Generation Mechanisms Determine the Neuronal Response to Fluctuating Inputs , 2003, The Journal of Neuroscience.

[22]  P. Latham,et al.  Synergy, Redundancy, and Independence in Population Codes, Revisited , 2005, The Journal of Neuroscience.

[23]  Aaditya V Rangan Diagrammatic expansion of pulse-coupled network dynamics. , 2009, Physical review letters.

[24]  Mark E. J. Newman,et al.  The Structure and Function of Complex Networks , 2003, SIAM Rev..

[25]  Brent Doiron,et al.  Oscillatory activity in electrosensory neurons increases with the spatial correlation of the stochastic input stimulus. , 2004, Physical review letters.

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

[27]  Aaditya V Rangan,et al.  Diagrammatic expansion of pulse-coupled network dynamics in terms of subnetworks. , 2009, Physical review. E, Statistical, nonlinear, and soft matter physics.

[28]  Peter Dayan,et al.  The Effect of Correlated Variability on the Accuracy of a Population Code , 1999, Neural Computation.

[29]  F. Chung,et al.  Connected Components in Random Graphs with Given Expected Degree Sequences , 2002 .

[30]  Sompolinsky,et al.  Theory of correlations in stochastic neural networks. , 1994, Physical review. E, Statistical physics, plasmas, fluids, and related interdisciplinary topics.

[31]  Robert Rosenbaum,et al.  Mechanisms That Modulate the Transfer of Spiking Correlations , 2011, Neural Computation.

[32]  Michael J. Berry,et al.  Synergy, Redundancy, and Independence in Population Codes , 2003, The Journal of Neuroscience.

[33]  Charles R. Johnson,et al.  Matrix analysis , 1985, Statistical Inference for Engineers and Data Scientists.

[34]  Eric Shea-Brown,et al.  Impact of Network Structure and Cellular Response on Spike Time Correlations , 2011, PLoS Comput. Biol..

[35]  P. Fries A mechanism for cognitive dynamics: neuronal communication through neuronal coherence , 2005, Trends in Cognitive Sciences.

[36]  A. Crofts,et al.  Structure and function of the -complex of , 1992 .

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

[38]  Alexandre Pouget,et al.  Insights from a Simple Expression for Linear Fisher Information in a Recurrently Connected Population of Spiking Neurons , 2011, Neural Computation.

[39]  Theoden I. Netoff,et al.  Synchronization from Second Order Network Connectivity Statistics , 2011, Front. Comput. Neurosci..

[40]  Alex Roxin,et al.  The Role of Degree Distribution in Shaping the Dynamics in Networks of Sparsely Connected Spiking Neurons , 2011, Front. Comput. Neurosci..

[41]  Xiao-Jing Wang,et al.  Mean-Field Theory of Irregularly Spiking Neuronal Populations and Working Memory in Recurrent Cortical Networks , 2003 .

[42]  A. Hawkes Point Spectra of Some Mutually Exciting Point Processes , 1971 .

[43]  O. Sporns,et al.  Motifs in Brain Networks , 2004, PLoS biology.

[44]  Hilbert J. Kappen,et al.  Input-Driven Oscillations in Networks with Excitatory and Inhibitory Neurons with Dynamic Synapses , 2007, Neural Computation.

[45]  Sen Song,et al.  Highly Nonrandom Features of Synaptic Connectivity in Local Cortical Circuits , 2005, PLoS biology.

[46]  Wulfram Gerstner,et al.  Spiking Neuron Models , 2002 .

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

[48]  Randy M Bruno,et al.  Synchrony in sensation , 2011, Current Opinion in Neurobiology.

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

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

[51]  L. Abbott,et al.  Eigenvalue spectra of random matrices for neural networks. , 2006, Physical review letters.

[52]  Stefan Rotter,et al.  How Structure Determines Correlations in Neuronal Networks , 2011, PLoS Comput. Biol..

[53]  Magnus J. E. Richardson,et al.  Spike-train spectra and network response functions for non-linear integrate-and-fire neurons , 2008, Biological Cybernetics.

[54]  L Schimansky-Geier,et al.  Transmission of noise coded versus additive signals through a neuronal ensemble. , 2001, Physical review letters.

[55]  M. Cohen,et al.  Measuring and interpreting neuronal correlations , 2011, Nature Neuroscience.

[56]  H. Sompolinsky,et al.  Population coding in neuronal systems with correlated noise. , 2001, Physical review. E, Statistical, nonlinear, and soft matter physics.

[57]  T. Sejnowski,et al.  Impact of Correlated Synaptic Input on Output Firing Rate and Variability in Simple Neuronal Models , 2000, The Journal of Neuroscience.

[58]  Peter Dayan,et al.  Theoretical Neuroscience: Computational and Mathematical Modeling of Neural Systems , 2001 .

[59]  Stefan Rotter,et al.  Recurrent interactions in spiking networks with arbitrary topology. , 2012, Physical review. E, Statistical, nonlinear, and soft matter physics.

[60]  A. Hawkes Spectra of some self-exciting and mutually exciting point processes , 1971 .

[61]  W Singer,et al.  Visual feature integration and the temporal correlation hypothesis. , 1995, Annual review of neuroscience.

[62]  Frances S. Chance,et al.  Effects of synaptic noise and filtering on the frequency response of spiking neurons. , 2001, Physical review letters.

[63]  Marc Timme,et al.  Synaptic Scaling in Combination with Many Generic Plasticity Mechanisms Stabilizes Circuit Connectivity , 2011, Front. Comput. Neurosci..

[64]  F. Rieke,et al.  Origin of correlated activity between parasol retinal ganglion cells , 2008, Nature Neuroscience.

[65]  Alexander S. Ecker,et al.  The Effect of Noise Correlations in Populations of Diversely Tuned Neurons , 2011, The Journal of Neuroscience.

[66]  Steven J. Cox,et al.  Mathematics for Neuroscientists , 2010 .