Frontiers in Computational Neuroscience Materials and Methods Measures of Correlation

Concerted neural activity can reflect specific features of sensory stimuli or behavioral tasks. Correlation coefficients and count correlations are frequently used to measure correlations between neurons, design synthetic spike trains and build population models. But are correlation coefficients always a reliable measure of input correlations? Here, we consider a stochastic model for the generation of correlated spike sequences which replicate neuronal pairwise correlations in many important aspects. We investigate under which conditions the correlation coefficients reflect the degree of input synchrony and when they can be used to build population models. We find that correlation coefficients can be a poor indicator of input synchrony for some cases of input correlations. In particular, count correlations computed for large time bins can vanish despite the presence of input correlations. These findings suggest that network models or potential coding schemes of neural population activity need to incorporate temporal properties of correlated inputs and take into consideration the regimes of firing rates and correlation strengths to ensure that their building blocks are an unambiguous measures of synchrony.

[1]  N. Brunel,et al.  Firing frequency of leaky intergrate-and-fire neurons with synaptic current dynamics. , 1998, Journal of theoretical biology.

[2]  Theiler,et al.  Generating surrogate data for time series with several simultaneously measured variables. , 1994, Physical review letters.

[3]  Nicolas Fourcaud-Trocmé,et al.  Correlation-induced Synchronization of Oscillations in Olfactory Bulb Neurons , 2022 .

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

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

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

[7]  Shun-ichi Amari,et al.  Measure of Correlation Orthogonal to Change in Firing Rate , 2009, Neural Computation.

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

[9]  J. Hüsler Extremes and related properties of random sequences and processes , 1984 .

[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]  E. Niebur,et al.  Growth patterns in the developing brain detected by using continuum mechanical tensor maps , 2022 .

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

[13]  Fred Wolf,et al.  Correlations and synchrony in threshold neuron models. , 2008, Physical review letters.

[14]  S. Rice Mathematical analysis of random noise , 1944 .

[15]  R K Powers,et al.  Relationship between simulated common synaptic input and discharge synchrony in cat spinal motoneurons. , 2001, Journal of neurophysiology.

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

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

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

[19]  Néstor Parga,et al.  Auto- and crosscorrelograms for the spike response of leaky integrate-and-fire neurons with slow synapses. , 2006, Physical review letters.

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

[21]  Robert E. Kass,et al.  Spike Count Correlation Increases with Length of Time Interval in the Presence of Trial-to-Trial Variation , 2006, Neural Computation.

[22]  Jude F. Mitchell,et al.  Spatial Attention Decorrelates Intrinsic Activity Fluctuations in Macaque Area V4 , 2009, Neuron.

[23]  David S. Greenberg,et al.  Population imaging of ongoing neuronal activity in the visual cortex of awake rats , 2008, Nature Neuroscience.

[24]  Haim Sompolinsky,et al.  Stimulus-Dependent Correlations in Threshold-Crossing Spiking Neurons , 2009, Neural Computation.

[25]  N. B,et al.  Firing Frequency of Leaky Integrate-and-fire Neurons with Synaptic Current Dynamics , 1998 .

[26]  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..

[27]  Daeyeol Lee,et al.  Neural Noise and Movement-Related Codes in the Macaque Supplementary Motor Area , 2003, The Journal of Neuroscience.

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

[29]  Peter Jung,et al.  STOCHASTIC RESONANCE AND OPTIMAL DESIGN OF THRESHOLD DETECTORS , 1995 .

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

[31]  G. Laurent,et al.  Impaired odour discrimination on desynchronization of odour-encoding neural assemblies , 1997, Nature.

[32]  M. A. Smith,et al.  Spatial and Temporal Scales of Neuronal Correlation in Primary Visual Cortex , 2008, The Journal of Neuroscience.

[33]  Jørn Hounsgaard,et al.  Influence of membrane properties on spike synchronization in neurons: theory and experiments , 2003, Network.

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

[35]  Michael Rudolph,et al.  The high-conductance state of neocortical neurons in vivo , 2003, Nature Reviews Neuroscience.

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

[37]  Nicolas Brunel,et al.  Dynamics of the Firing Probability of Noisy Integrate-and-Fire Neurons , 2002, Neural Computation.

[38]  C. Gray,et al.  Cellular Mechanisms Contributing to Response Variability of Cortical Neurons In Vivo , 1999, The Journal of Neuroscience.

[39]  Moritz Helias,et al.  Correlations in spiking neuronal networks with distance dependent connections , 2009, Journal of Computational Neuroscience.

[40]  A. Destexhe,et al.  The high-conductance state of neocortical neurons in vivo , 2003, Nature Reviews Neuroscience.

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

[42]  D. Ferster,et al.  Synchronous Membrane Potential Fluctuations in Neurons of the Cat Visual Cortex , 1999, Neuron.

[43]  Benjamin Lindner,et al.  Comparative study of different integrate-and-fire neurons: spontaneous activity, dynamical response, and stimulus-induced correlation. , 2009, Physical review. E, Statistical, nonlinear, and soft matter physics.