Spike-Field Granger Causality for Hybrid Neural Data Analysis.

Neurotechnological innovations allow for the simultaneous recording at various scales, ranging from spiking activity of individual neurons to large neural population's local field potentials (LFPs). This capability necessitates developing multiscale analysis of spike-field activity. A joint analysis of the hybrid neural data is crucial for bridging the scales between single neurons and local network. Granger causality is a fundamental measure to evaluate directional influences among neural signals. However, it is mainly limited to inferring causal influence between the same type of signals-either LFPs or spike trains-but not well-developed between two different signal types. Here we propose a model-free, nonparametric spike-field Granger causality measure for hybrid data analysis. Our measure is distinct from the existing methods in that we use the precise spike timing rather than the spike counts. The latter clearly distorts the information in the mixed analysis of spikes and LFP. Our measure is validated by an extensive set of simulated data. When applied to LFPs and spiking activity simultaneously recorded from visual areas V1 and V4 of monkeys performing a contour detection task, we are able to confirm computationally the long-standing experimental finding of the input-output relationship between LFPs and spikes. Importantly, we demonstrate that spike-field Granger causality can be used to reveal the modulatory effects that are inaccessible by traditional methods, such that the spike->LFP Granger causality is modulated by the behavioral task, whereas LFP->spike Granger causality is mainly related to the average synaptic input.

[1]  D. Slepian First Passage Time for a Particular Gaussian Process , 1961 .

[2]  C. Granger Investigating Causal Relations by Econometric Models and Cross-Spectral Methods , 1969 .

[3]  G. Wilson The Factorization of Matricial Spectral Densities , 1972 .

[4]  D. Thomson,et al.  Spectrum estimation and harmonic analysis , 1982, Proceedings of the IEEE.

[5]  J. Geweke,et al.  Measurement of Linear Dependence and Feedback between Multiple Time Series , 1982 .

[6]  J. Geweke,et al.  Measures of Conditional Linear Dependence and Feedback between Time Series , 1984 .

[7]  U. Mitzdorf Current source-density method and application in cat cerebral cortex: investigation of evoked potentials and EEG phenomena. , 1985, Physiological reviews.

[8]  P. Mitra,et al.  Analysis of dynamic brain imaging data. , 1998, Biophysical journal.

[9]  Hualou Liang,et al.  Short-window spectral analysis of cortical event-related potentials by adaptive multivariate autoregressive modeling: data preprocessing, model validation, and variability assessment , 2000, Biological Cybernetics.

[10]  R. Desimone,et al.  Modulation of Oscillatory Neuronal Synchronization by Selective Visual Attention , 2001, Science.

[11]  Partha P. Mitra,et al.  Sampling Properties of the Spectrum and Coherency of Sequences of Action Potentials , 2000, Neural Computation.

[12]  Ali H. Sayed,et al.  A survey of spectral factorization methods , 2001, Numer. Linear Algebra Appl..

[13]  N. Logothetis The neural basis of the blood-oxygen-level-dependent functional magnetic resonance imaging signal. , 2002, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[14]  Bijan Pesaran,et al.  Temporal structure in neuronal activity during working memory in macaque parietal cortex , 2000, Nature Neuroscience.

[15]  J. Csicsvari,et al.  Mechanisms of Gamma Oscillations in the Hippocampus of the Behaving Rat , 2003, Neuron.

[16]  C. Mehring,et al.  Inference of hand movements from local field potentials in monkey motor cortex , 2003, Nature Neuroscience.

[17]  C. Bédard,et al.  Modeling extracellular field potentials and the frequency-filtering properties of extracellular space. , 2003, Biophysical journal.

[18]  R. Andersen,et al.  Selecting the signals for a brain–machine interface , 2004, Current Opinion in Neurobiology.

[19]  Christof Koch,et al.  Electrical Interactions via the Extracellular Potential Near Cell Bodies , 1999, Journal of Computational Neuroscience.

[20]  S. Bressler,et al.  Beta oscillations in a large-scale sensorimotor cortical network: directional influences revealed by Granger causality. , 2004, Proceedings of the National Academy of Sciences of the United States of America.

[21]  P. König,et al.  A comparison of hemodynamic and neural responses in cat visual cortex using complex stimuli. , 2004, Cerebral cortex.

[22]  Evgueniy V. Lubenov,et al.  Prefrontal Phase Locking to Hippocampal Theta Oscillations , 2005, Neuron.

[23]  I. Fried,et al.  Coupling Between Neuronal Firing, Field Potentials, and fMRI in Human Auditory Cortex , 2005, Science.

[24]  Hualou Liang,et al.  Causal influence: advances in neurosignal analysis. , 2005, Critical reviews in biomedical engineering.

[25]  S. Bressler,et al.  Granger Causality: Basic Theory and Application to Neuroscience , 2006, q-bio/0608035.

[26]  S. Bressler,et al.  Frequency decomposition of conditional Granger causality and application to multivariate neural field potential data , 2006, Journal of Neuroscience Methods.

[27]  C. Gilbert,et al.  Contour Saliency in Primary Visual Cortex , 2006, Neuron.

[28]  C. Koch,et al.  On the origin of the extracellular action potential waveform: A modeling study. , 2006, Journal of neurophysiology.

[29]  W. Newsome,et al.  Local Field Potential in Cortical Area MT: Stimulus Tuning and Behavioral Correlations , 2006, The Journal of Neuroscience.

[30]  T. Poggio,et al.  Object Selectivity of Local Field Potentials and Spikes in the Macaque Inferior Temporal Cortex , 2006, Neuron.

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

[32]  Mingzhou Ding,et al.  Estimating Granger causality from fourier and wavelet transforms of time series data. , 2007, Physical review letters.

[33]  Arthur Gretton,et al.  Low-Frequency Local Field Potentials and Spikes in Primary Visual Cortex Convey Independent Visual Information , 2008, The Journal of Neuroscience.

[34]  Sean M Montgomery,et al.  Entrainment of Neocortical Neurons and Gamma Oscillations by the Hippocampal Theta Rhythm , 2008, Neuron.

[35]  Daniele Marinazzo,et al.  Kernel method for nonlinear granger causality. , 2007, Physical review letters.

[36]  Bijan Pesaran,et al.  Free choice activates a decision circuit between frontal and parietal cortex , 2008, Nature.

[37]  Arthur Gretton,et al.  Inferring spike trains from local field potentials. , 2008, Journal of neurophysiology.

[38]  Mingzhou Ding,et al.  Analyzing multiple spike trains with nonparametric granger causality , 2009, Journal of Computational Neuroscience.

[39]  M. Carandini,et al.  Local Origin of Field Potentials in Visual Cortex , 2009, Neuron.

[40]  M. Carandini,et al.  Stimulus contrast modulates functional connectivity in visual cortex , 2009, Nature Neuroscience.

[41]  T. Hafting,et al.  Frequency of gamma oscillations routes flow of information in the hippocampus , 2009, Nature.

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

[43]  R. Desimone,et al.  High-Frequency, Long-Range Coupling Between Prefrontal and Visual Cortex During Attention , 2009, Science.

[44]  Jeremy R. Manning,et al.  Broadband Shifts in Local Field Potential Power Spectra Are Correlated with Single-Neuron Spiking in Humans , 2009, The Journal of Neuroscience.

[45]  Shy Shoham,et al.  Multivariate Autoregressive Modeling and Granger Causality Analysis of Multiple Spike Trains , 2010, Comput. Intell. Neurosci..

[46]  K. Koepsell,et al.  Oscillatory phase coupling coordinates anatomically dispersed functional cell assemblies , 2010, Proceedings of the National Academy of Sciences.

[47]  Louise S. Delicato,et al.  Attention Reduces Stimulus-Driven Gamma Frequency Oscillations and Spike Field Coherence in V1 , 2010, Neuron.

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

[49]  Martin Vinck,et al.  The pairwise phase consistency: A bias-free measure of rhythmic neuronal synchronization , 2010, NeuroImage.

[50]  Martin Vinck,et al.  Improved measures of phase-coupling between spikes and the Local Field Potential , 2011, Journal of Computational Neuroscience.

[51]  A. Riehle,et al.  The Local Field Potential Reflects Surplus Spike Synchrony , 2010, Cerebral cortex.

[52]  Steven L. Bressler,et al.  Wiener–Granger Causality: A well established methodology , 2011, NeuroImage.

[53]  Valentin Dragoi,et al.  Adaptation-induced synchronization in laminar cortical circuits , 2011, Proceedings of the National Academy of Sciences.

[54]  Emery N. Brown,et al.  A Granger Causality Measure for Point Process Models of Ensemble Neural Spiking Activity , 2011, PLoS Comput. Biol..

[55]  Mark D Humphries,et al.  Spike-Train Communities: Finding Groups of Similar Spike Trains , 2011, The Journal of Neuroscience.

[56]  C. Schroeder,et al.  How Local Is the Local Field Potential? , 2011, Neuron.

[57]  Klas H. Pettersen,et al.  Modeling the Spatial Reach of the LFP , 2011, Neuron.

[58]  Mark A. Kramer,et al.  The Dependence of Spike Field Coherence on Expected Intensity , 2011, Neural Computation.

[59]  J. Alonso,et al.  Population receptive fields of ON and OFF thalamic inputs to an orientation column in visual cortex , 2011, Nature Neuroscience.

[60]  Guifen Chen,et al.  Hippocampal theta‐driving cells revealed by Granger causality , 2012, Hippocampus.

[61]  Gregor M. Hörzer,et al.  Theta coupling between V4 and prefrontal cortex predicts visual short-term memory performance , 2012, Nature Neuroscience.

[62]  Asohan Amarasingham,et al.  Conditional modeling and the jitter method of spike resampling. , 2012, Journal of neurophysiology.

[63]  C. Koch,et al.  The origin of extracellular fields and currents — EEG, ECoG, LFP and spikes , 2012, Nature Reviews Neuroscience.

[64]  Y. Saalmann,et al.  The Pulvinar Regulates Information Transmission Between Cortical Areas Based on Attention Demands , 2012, Science.

[65]  Mark A. Kramer,et al.  A procedure for testing across-condition rhythmic spike-field association change , 2012, Journal of Neuroscience Methods.

[66]  Stefano Panzeri,et al.  Modelling and analysis of local field potentials for studying the function of cortical circuits , 2013, Nature Reviews Neuroscience.

[67]  C. Gilbert,et al.  Top-Down Modulation of Lateral Interactions in Visual Cortex , 2013, The Journal of Neuroscience.

[68]  Y. Miyashita,et al.  Functional Microcircuit Recruited during Retrieval of Object Association Memory in Monkey Perirhinal Cortex , 2013, Neuron.

[69]  Hualou Liang,et al.  A copula approach to assessing Granger causality , 2014, NeuroImage.

[70]  Daniele Marinazzo,et al.  Synergy and redundancy in the Granger causal analysis of dynamical networks , 2014, New Journal of Physics.

[71]  Hualou Liang,et al.  Incremental Integration of Global Contours through Interplay between Visual Cortical Areas , 2014, Neuron.

[72]  M. Ding,et al.  Theta-rhythmic drive between medial septum and hippocampus in slow-wave sleep and microarousal: a Granger causality analysis. , 2015, Journal of neurophysiology.

[73]  A. Seth,et al.  Granger Causality Analysis in Neuroscience and Neuroimaging , 2015, The Journal of Neuroscience.

[74]  Kelsey L. Clark,et al.  Copula Regression Analysis of Simultaneously Recorded Frontal Eye Field and Inferotemporal Spiking Activity during Object-Based Working Memory , 2015, The Journal of Neuroscience.

[75]  A. Seth,et al.  Granger causality for state-space models. , 2015, Physical review. E, Statistical, nonlinear, and soft matter physics.

[76]  Hualou Liang,et al.  Synergistic Processing of Visual Contours across Cortical Layers in V1 and V2 , 2017, Neuron.

[77]  C. Gilbert,et al.  Interactions between feedback and lateral connections in the primary visual cortex , 2017, Proceedings of the National Academy of Sciences.

[78]  L. Faes,et al.  Multiscale Granger causality. , 2017, Physical review. E.

[79]  Luca Faes,et al.  On the interpretability and computational reliability of frequency-domain Granger causality , 2017, F1000Research.

[80]  Mikhail Prokopenko,et al.  Transfer entropy in continuous time, with applications to jump and neural spiking processes , 2016, Physical review. E.

[81]  Robin A. A. Ince Measuring multivariate redundant information with pointwise common change in surprisal , 2016, Entropy.

[82]  Bijan Pesaran,et al.  Investigating large-scale brain dynamics using field potential recordings: analysis and interpretation , 2018, Nature Neuroscience.

[83]  Anil K. Seth,et al.  Solved problems for Granger causality in neuroscience: A response to Stokes and Purdon , 2018, NeuroImage.

[84]  Hualou Liang,et al.  Granger-Geweke causality: Estimation and interpretation , 2018, NeuroImage.

[85]  Hualou Liang,et al.  A Copula-Based Granger Causality Measure for the Analysis of Neural Spike Train Data , 2018, IEEE/ACM Transactions on Computational Biology and Bioinformatics.