Characterization of network structure in stereoEEG data using consensus-based partial coherence

&NA; Coherence is a widely used measure to determine the frequency‐resolved functional connectivity between pairs of recording sites, but this measure is confounded by shared inputs to the pair. To remove shared inputs, the ‘partial coherence’ can be computed by conditioning the spectral matrices of the pair on all other recorded channels, which involves the calculation of a matrix (pseudo‐) inverse. It has so far remained a challenge to use the time‐resolved partial coherence to analyze intracranial recordings with a large number of recording sites. For instance, calculating the partial coherence using a pseudoinverse method produces a high number of false positives when it is applied to a large number of channels. To address this challenge, we developed a new method that randomly aggregated channels into a smaller number of effective channels on which the calculation of partial coherence was based. We obtained a ‘consensus’ partial coherence (cPCOH) by repeating this approach for several random aggregations of channels (permutations) and only accepting those activations in time and frequency with a high enough consensus. Using model data we show that the cPCOH method effectively filters out the effect of shared inputs and performs substantially better than the pseudo‐inverse. We successfully applied the cPCOH procedure to human stereotactic EEG data and demonstrated three key advantages of this method relative to alternative procedures. First, it reduces the number of false positives relative to the pseudo‐inverse method. Second, it allows for titration of the amount of false positives relative to the false negatives by adjusting the consensus threshold, thus allowing the data‐analyst to prioritize one over the other to meet specific analysis demands. Third, it substantially reduced the number of identified interactions compared to coherence, providing a sparser network of connections from which clear spatial patterns emerged. These patterns can serve as a starting point of further analyses that provide insight into network dynamics during cognitive processes. These advantages likely generalize to other modalities in which shared inputs introduce confounds, such as electroencephalography (EEG) and magneto‐encephalography (MEG). Graphical abstract Figure. No caption available. HighlightsA consensus‐based implementation for partial coherence (cPCOH) analysis is proposed.cPCOH is applicable to datasets with many recording sites and few trials.cPCOH outperforms standard partial coherence with fewer false positives.cPCOH reduces the number of time‐frequency blobs, yielding sparser networks.

[1]  William H. Press,et al.  Numerical recipes , 1990 .

[2]  Karl J. Friston,et al.  False discovery rate revisited: FDR and topological inference using Gaussian random fields , 2009, NeuroImage.

[3]  Paul H. E. Tiesinga,et al.  Top-down control of cortical gamma-band communication via pulvinar induced phase shifts in the alpha rhythm , 2017, PLoS Comput. Biol..

[4]  Jim Kay,et al.  Partial information decomposition as a unified approach to the specification of neural goal functions , 2015, Brain and Cognition.

[5]  S. Cerutti,et al.  Total and partial coherence analysis of spontaneous and evoked EEG by means of multi-variable autoregressive processing , 1997, Medical and Biological Engineering and Computing.

[6]  David M. W. Powers,et al.  Evaluation: from precision, recall and F-measure to ROC, informedness, markedness and correlation , 2011, ArXiv.

[7]  F. Varela,et al.  Measuring phase synchrony in brain signals , 1999, Human brain mapping.

[8]  Karl J. Friston,et al.  Assessing the significance of focal activations using their spatial extent , 1994, Human brain mapping.

[9]  Fred Wolf,et al.  Flexible information routing by transient synchrony , 2017, Nature Neuroscience.

[10]  Giuseppe Casaceli,et al.  Four-dimensional maps of the human somatosensory system , 2016, Proceedings of the National Academy of Sciences.

[11]  J. R. Rosenberg,et al.  Identification of patterns of neuronal connectivity—partial spectra, partial coherence, and neuronal interactions , 1998, Journal of Neuroscience Methods.

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

[13]  P. Fries,et al.  Robust Gamma Coherence between Macaque V1 and V2 by Dynamic Frequency Matching , 2013, Neuron.

[14]  Vangelis Sakkalis,et al.  Review of advanced techniques for the estimation of brain connectivity measured with EEG/MEG , 2011, Comput. Biol. Medicine.

[15]  A. T. Walden,et al.  Graphical modelling for brain connectivity via partial coherence , 2009, Journal of Neuroscience Methods.

[16]  M. Scanziani,et al.  Instantaneous Modulation of Gamma Oscillation Frequency by Balancing Excitation with Inhibition , 2009, Neuron.

[17]  C. Munari,et al.  Stereo‐electroencephalography methodology: advantages and limits , 1994, Acta neurologica Scandinavica. Supplementum.

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

[19]  Eric L. Denovellis,et al.  Synchronous Oscillatory Neural Ensembles for Rules in the Prefrontal Cortex , 2012, Neuron.

[20]  J. Maunsell,et al.  Differences in Gamma Frequencies across Visual Cortex Restrict Their Possible Use in Computation , 2010, Neuron.

[21]  Hanan Samet,et al.  A general approach to connected-component labeling for arbitrary image representations , 1992, JACM.

[22]  Peter A. Flach The Geometry of ROC Space: Understanding Machine Learning Metrics through ROC Isometrics , 2003, ICML.

[23]  G Rizzolatti,et al.  Decomposing Tool-Action Observation: A Stereo-EEG Study , 2017, Cerebral cortex.

[24]  G. Buzsáki,et al.  Interdependence of Multiple Theta Generators in the Hippocampus: a Partial Coherence Analysis , 1999, The Journal of Neuroscience.

[25]  Ned T. Sahin,et al.  Dynamic circuit motifs underlying rhythmic gain control, gating and integration , 2014, Nature Neuroscience.

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

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

[28]  J. R. Rosenberg,et al.  The Fourier approach to the identification of functional coupling between neuronal spike trains. , 1989, Progress in biophysics and molecular biology.

[29]  Jianfeng Feng,et al.  Is partial coherence a viable technique for identifying generators of neural oscillations? , 2004, Biological Cybernetics.

[30]  H. Kennedy,et al.  Visual Areas Exert Feedforward and Feedback Influences through Distinct Frequency Channels , 2014, Neuron.

[31]  Robert Oostenveld,et al.  FieldTrip: Open Source Software for Advanced Analysis of MEG, EEG, and Invasive Electrophysiological Data , 2010, Comput. Intell. Neurosci..

[32]  J. Palva,et al.  Discovering oscillatory interaction networks with M/EEG: challenges and breakthroughs , 2012, Trends in Cognitive Sciences.

[33]  P. Roelfsema,et al.  Alpha and gamma oscillations characterize feedback and feedforward processing in monkey visual cortex , 2014, Proceedings of the National Academy of Sciences.

[34]  W. Press,et al.  Numerical Recipes: The Art of Scientific Computing , 1987 .

[35]  David Rudrauf,et al.  Estimating the time-course of coherence between single-trial brain signals: an introduction to wavelet coherence , 2002, Neurophysiologie Clinique/Clinical Neurophysiology.

[36]  H. Edelsbrunner,et al.  Efficient algorithms for agglomerative hierarchical clustering methods , 1984 .

[37]  Joël M. H. Karel,et al.  Quantifying Neural Oscillatory Synchronization: A Comparison between Spectral Coherence and Phase-Locking Value Approaches , 2016, PloS one.

[38]  Gregor Thut,et al.  Lip movements entrain the observers’ low-frequency brain oscillations to facilitate speech intelligibility , 2016, eLife.

[39]  Stephen M. Smith,et al.  A global optimisation method for robust affine registration of brain images , 2001, Medical Image Anal..

[40]  John-Stuart Brittain,et al.  Single-Trial Multiwavelet Coherence in Application to Neurophysiological Time Series , 2007, IEEE Transactions on Biomedical Engineering.

[41]  Mark W. Woolrich,et al.  Measuring functional connectivity in MEG: A multivariate approach insensitive to linear source leakage , 2012, NeuroImage.

[42]  Byron M. Yu,et al.  Dimensionality reduction for large-scale neural recordings , 2014, Nature Neuroscience.

[43]  F. H. Lopes da Silva,et al.  Relative contributions of intracortical and thalamo-cortical processes in the generation of alpha rhythms, revealed by partial coherence analysis. , 1980, Electroencephalography and clinical neurophysiology.

[44]  Jan-Mathijs Schoffelen,et al.  A Tutorial Review of Functional Connectivity Analysis Methods and Their Interpretational Pitfalls , 2016, Front. Syst. Neurosci..

[45]  Paul H. E. Tiesinga,et al.  Phase Difference between Model Cortical Areas Determines Level of Information Transfer , 2017, Front. Comput. Neurosci..

[46]  T. Womelsdorf,et al.  Attentional Stimulus Selection through Selective Synchronization between Monkey Visual Areas , 2012, Neuron.

[47]  Peter A. Flach,et al.  A Unified View of Performance Metrics: Translating Threshold Choice into Expected Classification Loss C` Esar Ferri , 2012 .

[48]  Francesco Cardinale,et al.  Stereoelectroencephalography in the Presurgical Evaluation of Focal Epilepsy: A Retrospective Analysis of 215 Procedures , 2005, Neurosurgery.

[49]  Conrado A. Bosman,et al.  How to detect the Granger-causal flow direction in the presence of additive noise? , 2015, NeuroImage.

[50]  Henry Kennedy,et al.  Cortical High-Density Counterstream Architectures , 2013, Science.

[51]  Rodrigo Quian Quiroga,et al.  Nonlinear multivariate analysis of neurophysiological signals , 2005, Progress in Neurobiology.

[52]  E. Bullmore,et al.  Undirected graphs of frequency-dependent functional connectivity in whole brain networks , 2005, Philosophical Transactions of the Royal Society B: Biological Sciences.

[53]  Peter De Weerd,et al.  A quantitative theory of gamma synchronization in macaque V1 , 2017, eLife.

[54]  Zoltán Toroczkai,et al.  The role of long-range connections on the specificity of the macaque interareal cortical network , 2013, Proceedings of the National Academy of Sciences.

[55]  W. Gersch,et al.  Epileptic Focus Location: Spectral Analysis Method , 1970, Science.

[56]  R. Oostenveld,et al.  Nonparametric statistical testing of EEG- and MEG-data , 2007, Journal of Neuroscience Methods.

[57]  P. Fries Rhythms for Cognition: Communication through Coherence , 2015, Neuron.

[58]  Bernhard Schölkopf,et al.  Shifts of Gamma Phase across Primary Visual Cortical Sites Reflect Dynamic Stimulus-Modulated Information Transfer , 2015, PLoS biology.

[59]  Y. Benjamini,et al.  Controlling the false discovery rate: a practical and powerful approach to multiple testing , 1995 .

[60]  Lee M. Miller,et al.  Measuring interregional functional connectivity using coherence and partial coherence analyses of fMRI data , 2004, NeuroImage.

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

[62]  Daniele Marinazzo,et al.  Causal Information Approach to Partial Conditioning in Multivariate Data Sets , 2011, Comput. Math. Methods Medicine.

[63]  Mark W. Woolrich,et al.  A symmetric multivariate leakage correction for MEG connectomes , 2015, NeuroImage.

[64]  J. Schoffelen,et al.  Comparing spectra and coherences for groups of unequal size , 2007, Journal of Neuroscience Methods.