The influence of filtering and downsampling on the estimation of transfer entropy

Transfer entropy (TE) provides a generalized and model-free framework to study Wiener-Granger causality between brain regions. Because of its nonparametric character, TE can infer directed information flow also from nonlinear systems. Despite its increasing number of applications in neuroscience, not much is known regarding the influence of common electrophysiological preprocessing on its estimation. We test the influence of filtering and downsampling on a recently proposed nearest neighborhood based TE estimator. Different filter settings and downsampling factors were tested in a simulation framework using a model with a linear coupling function and two nonlinear models with sigmoid and logistic coupling functions. For nonlinear coupling and progressively lower low-pass filter cut-off frequencies up to 72% false negative direct connections and up to 26% false positive connections were identified. In contrast, for the linear model, a monotonic increase was only observed for missed indirect connections (up to 86%). High-pass filtering (1 Hz, 2 Hz) had no impact on TE estimation. After low-pass filtering interaction delays were significantly underestimated. Downsampling the data by a factor greater than the assumed interaction delay erased most of the transmitted information and thus led to a very high percentage (67–100%) of false negative direct connections. Low-pass filtering increases the number of missed connections depending on the filters cut-off frequency. Downsampling should only be done if the sampling factor is smaller than the smallest assumed interaction delay of the analyzed network.

[1]  M. G. Kendall,et al.  A Study in the Analysis of Stationary Time-Series. , 1955 .

[2]  B L Finlay,et al.  Quantitative studies of single-cell properties in monkey striate cortex. IV. Corticotectal cells. , 1976, Journal of neurophysiology.

[3]  Robert M. May,et al.  Simple mathematical models with very complicated dynamics , 1976, Nature.

[4]  F. Takens Detecting strange attractors in turbulence , 1981 .

[5]  Koichi Sameshima,et al.  Using partial directed coherence to describe neuronal ensemble interactions , 1999, Journal of Neuroscience Methods.

[6]  Schreiber,et al.  Measuring information transfer , 2000, Physical review letters.

[7]  L. Glass Synchronization and rhythmic processes in physiology , 2001, Nature.

[8]  C. Granger Investigating causal relations by econometric models and cross-spectral methods , 1969 .

[9]  Jürgen Kurths,et al.  Synchronization - A Universal Concept in Nonlinear Sciences , 2001, Cambridge Nonlinear Science Series.

[10]  J. Martinerie,et al.  The brainweb: Phase synchronization and large-scale integration , 2001, Nature Reviews Neuroscience.

[11]  Jürgen Kurths,et al.  Synchronization: Phase locking and frequency entrainment , 2001 .

[12]  Norman R. Swanson,et al.  Temporal aggregation and spurious instantaneous causality in multiple time series models , 2002 .

[13]  H. Kantz,et al.  Analysing the information flow between financial time series , 2002 .

[14]  Mario Ragwitz,et al.  Markov models from data by simple nonlinear time series predictors in delay embedding spaces. , 2002, Physical review. E, Statistical, nonlinear, and soft matter physics.

[15]  R. Wurtz,et al.  Comparison of cortico-cortical and cortico-collicular signals for the generation of saccadic eye movements. , 2002, Journal of neurophysiology.

[16]  J. Martinerie,et al.  Statistical assessment of nonlinear causality: application to epileptic EEG signals , 2003, Journal of Neuroscience Methods.

[17]  Philippe Faure,et al.  Is there chaos in the brain? II. Experimental evidence and related models. , 2003, Comptes rendus biologies.

[18]  H. Swadlow,et al.  Characteristics of interhemispheric impulse conduction between prelunate gyri of the rhesus monkey , 1978, Experimental Brain Research.

[19]  A. Kraskov,et al.  Estimating mutual information. , 2003, Physical review. E, Statistical, nonlinear, and soft matter physics.

[20]  Katarzyna J. Blinowska,et al.  Determination of EEG activity propagation: pair-wise versus multichannel estimate , 2004, IEEE Transactions on Biomedical Engineering.

[21]  A Kraskov,et al.  Synchronization and Interdependence Measures and their Applications to the Electroencephalogram of Epilepsy Patients and Clustering of Data (PhD Thesis) , 2004 .

[22]  C. Stam,et al.  Nonlinear dynamical analysis of EEG and MEG: Review of an emerging field , 2005, Clinical Neurophysiology.

[23]  Sang Joon Kim,et al.  A Mathematical Theory of Communication , 2006 .

[24]  G Perea,et al.  EEG-like signals generated by a simple chaotic model based on the logistic equation , 2006, Journal of neural engineering.

[25]  Boris Gourévitch,et al.  Evaluating information transfer between auditory cortical neurons. , 2007, Journal of neurophysiology.

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

[27]  O. Sporns,et al.  Dynamical consequences of lesions in cortical networks , 2008, Human brain mapping.

[28]  Matthäus Staniek,et al.  Symbolic transfer entropy. , 2008, Physical review letters.

[29]  A. Engel,et al.  Is the synchronization between pallidal and muscle activity in primary dystonia due to peripheral afferance or a motor drive? , 2008, Brain : a journal of neurology.

[30]  Nabil H. Farhat,et al.  Self-Organization in a Parametrically Coupled Logistic Map Network: A Model for Information Processing in the Visual Cortex , 2009, IEEE Transactions on Neural Networks.

[31]  A. Seth,et al.  Granger causality and transfer entropy are equivalent for Gaussian variables. , 2009, Physical review letters.

[32]  Joachim Gross,et al.  The effect of filtering on Granger causality based multivariate causality measures , 2010, NeuroImage.

[33]  K. Meador,et al.  Theta oscillations mediate interaction between prefrontal cortex and medial temporal lobe in human memory. , 2010, Cerebral cortex.

[34]  Andrzej Cichocki,et al.  A comparative study of synchrony measures for the early diagnosis of Alzheimer's disease based on EEG , 2010, NeuroImage.

[35]  Gordon Pipa,et al.  Transfer entropy—a model-free measure of effective connectivity for the neurosciences , 2010, Journal of Computational Neuroscience.

[36]  H. Freund,et al.  The causal relationship between subcortical local field potential oscillations and Parkinsonian resting tremor , 2010, Journal of neural engineering.

[37]  Joachim Gross,et al.  Causality between local field potentials of the subthalamic nucleus and electromyograms of forearm muscles in Parkinson’s disease , 2010, The European journal of neuroscience.

[38]  Stephan Moratti,et al.  Prefrontal-Occipitoparietal Coupling Underlies Late Latency Human Neuronal Responses to Emotion , 2011, The Journal of Neuroscience.

[39]  Jochen Kaiser,et al.  Transfer entropy in magnetoencephalographic data: quantifying information flow in cortical and cerebellar networks. , 2011, Progress in biophysics and molecular biology.

[40]  Viola Priesemann,et al.  TRENTOOL: A Matlab open source toolbox to analyse information flow in time series data with transfer entropy , 2011, BMC Neuroscience.

[41]  S. Pethel,et al.  Distinguishing anticipation from causality: anticipatory bias in the estimation of information flow. , 2011, Physical review letters.

[42]  Klaus Lehnertz,et al.  Inferring directional interactions from transient signals with symbolic transfer entropy. , 2011, Physical review. E, Statistical, nonlinear, and soft matter physics.

[43]  A. Seth,et al.  Behaviour of Granger causality under filtering: Theoretical invariance and practical application , 2011, Journal of Neuroscience Methods.

[44]  John M. Beggs,et al.  Extending Transfer Entropy Improves Identification of Effective Connectivity in a Spiking Cortical Network Model , 2011, PloS one.

[45]  Ulrich Meyer,et al.  Revisiting Wiener's principle of causality — interaction-delay reconstruction using transfer entropy and multivariate analysis on delay-weighted graphs , 2012, 2012 Annual International Conference of the IEEE Engineering in Medicine and Biology Society.

[46]  J. A. Scott Kelso,et al.  Multistability and metastability: understanding dynamic coordination in the brain , 2012, Philosophical Transactions of the Royal Society B: Biological Sciences.

[47]  Albert Y. Zomaya,et al.  Local measures of information storage in complex distributed computation , 2012, Inf. Sci..

[48]  Chaofei Ma,et al.  Estimating causal interaction between prefrontal cortex and striatum by transfer entropy , 2013, Cognitive Neurodynamics.

[49]  D. Smirnov,et al.  Spurious causalities due to low temporal resolution: Towards detection of bidirectional coupling from time series , 2012 .

[50]  Annette Witt,et al.  Dynamic Effective Connectivity of Inter-Areal Brain Circuits , 2011, PLoS Comput. Biol..

[51]  Dimitris Kugiumtzis,et al.  Direct coupling information measure from non-uniform embedding , 2013, Physical review. E, Statistical, nonlinear, and soft matter physics.

[52]  Dmitry A Smirnov,et al.  Spurious causalities with transfer entropy. , 2013, Physical review. E, Statistical, nonlinear, and soft matter physics.

[53]  Dante R Chialvo,et al.  Disruption of transfer entropy and inter-hemispheric brain functional connectivity in patients with disorder of consciousness , 2013, Front. Neuroinform..

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

[55]  Viola Priesemann,et al.  Measuring Information-Transfer Delays , 2013, PloS one.

[56]  Piotr J. Franaszczuk,et al.  Ictal propagation of high frequency activity is recapitulated in interictal recordings: Effective connectivity of epileptogenic networks recorded with intracranial EEG , 2014, NeuroImage.

[57]  Wayne Luk,et al.  Accelerating transfer entropy computation , 2014, 2014 International Conference on Field-Programmable Technology (FPT).

[58]  Luca Faes,et al.  MuTE: A MATLAB Toolbox to Compare Established and Novel Estimators of the Multivariate Transfer Entropy , 2014, PloS one.

[59]  Klaus Lehnertz,et al.  Identifying delayed directional couplings with symbolic transfer entropy. , 2014, Physical review. E, Statistical, nonlinear, and soft matter physics.

[60]  Constantinos I. Siettos,et al.  Granger causality analysis reveals distinct spatio-temporal connectivity patterns in motor and perceptual visuo-spatial working memory , 2014, Front. Comput. Neurosci..

[61]  Henrik Jeldtoft Jensen,et al.  Quantifying ‘Causality’ in Complex Systems: Understanding Transfer Entropy , 2013, PloS one.

[62]  Frank Huethe,et al.  Enhanced corticomuscular coherence by external stochastic noise , 2014, Front. Hum. Neurosci..

[63]  Carmen C Canavier,et al.  Phase-resetting as a tool of information transmission , 2015, Current Opinion in Neurobiology.

[64]  Luca Faes,et al.  Neural networks with non-uniform embedding and explicit validation phase to assess Granger causality , 2015, Neural Networks.

[65]  Chin-Teng Lin,et al.  Identifying changes in EEG information transfer during drowsy driving by transfer entropy , 2015, Front. Hum. Neurosci..

[66]  Nikolaus Kriegeskorte,et al.  Deep neural networks: a new framework for modelling biological vision and brain information processing , 2015, bioRxiv.

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

[68]  K. Hamacher,et al.  Efficient computation and statistical assessment of transfer entropy , 2015, Front. Phys..

[69]  Ichiro Tsuda,et al.  Chaotic itinerancy and its roles in cognitive neurodynamics , 2015, Current Opinion in Neurobiology.

[70]  Victor Solo,et al.  State-Space Analysis of Granger-Geweke Causality Measures with Application to fMRI , 2016, Neural Computation.

[71]  Mukesh Dhamala,et al.  The salience network dynamics in perceptual decision-making , 2016, NeuroImage.

[72]  Cynthia A. Chestek,et al.  Disruption of corticocortical information transfer during ketamine anesthesia in the primate brain , 2016, NeuroImage.

[73]  Anil K. Seth,et al.  Detectability of Granger causality for subsampled continuous-time neurophysiological processes , 2016, Journal of Neuroscience Methods.