Efficient Transfer Entropy Analysis of Non-Stationary Neural Time Series

Information theory allows us to investigate information processing in neural systems in terms of information transfer, storage and modification. Especially the measure of information transfer, transfer entropy, has seen a dramatic surge of interest in neuroscience. Estimating transfer entropy from two processes requires the observation of multiple realizations of these processes to estimate associated probability density functions. To obtain these necessary observations, available estimators typically assume stationarity of processes to allow pooling of observations over time. This assumption however, is a major obstacle to the application of these estimators in neuroscience as observed processes are often non-stationary. As a solution, Gomez-Herrero and colleagues theoretically showed that the stationarity assumption may be avoided by estimating transfer entropy from an ensemble of realizations. Such an ensemble of realizations is often readily available in neuroscience experiments in the form of experimental trials. Thus, in this work we combine the ensemble method with a recently proposed transfer entropy estimator to make transfer entropy estimation applicable to non-stationary time series. We present an efficient implementation of the approach that is suitable for the increased computational demand of the ensemble method's practical application. In particular, we use a massively parallel implementation for a graphics processing unit to handle the computationally most heavy aspects of the ensemble method for transfer entropy estimation. We test the performance and robustness of our implementation on data from numerical simulations of stochastic processes. We also demonstrate the applicability of the ensemble method to magnetoencephalographic data. While we mainly evaluate the proposed method for neuroscience data, we expect it to be applicable in a variety of fields that are concerned with the analysis of information transfer in complex biological, social, and artificial systems.

[1]  Roberto Hornero,et al.  Cross-Approximate Entropy parallel computation on GPUs for biomedical signal analysis. Application to MEG recordings , 2013, Comput. Methods Programs Biomed..

[2]  Patrick Cavanagh,et al.  What's up in top-down processing? , 1991 .

[3]  Manuel Schabus,et al.  Phase-locked alpha and theta oscillations generate the P1-N1 complex and are related to memory performance. , 2004, Brain research. Cognitive brain research.

[4]  Joseph T. Lizier,et al.  Measuring the Dynamics of Information Processing on a Local Scale in Time and Space , 2014 .

[5]  W. Singer,et al.  The Phase of Thalamic Alpha Activity Modulates Cortical Gamma-Band Activity: Evidence from Resting-State MEG Recordings , 2013, The Journal of Neuroscience.

[6]  Proceedings of the London Mathematical Society , 1877, Nature.

[7]  Viola Priesemann,et al.  Local active information storage as a tool to understand distributed neural information processing , 2013, Front. Neuroinform..

[8]  William W. Lytton,et al.  Synaptic information transfer in computer models of neocortical columns , 2011, Journal of Computational Neuroscience.

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

[10]  B. Jansen,et al.  Phase synchronization of the ongoing EEG and auditory EP generation , 2003, Clinical Neurophysiology.

[11]  B. MCA. SAVERS,et al.  The Mechanism of Auditory Evoked EEG Responses , 1974, Nature.

[12]  J. Victor Binless strategies for estimation of information from neural data. , 2002, Physical review. E, Statistical, nonlinear, and soft matter physics.

[13]  Randall D. Beer,et al.  Nonnegative Decomposition of Multivariate Information , 2010, ArXiv.

[14]  Lizhe Wang,et al.  Massively Parallel Neural Signal Processing on a Many-Core Platform , 2011, Computing in Science & Engineering.

[15]  Antonio Napolitano,et al.  Cyclostationarity: Half a century of research , 2006, Signal Process..

[16]  W. Klimesch,et al.  Are event-related potential components generated by phase resetting of brain oscillations? A critical discussion , 2007, Neuroscience.

[17]  Luca Faes,et al.  Compensated Transfer Entropy as a Tool for Reliably Estimating Information Transfer in Physiological Time Series , 2013, Entropy.

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

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

[20]  Eckehard Olbrich,et al.  Shared Information -- New Insights and Problems in Decomposing Information in Complex Systems , 2012, ArXiv.

[21]  A. N. Sharkovskiĭ Dynamic systems and turbulence , 1989 .

[22]  Matthew J. Brookes,et al.  Optimising experimental design for MEG beamformer imaging , 2008, NeuroImage.

[23]  Natasa Kovacevic,et al.  Exploring transient transfer entropy based on a group-wise ICA decomposition of EEG data , 2010, NeuroImage.

[24]  Nikos K Logothetis,et al.  Testing methodologies for the nonlinear analysis of causal relationships in neurovascular coupling. , 2010, Magnetic resonance imaging.

[25]  Mikhail Prokopenko,et al.  Differentiating information transfer and causal effect , 2008, 0812.4373.

[26]  M Palus,et al.  Synchronization as adjustment of information rates: detection from bivariate time series. , 2001, Physical review. E, Statistical, nonlinear, and soft matter physics.

[27]  J. Cremona,et al.  Proceedings of the London Mathematical Society , 1893 .

[28]  Daniel Polani,et al.  Information Flows in Causal Networks , 2008, Adv. Complex Syst..

[29]  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.

[30]  M Steinschneider,et al.  Localization of ERP generators and identification of underlying neural processes. , 1995, Electroencephalography and clinical neurophysiology. Supplement.

[31]  Albert Y. Zomaya,et al.  The local information dynamics of distributed computation in complex systems , 2012 .

[32]  L. Faes,et al.  Information-based detection of nonlinear Granger causality in multivariate processes via a nonuniform embedding technique. , 2011, Physical review. E, Statistical, nonlinear, and soft matter physics.

[33]  Sunil Arya,et al.  An optimal algorithm for approximate nearest neighbor searching fixed dimensions , 1998, JACM.

[34]  P. F. Verdes Assessing causality from multivariate time series. , 2005, Physical review. E, Statistical, nonlinear, and soft matter physics.

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

[36]  Joseph T. Lizier,et al.  Towards a synergy-based approach to measuring information modification , 2013, 2013 IEEE Symposium on Artificial Life (ALife).

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

[38]  Raul Vicente,et al.  Efficient Estimation of Information Transfer , 2014 .

[39]  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.

[40]  Ankoor S. Shah,et al.  Neural dynamics and the fundamental mechanisms of event-related brain potentials. , 2004, Cerebral cortex.

[41]  David G. Lowe,et al.  Fast Approximate Nearest Neighbors with Automatic Algorithm Configuration , 2009, VISAPP.

[42]  Jon Louis Bentley,et al.  Data Structures for Range Searching , 1979, CSUR.

[43]  John D. Owens,et al.  kANN on the GPU with shifted sorting , 2012, EGGH-HPG'12.

[44]  Dinesh Manocha,et al.  Bi-level Locality Sensitive Hashing for k-Nearest Neighbor Computation , 2012, 2012 IEEE 28th International Conference on Data Engineering.

[45]  Mooney Cm,et al.  A new closure test. , 1951 .

[46]  Christof Koch,et al.  Quantifying synergistic mutual information , 2012, ArXiv.

[47]  Luca Faes,et al.  Conditional Entropy-Based Evaluation of Information Dynamics in Physiological Systems , 2014 .

[48]  Barrie W. Jervis,et al.  A Fundamental Investigation of the Composition of Auditory Evoked Potentials , 1983, IEEE Transactions on Biomedical Engineering.

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

[50]  A. Ledberg,et al.  When two become one: the limits of causality analysis of brain dynamics. , 2012, PloS one.

[51]  Albert Y. Zomaya,et al.  Local information transfer as a spatiotemporal filter for complex systems. , 2008, Physical review. E, Statistical, nonlinear, and soft matter physics.

[52]  Panagiotis D. Bamidis,et al.  Real time emotion aware applications: A case study employing emotion evocative pictures and neuro-physiological sensing enhanced by Graphic Processor Units , 2012, Comput. Methods Programs Biomed..

[53]  Raul Vicente,et al.  Transfer Entropy in Neuroscience , 2014 .

[54]  Randall D. Beer,et al.  Generalized Measures of Information Transfer , 2011, ArXiv.

[55]  W. Singer,et al.  Neuroelectromagnetic Correlates of Perceptual Closure Processes , 2010, The Journal of Neuroscience.

[56]  Christoph Salge,et al.  A Bivariate Measure of Redundant Information , 2012, Physical review. E, Statistical, nonlinear, and soft matter physics.

[57]  T. Sejnowski,et al.  Dynamic Brain Sources of Visual Evoked Responses , 2002, Science.

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

[59]  Sungroh Yoon,et al.  Entropy-Based Analysis and Bioinformatics-Inspired Integration of Global Economic Information Transfer , 2013, PloS one.

[60]  Guy A. Orban,et al.  The Extraction of 3D Shape from Texture and Shading in the Human Brain , 2008, Cerebral cortex.

[61]  K. Nakayama,et al.  The effect of face inversion on the human fusiform face area , 1998, Cognition.

[62]  A. Turing On Computable Numbers, with an Application to the Entscheidungsproblem. , 1937 .

[63]  Melanie Mitchell,et al.  Computation in Cellular Automata: A Selected Review , 2005, Non-standard Computation.

[64]  F. Tong,et al.  The timing of perceptual decisions for ambiguous face stimuli in the human ventral visual cortex. , 2006, Cerebral cortex.

[65]  Anthony Randal McIntosh,et al.  Empirical and Theoretical Aspects of Generation and Transfer of Information in a Neuromagnetic Source Network , 2011, Front. Syst. Neurosci..

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

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

[68]  B. Pompe,et al.  Momentary information transfer as a coupling measure of time series. , 2011, Physical review. E, Statistical, nonlinear, and soft matter physics.

[69]  Parlitz,et al.  Fast nearest-neighbor searching for nonlinear signal processing , 2000, Physical review. E, Statistical physics, plasmas, fluids, and related interdisciplinary topics.

[70]  Albert Y. Zomaya,et al.  Information modification and particle collisions in distributed computation. , 2010, Chaos.

[71]  W. Hesse,et al.  The use of time-variant EEG Granger causality for inspecting directed interdependencies of neural assemblies , 2003, Journal of Neuroscience Methods.

[72]  Denis Schluppeck,et al.  Neural responses to Mooney images reveal a modular representation of faces in human visual cortex , 2004, NeuroImage.

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

[74]  Florentin Wörgötter,et al.  Information dynamics based self-adaptive reservoir for delay temporal memory tasks , 2013, Evol. Syst..

[75]  J. Kaiser,et al.  Decomposition of working memory-related scalp ERPs: crossvalidation of fMRI-constrained source analysis and ICA. , 2008, International journal of psychophysiology : official journal of the International Organization of Psychophysiology.

[76]  Jakob Heinzle,et al.  Multivariate information-theoretic measures reveal directed information structure and task relevant changes in fMRI connectivity , 2010, Journal of Computational Neuroscience.

[77]  Gordon Pipa,et al.  Assessing coupling dynamics from an ensemble of time series , 2010, Entropy.

[78]  Olivier J. J. Michel,et al.  On directed information theory and Granger causality graphs , 2010, Journal of Computational Neuroscience.

[79]  C. M. Mooney,et al.  A new closure test. , 1951, Canadian journal of psychology.

[80]  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.

[81]  Wolf Singer,et al.  Quantifying additive evoked contributions to the event-related potential , 2012, NeuroImage.

[82]  Eckehard Olbrich,et al.  Quantifying unique information , 2013, Entropy.

[83]  S. Makeig,et al.  Mining event-related brain dynamics , 2004, Trends in Cognitive Sciences.

[84]  Matthäus Staniek,et al.  Symbolic transfer entropy: inferring directionality in biosignals , 2009, Biomedizinische Technik. Biomedical engineering.

[85]  M. A. A. Barbosa,et al.  Entropy reduction effect imposed by hydrogen bond formation on protein folding cooperativity: evidence from a hydrophobic minimalist model. , 2005, Physical review. E, Statistical, nonlinear, and soft matter physics.

[86]  E. Halgren,et al.  Top-down facilitation of visual recognition. , 2006, Proceedings of the National Academy of Sciences of the United States of America.

[87]  Justin C. Williams,et al.  Massively Parallel Signal Processing using the Graphics Processing Unit for Real-Time Brain–Computer Interface Feature Extraction , 2009, Front. Neuroeng..

[88]  Okyu Kwon,et al.  Information flow between stock indices , 2008, 0802.1747.

[89]  Xiaobai Sun,et al.  Parallel search of k-nearest neighbors with synchronous operations , 2012, 2012 IEEE Conference on High Performance Extreme Computing.

[90]  Yongchao Liu,et al.  CUDA-MEME: Accelerating motif discovery in biological sequences using CUDA-enabled graphics processing units , 2010, Pattern Recognit. Lett..

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

[92]  G. G. Stokes "J." , 1890, The New Yale Book of Quotations.

[93]  George R. Mangun,et al.  Human Visual Evoked Potentials: Induced Rhythms or Separable Components? , 1992 .

[94]  廣瀬雄一,et al.  Neuroscience , 2019, Workplace Attachments.

[95]  M. Arnold,et al.  Instantaneous multivariate EEG coherence analysis by means of adaptive high-dimensional autoregressive models , 2001, Journal of Neuroscience Methods.

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

[97]  R. Rosenfeld Nature , 2009, Otolaryngology--head and neck surgery : official journal of American Academy of Otolaryngology-Head and Neck Surgery.

[98]  Gustavo Deco,et al.  Optimal Information Transfer in the Cortex through Synchronization , 2010, PLoS Comput. Biol..

[99]  Frank Nielsen,et al.  K-nearest neighbor search: Fast GPU-based implementations and application to high-dimensional feature matching , 2010, 2010 IEEE International Conference on Image Processing.

[100]  Regina Berretta,et al.  GPU-FS-kNN: A Software Tool for Fast and Scalable kNN Computation Using GPUs , 2012, PloS one.

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

[102]  Herbert Witte,et al.  Development of interaction measures based on adaptive non-linear time series analysis of biomedical signals / Entwicklung von Interaktionsmaßen auf der Grundlage adaptiver, nichtlinearer Zeitreihenanalyse von biomedizinischen Signalen , 2006, Biomedizinische Technik. Biomedical engineering.

[103]  John M. Findlay,et al.  Representations of Vision: Trends and Tacit Assumptions in Vision Research , 2009 .

[104]  Vasily A. Vakorin,et al.  Confounding effects of indirect connections on causality estimation , 2009, Journal of Neuroscience Methods.

[105]  Viola Priesemann,et al.  Transfer entropy as a tool for reconstructing interaction delays in neural signals , 2013, International Symposium on Signals, Circuits and Systems ISSCS2013.

[106]  J. Rogers Chaos , 1876 .

[107]  Sergio Martinoia,et al.  Evaluation of the Performance of Information Theory-Based Methods and Cross-Correlation to Estimate the Functional Connectivity in Cortical Networks , 2009, PloS one.

[108]  Luca Faes,et al.  Bivariate nonlinear prediction to quantify the strength of complex dynamical interactions in short-term cardiovascular variability , 2006, Medical and Biological Engineering and Computing.

[109]  Arthur W. Toga,et al.  CUDA optimization strategies for compute- and memory-bound neuroimaging algorithms , 2012, Comput. Methods Programs Biomed..

[110]  Daniele Marinazzo,et al.  Information Transfer in the Brain: Insights from a Unified Approach , 2014 .

[111]  Martin Lilleeng Sætra,et al.  Graphics processing unit (GPU) programming strategies and trends in GPU computing , 2013, J. Parallel Distributed Comput..

[112]  W Bialek,et al.  On the application of information theory to neural spike trains. , 1998, Pacific Symposium on Biocomputing. Pacific Symposium on Biocomputing.

[113]  Bernhard Schölkopf,et al.  Causal relationships between frequency bands of extracellular signals in visual cortex revealed by an information theoretic analysis , 2010, Journal of Computational Neuroscience.

[114]  W. Marsden I and J , 2012 .

[115]  A. Kraskov,et al.  Erratum: Estimating mutual information [Phys. Rev. E 69, 066138 (2004)] , 2011 .

[116]  Joseph T. Lizier,et al.  Multivariate construction of effective computational networks from observational data , 2012 .

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

[118]  Luca Faes,et al.  Non-uniform multivariate embedding to assess the information transfer in cardiovascular and cardiorespiratory variability series , 2012, Comput. Biol. Medicine.

[119]  K. Tsakalis,et al.  Information Flow and Application to Epileptogenic Focus Localization From Intracranial EEG , 2009, IEEE Transactions on Neural Systems and Rehabilitation Engineering.

[120]  Michael I. Ham,et al.  Functional structure of cortical neuronal networks grown in vitro. , 2007, Physical review. E, Statistical, nonlinear, and soft matter physics.

[121]  Christopher G. Langton,et al.  Computation at the edge of chaos: Phase transitions and emergent computation , 1990 .

[122]  Ralph G. Andrzejak,et al.  Detecting event-related time-dependent directional couplings , 2006 .

[123]  J Gross,et al.  REPRINTS , 1962, The Lancet.

[124]  正人 木村 Max-Planck-Institute for Mathematics in the Sciences(海外,ラボラトリーズ) , 2001 .

[125]  Joseph T. Lizier,et al.  Reduced predictable information in brain signals in autism spectrum disorder , 2014, Front. Neuroinform..

[126]  John D. Owens,et al.  GPU Computing , 2008, Proceedings of the IEEE.