A Data-Driven Measure of Effective Connectivity Based on Renyi's α-Entropy

Transfer entropy (TE) is a model-free effective connectivity measure based on information theory. It has been increasingly used in neuroscience because of its ability to detect unknown non-linear interactions, which makes it well suited for exploratory brain effective connectivity analyses. Like all information theoretic quantities, TE is defined regarding the probability distributions of the system under study, which in practice are unknown and must be estimated from data. Commonly used methods for TE estimation rely on a local approximation of the probability distributions from nearest neighbor distances, or on symbolization schemes that then allow the probabilities to be estimated from the symbols' relative frequencies. However, probability estimation is a challenging problem, and avoiding this intermediate step in TE computation is desirable. In this work, we propose a novel TE estimator using functionals defined on positive definite and infinitely divisible kernels matrices that approximate Renyi's entropy measures of order α. Our data-driven approach estimates TE directly from data, sidestepping the need for probability distribution estimation. Also, the proposed estimator encompasses the well-known definition of TE as a sum of Shannon entropies in the limiting case when α → 1. We tested our proposal on a simulation framework consisting of two linear models, based on autoregressive approaches and a linear coupling function, respectively, and on the public electroencephalogram (EEG) database BCI Competition IV, obtained under a motor imagery paradigm. For the synthetic data, the proposed kernel-based TE estimation method satisfactorily identifies the causal interactions present in the data. Also, it displays robustness to varying noise levels and data sizes, and to the presence of multiple interaction delays in the same connected network. Obtained results for the motor imagery task show that our approach codes discriminant spatiotemporal patterns for the left and right-hand motor imagination tasks, with classification performances that compare favorably to the state-of-the-art.

[1]  U. Rajendra Acharya,et al.  Application of entropies for automated diagnosis of epilepsy using EEG signals: A review , 2015, Knowl. Based Syst..

[2]  Xiaoli Li,et al.  EEG entropy measures in anesthesia , 2015, Front. Comput. Neurosci..

[3]  Michael Vourkas,et al.  A novel symbolization scheme for multichannel recordings with emphasis on phase information and its application to differentiate EEG activity from different mental tasks , 2011, Cognitive Neurodynamics.

[4]  Karl J. Friston Functional and Effective Connectivity: A Review , 2011, Brain Connect..

[5]  Kup-Sze Choi,et al.  Discrimination of motor imagery tasks via information flow pattern of brain connectivity. , 2016, Technology and health care : official journal of the European Society for Engineering and Medicine.

[6]  P. Jackson,et al.  The neural network of motor imagery: An ALE meta-analysis , 2013, Neuroscience & Biobehavioral Reviews.

[7]  L. Timmermann,et al.  The influence of filtering and downsampling on the estimation of transfer entropy , 2017, PloS one.

[8]  Germán Castellanos-Domínguez,et al.  Short Time EEG Connectivity Features to Support Interpretability of MI Discrimination , 2018, CIARP.

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

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

[11]  Francisco Javier Díaz Pernas,et al.  Efficient Transfer Entropy Analysis of Non-Stationary Neural Time Series , 2014, PloS one.

[12]  L. Baccalá,et al.  Methods in Brain Connectivity Inference through Multivariate Time Series Analysis , 2014 .

[13]  Nicholas M. Timme,et al.  A Tutorial for Information Theory in Neuroscience , 2018, eNeuro.

[14]  Nitish Thakor,et al.  Revealing Cross-Frequency Causal Interactions During a Mental Arithmetic Task Through Symbolic Transfer Entropy: A Novel Vector-Quantization Approach , 2016, IEEE Transactions on Neural Systems and Rehabilitation Engineering.

[15]  Anil K. Seth,et al.  A MATLAB toolbox for Granger causal connectivity analysis , 2010, Journal of Neuroscience Methods.

[16]  Nigel H. Lovell,et al.  Estimating cognitive workload using wavelet entropy-based features during an arithmetic task , 2013, Comput. Biol. Medicine.

[17]  Ad Aertsen,et al.  Review of the BCI Competition IV , 2012, Front. Neurosci..

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

[19]  G. Crooks On Measures of Entropy and Information , 2015 .

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

[21]  Stefan Haufe,et al.  A critical assessment of connectivity measures for EEG data: A simulation study , 2013, NeuroImage.

[22]  Jianbo Gao,et al.  Shannon and Renyi Entropies to Classify Effects of Mild Traumatic Brain Injury on Postural Sway , 2011, PloS one.

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

[24]  Michael X. Cohen,et al.  Comparison of different spatial transformations applied to EEG data: A case study of error processing. , 2015, International journal of psychophysiology : official journal of the International Organization of Psychophysiology.

[25]  Anthony Widjaja,et al.  Learning with Kernels: Support Vector Machines, Regularization, Optimization, and Beyond , 2003, IEEE Transactions on Neural Networks.

[26]  Jose C. Principe,et al.  Measures of Entropy From Data Using Infinitely Divisible Kernels , 2012, IEEE Transactions on Information Theory.

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

[28]  Hongxin Zhang,et al.  A self-adaptive frequency selection common spatial pattern and least squares twin support vector machine for motor imagery electroencephalography recognition , 2018, Biomed. Signal Process. Control..

[29]  Weifeng Liu,et al.  Kernel Adaptive Filtering: A Comprehensive Introduction , 2010 .

[30]  Jose C. Principe,et al.  Information Theoretic Learning - Renyi's Entropy and Kernel Perspectives , 2010, Information Theoretic Learning.

[31]  Francesco Carlo Morabito,et al.  Differentiating Interictal and Ictal States in Childhood Absence Epilepsy through Permutation Rényi Entropy , 2015, Entropy.

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

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

[34]  Yunfa Fu,et al.  Time–Frequency Cross Mutual Information Analysis of the Brain Functional Networks Underlying Multiclass Motor Imagery , 2018, Journal of motor behavior.

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

[36]  Huazhong Shu,et al.  Contribution to Transfer Entropy Estimation via the k-Nearest-Neighbors Approach , 2015, Entropy.

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

[38]  Didier Grandjean,et al.  Time, frequency, and time‐varying Granger‐causality measures in neuroscience , 2018, Statistics in medicine.

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

[40]  F. Perrin,et al.  Spherical splines for scalp potential and current density mapping. , 1989, Electroencephalography and clinical neurophysiology.

[41]  Uta Noppeney,et al.  Reliability-Weighted Integration of Audiovisual Signals Can Be Modulated by Top-down Attention , 2018, eNeuro.

[42]  Seif Eldawlatly,et al.  Dynamic Bayesian Networks for EEG motor imagery feature extraction , 2015, 2015 7th International IEEE/EMBS Conference on Neural Engineering (NER).

[43]  G. Prasad,et al.  Single-trial effective brain connectivity patterns enhance discriminability of mental imagery tasks , 2017, Journal of neural engineering.