journal article·2021-07-21Open access

Kernel-Based Phase Transfer Entropy with Enhanced Feature Relevance Analysis for Brain Computer Interfaces

Iván De La Pava Panche, Andrés Álvarez-Meza, Paula Marcela Herrera Gómez, David Cárdenas-Peña, Jorge Iván Ríos Patiño, Álvaro Orozco-Gutiérrez

Applied Sciences· Volume 11· Issue 15

Abstract

Neural oscillations are present in the brain at different spatial and temporal scales, and they are linked to several cognitive functions. Furthermore, the information carried by their phases is fundamental for the coordination of anatomically distributed processing in the brain. The concept of phase transfer entropy refers to an information theory-based measure of directed connectivity among neural oscillations that allows studying such distributed processes. Phase TE is commonly obtained from probability estimations carried out over data from multiple trials, which bars its use as a characterization strategy in brain–computer interfaces. In this work, we propose a novel methodology to estimate TE between single pairs of instantaneous phase time series. Our approach combines a kernel-based TE estimator defined in terms of Renyi’s α entropy, which sidesteps the need for probability distribution computation with phase time series obtained by complex filtering the neural signals. Besides, a kernel-alignment-based relevance analysis is added to highlight relevant features from effective connectivity-based representation supporting further classification stages in EEG-based brain–computer interface systems. Our proposal is tested on simulated coupled data and two publicly available databases containing EEG signals recorded under motor imagery and visual working memory paradigms. Attained results demonstrate how the introduced effective connectivity succeeds in detecting the interactions present in the data for the former, with statistically significant results around the frequencies of interest. It also reflects differences in coupling strength, is robust to realistic noise and signal mixing levels, and captures bidirectional interactions of localized frequency content. Obtained results for the motor imagery and working memory databases show that our approach, combined with the relevance analysis strategy, codes discriminant spatial and frequency-dependent patterns for the different conditions in each experimental paradigm, with classification performances that do well in comparison with those of alternative methods of similar nature.
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Research context

OpenAlex topics: EEG and Brain-Computer Interfaces · Neural dynamics and brain function · Functional Brain Connectivity Studies

SciVX discovery tags are terminology-based. OpenAlex topics are source-provided classifications.

Affiliations

Automatic Research Group, Universidad Tecnológica de Pereira, Pereira 660003, Colombia

Signal Processing and Recognition Group, Universidad Nacional de Colombia, Manizales 170003, Colombia

Psychiatry, Neuroscience and Community Research Group, Universidad Tecnológica de Pereira, Pereira 660003, Colombia

Funding

Ministerio de Ciencia Tecnología e Innovación de Colombia

References (65)

Show source-provided references
1. La Tour, T.D., Tallot, L., Grabot, L., Doyère, V., Van Wassenhove, V., Grenier, Y., and Gramfort, A. (2017). Non-linear auto-regressive models for cross-frequency coupling in neural time series. PLoS Comput. Biol., 13.10.1371/journal.pcbi.1005893 ↗
2. Da Silva, F.L. (2009). EEG: Origin and measurement. EEg-fMRI, Springer.10.1007/978-3-540-87919-0_2 ↗
3. The roles of alpha oscillation in working memory retention10.1002/brb3.1263 ↗
4. Neural cross-frequency coupling: Connecting architectures, mechanisms, and functions10.1016/j.tins.2015.09.001 ↗
5. Cross-frequency and iso-frequency estimation of functional corticomuscular coupling after stroke10.1007/s11571-020-09635-0 ↗
6. Decoding covert visual attention based on phase transfer entropy10.1016/j.physbeh.2020.112932 ↗
7. Phase permutation entropy: A complexity measure for nonlinear time series incorporating phase information10.1016/j.physa.2020.125686 ↗
8. Phase transfer entropy: A novel phase-based measure for directed connectivity in networks coupled by oscillatory interactions10.1016/j.neuroimage.2013.08.056 ↗
9. Review of advanced techniques for the estimation of brain connectivity measured with EEG/MEG10.1016/j.compbiomed.2011.06.020 ↗
10. A data-driven measure of effective connectivity based on Renyi’s α-entropy10.3389/fnins.2019.01277 ↗
11. Time, frequency, and time-varying Granger-causality measures in neuroscience10.1002/sim.7621 ↗
12. Robustly estimating the flow direction of information in complex physical systems10.1103/PhysRevLett.100.234101 ↗
13. Measuring directionality between neuronal oscillations of different frequencies10.1016/j.neuroimage.2015.05.044 ↗
14. Measuring information transfer10.1103/PhysRevLett.85.461 ↗
15. Contribution to transfer entropy estimation via the k-nearest-neighbors approach10.3390/e17064173 ↗
16. Wilmer, A., de Lussanet, M., and Lappe, M. (2012). Time-delayed mutual information of the phase as a measure of functional connectivity. PLoS ONE, 7.10.1371/journal.pone.0044633 ↗
17. Functional connectivity and network analysis during hypoactive delirium and recovery from anesthesia10.1016/j.clinph.2017.02.022 ↗
18. Direction of information flow in large-scale resting-state networks is frequency-dependent10.1073/pnas.1515657113 ↗
19. A Study on Resting EEG Effective Connectivity Difference before and after Neurofeedback for Children with ADHD10.1016/j.neuroscience.2020.12.038 ↗
20. Financial time series analysis based on effective phase transfer entropy10.1016/j.physa.2016.10.085 ↗
21. Single-trial effective brain connectivity patterns enhance discriminability of mental imagery tasks10.1088/1741-2552/aa785c ↗
22. Using brain network features to increase the classification accuracy of MI-BCI inefficiency subject10.1109/ACCESS.2019.2917327 ↗
23. García-Murillo, D.G., Alvarez-Meza, A., and Castellanos-Dominguez, G. (2021). Single-Trial Kernel-Based Functional Connectivity for Enhanced Feature Extraction in Motor-Related Tasks. Sensors, 21.10.3390/s21082750 ↗
24. Transfer spectral entropy and application to functional corticomuscular coupling10.1109/TNSRE.2019.2907148 ↗
25. Pinzuti, E., Wollstadt, P., Gutknecht, A., Tüscher, O., and Wibral, M. (2020). Measuring spectrally-resolved information transfer. PLoS Comput. Biol., 16.10.1371/journal.pcbi.1008526 ↗
26. Rényi, A. (1961). On measures of entropy and information. Proceedings of the Fourth Berkeley Symposium on Mathematical Statistics and Probability, Volume 1: Contributions to the Theory of Statistics, The Regents of the University of California.
27. Principe, J.C. (2010). Information Theoretic Learning: Renyi’s Entropy and Kernel Perspectives, Springer Science & Business Media.10.1007/978-1-4419-1570-2 ↗
28. Measures of entropy from data using infinitely divisible kernels10.1109/TIT.2014.2370058 ↗
29. Algorithms for learning kernels based on centered alignment
30. Wibral, M., Pampu, N., Priesemann, V., Siebenhühner, F., Seiwert, H., Lindner, M., Lizier, J.T., and Vicente, R. (2013). Measuring information-transfer delays. PLoS ONE, 8.10.1371/journal.pone.0055809 ↗
31. Transfer entropy—A model-free measure of effective connectivity for the neurosciences10.1007/s10827-010-0262-3 ↗
32. Takens, F. (1981). Detecting strange attractors in turbulence. Dynamical Systems and Turbulence, Warwick 1980, Springer.10.1007/BFb0091924 ↗
33. Estimating mutual information10.1103/PhysRevE.69.066138 ↗
34. Lindner, M., Vicente, R., Priesemann, V., and Wibral, M. (2011). TRENTOOL: A Matlab open source toolbox to analyse information flow in time series data with transfer entropy. BMC Neurosci., 12.10.1186/1471-2202-12-119 ↗
35. Revealing cross-frequency causal interactions during a mental arithmetic task through symbolic transfer entropy: A novel vector-quantization approach10.1109/TNSRE.2016.2516107 ↗
36. Granger causality and transfer entropy are equivalent for Gaussian variables10.1103/PhysRevLett.103.238701 ↗
37. Liu, W., Principe, J.C., and Haykin, S. (2011). Kernel Adaptive Filtering: A Comprehensive Introduction, John Wiley & Sons.10.1002/9780470608593 ↗
38. Video-based social behavior recognition based on kernel relevance analysis10.1007/s00371-019-01754-y ↗
39. A neural mass model for MEG/EEG:: Coupling and neuronal dynamics10.1016/j.neuroimage.2003.07.015 ↗
40. Evaluation of different measures of functional connectivity using a neural mass model10.1016/j.neuroimage.2003.10.006 ↗
41. Transfer Entropy as a Measure of Brain Connectivity: A Critical Analysis With the Help of Neural Mass Models10.3389/fncom.2020.00045 ↗
42. Weber, I., Florin, E., Von Papen, M., and Timmermann, L. (2017). The influence of filtering and downsampling on the estimation of transfer entropy. PLoS ONE, 12.10.1371/journal.pone.0188210 ↗
43. CNN-based framework using spatial dropping for enhanced interpretation of neural activity in motor imagery classification
44. Review of the BCI competition IV10.3389/fnins.2012.00055 ↗
45. Spherical splines for scalp potential and current density mapping10.1016/0013-4694(89)90180-6 ↗
46. Comparison of different spatial transformations applied to EEG data: A case study of error processing10.1016/j.ijpsycho.2014.09.013 ↗
47. Functional connectivity among multi-channel EEGs when working memory load reaches the capacity10.1016/j.brainres.2015.11.036 ↗
48. Data from brain activity during visual working memory replicates the correlation between contralateral delay activity and memory capacity10.1016/j.dib.2019.105042 ↗
49. Neural activity predicts individual differences in visual working memory capacity10.1038/nature02447 ↗
50. Johnson, E.L., Adams, J.N., Solbakk, A.K., Endestad, T., Larsson, P.G., Ivanovic, J., Meling, T.R., Lin, J.J., and Knight, R.T. (2018). Dynamic frontotemporal systems process space and time in working memory. PLoS Biol., 16.10.1371/journal.pbio.2004274 ↗
51. Spectral imprints of working memory for everyday associations in the frontoparietal network10.3389/fnsys.2018.00065 ↗
52. Scikit-learn: Machine Learning in Python
53. Practical method for determining the minimum embedding dimension of a scalar time series10.1016/S0167-2789(97)00118-8 ↗
54. Schölkopf, B., Smola, A.J., and Bach, F. (2002). Learning with Kernels: Support Vector Machines, Regularization, Optimization, and Beyond, MIT Press.10.7551/mitpress/4175.001.0001 ↗
55. A new look at the statistical model identification10.1109/TAC.1974.1100705 ↗
56. Time–Frequency Cross Mutual Information Analysis of the Brain Functional Networks Underlying Multiclass Motor Imagery10.1080/00222895.2017.1327417 ↗
57. How about taking a low-cost, small, and wireless EEG for a walk?10.1111/j.1469-8986.2012.01471.x ↗
58. Validation of ICA as a tool to remove eye movement artifacts from EEG/ERP
59. A self-adaptive frequency selection common spatial pattern and least squares twin support vector machine for motor imagery electroencephalography recognition10.1016/j.bspc.2017.11.014 ↗
60. Gómez, V., Álvarez, A., Herrera, P., Castellanos, G., and Orozco, A. (2018). Short Time EEG Connectivity Features to Support Interpretability of MI Discrimination. Iberoamerican Congress on Pattern Recognition, Springer.10.1007/978-3-030-13469-3_81 ↗
61. Elasuty, B., and Eldawlatly, S. (2015, January 22–24). Dynamic Bayesian Networks for EEG motor imagery feature extraction. Proceedings of the 2015 7th International IEEE/EMBS Conference on Neural Engineering (NER), Montpellier, France.10.1109/NER.2015.7146587 ↗
62. Discrimination of motor imagery tasks via information flow pattern of brain connectivity10.3233/THC-161212 ↗
63. Clustering with t-SNE, provably10.1137/18M1216134 ↗
64. The neural network of motor imagery: An ALE meta-analysis10.1016/j.neubiorev.2013.03.017 ↗
65. Martínez-Cancino, R., Delorme, A., Wagner, J., Kreutz-Delgado, K., Sotero, R.C., and Makeig, S. (2020). What can local transfer entropy tell us about phase-amplitude coupling in electrophysiological signals?. Entropy, 22.10.20944/preprints202010.0006.v1 ↗