Robust electroencephalogram phase estimation with applications in brain-computer interface systems

OBJECTIVE In this study, a robust method is developed for frequency-specific electroencephalogram (EEG) phase extraction using the analytic representation of the EEG. Based on recent theoretical findings in this area, it is shown that some of the phase variations-previously associated to the brain response-are systematic side-effects of the methods used for EEG phase calculation, especially during low analytical amplitude segments of the EEG. APPROACH With this insight, the proposed method generates randomized ensembles of the EEG phase using minor perturbations in the zero-pole loci of narrow-band filters, followed by phase estimation using the signal's analytical form and ensemble averaging over the randomized ensembles to obtain a robust EEG phase and frequency. This Monte Carlo estimation method is shown to be very robust to noise and minor changes of the filter parameters and reduces the effect of fake EEG phase jumps, which do not have a cerebral origin. MAIN RESULTS As proof of concept, the proposed method is used for extracting EEG phase features for a brain computer interface (BCI) application. The results show significant improvement in classification rates using rather simple phase-related features and a standard K-nearest neighbors and random forest classifiers, over a standard BCI dataset. SIGNIFICANCE The average performance was improved between 4-7% (in absence of additive noise) and 8-12% (in presence of additive noise). The significance of these improvements was statistically confirmed by a paired sample t-test, with 0.01 and 0.03 p-values, respectively. The proposed method for EEG phase calculation is very generic and may be applied to other EEG phase-based studies.

[1]  Dean J. Krusienski,et al.  Value of amplitude, phase, and coherence features for a sensorimotor rhythm-based brain–computer interface , 2012, Brain Research Bulletin.

[2]  Yijun Wang,et al.  Phase Synchrony Measurement in Motor Cortex for Classifying Single-trial EEG during Motor Imagery , 2006, 2006 International Conference of the IEEE Engineering in Medicine and Biology Society.

[3]  J. Martinerie,et al.  Comparison of Hilbert transform and wavelet methods for the analysis of neuronal synchrony , 2001, Journal of Neuroscience Methods.

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

[5]  W. Singer,et al.  Oscillatory responses in cat visual cortex exhibit inter-columnar synchronization which reflects global stimulus properties , 1989, Nature.

[6]  徹 川田 第36 回Annual International Conference of the IEEE Engineering in Medicine and Biology Society , 2015 .

[7]  Miroslav D. Lutovac,et al.  Filter Design for Signal Processing Using MATLAB and Mathematica , 2000 .

[8]  Alan V. Oppenheim,et al.  Discrete-time Signal Processing. Vol.2 , 2001 .

[9]  Xiaorong Gao,et al.  Enhancing the classification accuracy of steady-state visual evoked potential-based brain–computer interfaces using phase constrained canonical correlation analysis , 2011, Journal of neural engineering.

[10]  Bernard C. Picinbono,et al.  On instantaneous amplitude and phase of signals , 1997, IEEE Trans. Signal Process..

[11]  G Calhoun,et al.  Brain-computer interfaces based on the steady-state visual-evoked response. , 2000, IEEE transactions on rehabilitation engineering : a publication of the IEEE Engineering in Medicine and Biology Society.

[12]  N. Birbaumer,et al.  BCI2000: a general-purpose brain-computer interface (BCI) system , 2004, IEEE Transactions on Biomedical Engineering.

[13]  K Itoh,et al.  Analysis of the phase unwrapping algorithm. , 1982, Applied optics.

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

[15]  Yi Feng,et al.  Using phase information to reveal the nature of event-related desynchronization , 2008, Biomed. Signal Process. Control..

[16]  Clemens Brunner,et al.  Phase relationships between different subdural electrode recordings in man , 2005, Neuroscience Letters.

[17]  Jeffrey M. Hausdorff,et al.  Physionet: Components of a New Research Resource for Complex Physiologic Signals". Circu-lation Vol , 2000 .

[18]  Masato Okada,et al.  Statistical method for detecting phase shifts in alpha rhythm from human electroencephalogram data. , 2013, Physical review. E, Statistical, nonlinear, and soft matter physics.

[19]  José del R. Millán,et al.  Phase-based features for motor imagery brain-computer interfaces , 2011, 2011 Annual International Conference of the IEEE Engineering in Medicine and Biology Society.

[20]  J. Fell,et al.  The role of phase synchronization in memory processes , 2011, Nature Reviews Neuroscience.

[21]  F. Mormann,et al.  Epileptic seizures are preceded by a decrease in synchronization , 2003, Epilepsy Research.

[22]  Stefan Haufe,et al.  The Berlin Brain-Computer Interface: Progress Beyond Communication and Control , 2016, Front. Neurosci..

[23]  P. Ktonas,et al.  Instantaneous envelope and phase extraction from real signals: Theory, implementation, and an application to EEG analysis , 1980 .

[24]  Boualem Boashash,et al.  Estimating and interpreting the instantaneous frequency of a signal. I. Fundamentals , 1992, Proc. IEEE.

[25]  Carlos Carreiras,et al.  Phase-locking factor in a motor imagery brain-computer interface , 2012, 2012 Annual International Conference of the IEEE Engineering in Medicine and Biology Society.

[26]  K Lehnertz,et al.  Indications of nonlinear deterministic and finite-dimensional structures in time series of brain electrical activity: dependence on recording region and brain state. , 2001, Physical review. E, Statistical, nonlinear, and soft matter physics.

[27]  Reza Sameni,et al.  A Robust Statistical Framework for Instantaneous Electroencephalogram Phase and Frequency Analysis , 2016 .

[28]  David Rudrauf,et al.  Frequency flows and the time-frequency dynamics of multivariate phase synchronization in brain signals , 2006, NeuroImage.

[29]  Klaus-Robert Müller,et al.  Decoding of top-down cognitive processing for SSVEP-controlled BMI , 2016, Scientific Reports.

[30]  Hongzhi Qi,et al.  A novel technique for phase synchrony measurement from the complex motor imaginary potential of combined body and limb action , 2010, Journal of neural engineering.

[31]  F. Mormann,et al.  Mean phase coherence as a measure for phase synchronization and its application to the EEG of epilepsy patients , 2000 .

[32]  Kurths,et al.  Phase synchronization of chaotic oscillators. , 1996, Physical review letters.

[33]  M. Besserve,et al.  Towards a proper estimation of phase synchronization from time series , 2006, Journal of Neuroscience Methods.

[34]  Klaus-Robert Müller,et al.  Interpretable deep neural networks for single-trial EEG classification , 2016, Journal of Neuroscience Methods.

[35]  Yijun Wang,et al.  Amplitude and phase coupling measures for feature extraction in an EEG-based brain–computer interface , 2007, Journal of neural engineering.

[36]  Yi Zhou,et al.  Combination of amplitude and phase features under a uniform framework with EMD in EEG-based Brain-Computer Interface , 2012, 2012 Annual International Conference of the IEEE Engineering in Medicine and Biology Society.

[37]  Petra Kaufmann,et al.  Two Dimensional Phase Unwrapping Theory Algorithms And Software , 2016 .

[38]  W. Freeman Origin, structure, and role of background EEG activity. Part 2. Analytic phase , 2004, Clinical Neurophysiology.