Advantages of EEG phase patterns for the detection of gait intention in healthy and stroke subjects

OBJECTIVE One use of EEG-based brain-computer interfaces (BCIs) in rehabilitation is the detection of movement intention. In this paper we investigate for the first time the instantaneous phase of movement related cortical potential (MRCP) and its application to the detection of gait intention. APPROACH We demonstrate the utility of MRCP phase in two independent datasets, in which 10 healthy subjects and 9 chronic stroke patients executed a self-initiated gait task in three sessions. Phase features were compared to more conventional amplitude and power features. MAIN RESULTS The neurophysiology analysis showed that phase features have higher signal-to-noise ratio than the other features. Also, BCI detectors of gait intention based on phase, amplitude, and their combination were evaluated under three conditions: session-specific calibration, intersession transfer, and intersubject transfer. Results show that the phase based detector is the most accurate for session-specific calibration (movement intention was correctly detected in 66.5% of trials in healthy subjects, and in 63.3% in stroke patients). However, in intersession and intersubject transfer, the detector that combines amplitude and phase features is the most accurate one and the only that retains its accuracy (62.5% in healthy subjects and 59% in stroke patients) w.r.t. session-specific calibration. SIGNIFICANCE MRCP phase features improve the detection of gait intention and could be used in practice to remove time-consuming BCI recalibration.

[1]  W. Klimesch,et al.  Alpha phase synchronization predicts P1 and N1 latency and amplitude size. , 2005, Cerebral cortex.

[2]  Daniel P. Ferris,et al.  Removal of movement artifact from high-density EEG recorded during walking and running. , 2010, Journal of neurophysiology.

[3]  Klaus-Robert Müller,et al.  Learning From More Than One Data Source: Data Fusion Techniques for Sensorimotor Rhythm-Based Brain–Computer Interfaces , 2015, Proceedings of the IEEE.

[4]  M. Molinari,et al.  Rehabilitation of gait after stroke: a review towards a top-down approach , 2011, Journal of NeuroEngineering and Rehabilitation.

[5]  Andrés Úbeda,et al.  EEG-Based Detection of Starting and Stopping During Gait Cycle , 2016, Int. J. Neural Syst..

[6]  Dario Farina,et al.  Detection of movement-related cortical potentials based on subject-independent training , 2013, Medical & Biological Engineering & Computing.

[7]  Cuntai Guan,et al.  Learning from other subjects helps reducing Brain-Computer Interface calibration time , 2010, 2010 IEEE International Conference on Acoustics, Speech and Signal Processing.

[8]  Arnaud Delorme,et al.  EEGLAB: an open source toolbox for analysis of single-trial EEG dynamics including independent component analysis , 2004, Journal of Neuroscience Methods.

[9]  Lüder Deecke,et al.  Voluntary finger movement in man: Cerebral potentials and theory , 1976, Biological Cybernetics.

[10]  Klaus-Robert Müller,et al.  ℓ1-penalized linear mixed-effects models for high dimensional data with application to BCI , 2011, NeuroImage.

[11]  G. Cheron,et al.  About the cortical origin of the low-delta and high-gamma rhythms observed in EEG signals during treadmill walking , 2014, Neuroscience Letters.

[12]  Nicola Smania,et al.  Modulation of event-related desynchronization in robot-assisted hand performance: brain oscillatory changes in active, passive and imagined movements , 2013, Journal of NeuroEngineering and Rehabilitation.

[13]  J. Millán,et al.  Single trial analysis of slow cortical potentials: a study on anticipation related potentials , 2013, Journal of neural engineering.

[14]  A. Grinvald,et al.  Dynamics of Ongoing Activity: Explanation of the Large Variability in Evoked Cortical Responses , 1996, Science.

[15]  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.

[16]  Thilo Womelsdorf,et al.  A Role of Phase-Resetting in Coordinating Large Scale Neural Networks During Attention and Goal-Directed Behavior , 2016, Front. Syst. Neurosci..

[17]  Dennis J. McFarland,et al.  Brain–computer interfaces for communication and control , 2002, Clinical Neurophysiology.

[18]  Ning Jiang,et al.  Enhanced Low-Latency Detection of Motor Intention From EEG for Closed-Loop Brain-Computer Interface Applications , 2014, IEEE Transactions on Biomedical Engineering.

[19]  L. Montesano,et al.  Detecting intention to walk in stroke patients from pre-movement EEG correlates , 2015, Journal of NeuroEngineering and Rehabilitation.

[20]  Peter A. Tass,et al.  Phase Resetting in Medicine and Biology: Stochastic Modelling and Data Analysis , 1999 .

[21]  Jose L Pons,et al.  Detection of the Onset of Voluntary Movements Based on the Combination of ERD and BP Cortical Patterns , 2014 .

[22]  M. Hallett,et al.  Prediction of human voluntary movement before it occurs , 2011, Clinical Neurophysiology.

[23]  Ian Daly,et al.  Brain computer interface control via functional connectivity dynamics , 2012, Pattern Recognit..

[24]  Guy Cheron,et al.  Movement gating of beta/gamma oscillations involved in the N30 somatosensory evoked potential , 2009, Human brain mapping.

[25]  Daniel P. Ferris,et al.  Electrocortical activity is coupled to gait cycle phase during treadmill walking , 2011, NeuroImage.

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

[27]  Fabien Lotte,et al.  Signal Processing Approaches to Minimize or Suppress Calibration Time in Oscillatory Activity-Based Brain–Computer Interfaces , 2015, Proceedings of the IEEE.

[28]  Klaus-Robert Müller,et al.  Subject independent EEG-based BCI decoding , 2009, NIPS.

[29]  C. Neuper,et al.  It's how you get there: walking down a virtual alley activates premotor and parietal areas , 2014, Front. Hum. Neurosci..

[30]  Ross Ihaka,et al.  Gentleman R: R: A language for data analysis and graphics , 1996 .

[31]  Klaus-Robert Müller,et al.  Towards Zero Training for Brain-Computer Interfacing , 2008, PloS one.

[32]  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.

[33]  Lüder Deecke,et al.  Brain potential changes in voluntary and passive movements in humans: readiness potential and reafferent potentials , 2016, Pflügers Archiv - European Journal of Physiology.

[34]  Brendan Z. Allison,et al.  Is It Significant? Guidelines for Reporting BCI Performance , 2012 .

[35]  Jose L. Contreras-Vidal,et al.  Negligible Motion Artifacts in Scalp Electroencephalography (EEG) During Treadmill Walking , 2016, Front. Hum. Neurosci..

[36]  J. Millán,et al.  Detection of self-paced reaching movement intention from EEG signals , 2012, Front. Neuroeng..

[37]  M. Hallett,et al.  Classifying EEG signals preceding right hand, left hand, tongue, and right foot movements and motor imageries , 2008, Clinical Neurophysiology.

[38]  Hiroshi Shibasaki,et al.  How does the brain respond to unimodal and bimodal sensory demand in movement of the lower extremity? , 2007, Experimental Brain Research.

[39]  H. Kornhuber,et al.  [CHANGES IN THE BRAIN POTENTIAL IN VOLUNTARY MOVEMENTS AND PASSIVE MOVEMENTS IN MAN: READINESS POTENTIAL AND REAFFERENT POTENTIALS]. , 1965, Pflugers Archiv fur die gesamte Physiologie des Menschen und der Tiere.

[40]  D. Farina,et al.  A brain–computer interface for single-trial detection of gait initiation from movement related cortical potentials , 2015, Clinical Neurophysiology.

[41]  Luis Montesano,et al.  Brain-machine interfaces for motor rehabilitation: Is recalibration important? , 2015, 2015 IEEE International Conference on Rehabilitation Robotics (ICORR).

[42]  Ning Jiang,et al.  An Accurate, Versatile, and Robust Brain Switch for Neurorehabilitation , 2014, Brain-Computer Interface Research.

[43]  Klaus-Robert Müller,et al.  Subject-independent mental state classification in single trials , 2009, Neural Networks.

[44]  S. Holm A Simple Sequentially Rejective Multiple Test Procedure , 1979 .

[45]  H. Kornhuber,et al.  Hirnpotentialänderungen bei Willkürbewegungen und passiven Bewegungen des Menschen: Bereitschaftspotential und reafferente Potentiale , 1965, Pflüger's Archiv für die gesamte Physiologie des Menschen und der Tiere.

[46]  Klaus-Robert Müller,et al.  Introduction to machine learning for brain imaging , 2011, NeuroImage.

[47]  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.

[48]  Alessandro Presacco,et al.  Towards a non-invasive brain-machine interface system to restore gait function in humans , 2011, 2011 Annual International Conference of the IEEE Engineering in Medicine and Biology Society.

[49]  Cuntai Guan,et al.  Omitting the intra-session calibration in EEG-based brain computer interface used for stroke rehabilitation , 2012, 2012 Annual International Conference of the IEEE Engineering in Medicine and Biology Society.

[50]  Jose L. Contreras-Vidal,et al.  Sitting and standing intention can be decoded from scalp EEG recorded prior to movement execution , 2014, Front. Neurosci..

[51]  Clemens Brunner,et al.  Mu rhythm (de)synchronization and EEG single-trial classification of different motor imagery tasks , 2006, NeuroImage.

[52]  Valer Jurcak,et al.  10/20, 10/10, and 10/5 systems revisited: Their validity as relative head-surface-based positioning systems , 2007, NeuroImage.

[53]  Christoph Zrenner,et al.  Closed-Loop Neuroscience and Non-Invasive Brain Stimulation: A Tale of Two Loops , 2016, Front. Cell. Neurosci..

[54]  Cuntai Guan,et al.  EEG Data Space Adaptation to Reduce Intersession Nonstationarity in Brain-Computer Interface , 2013, Neural Computation.

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

[56]  Dario Farina,et al.  A Novel Brain-Computer Interface for Chronic Stroke Patients , 2014 .

[57]  Aapo Hyvärinen,et al.  A Fast Fixed-Point Algorithm for Independent Component Analysis of Complex Valued Signals , 2000, Int. J. Neural Syst..

[58]  Shiliang Sun,et al.  A subject transfer framework for EEG classification , 2012, Neurocomputing.

[59]  Michael X Cohen,et al.  Analyzing Neural Time Series Data: Theory and Practice , 2014 .

[60]  Benedict Shien Wei Ng,et al.  EEG phase patterns reflect the selectivity of neural firing. , 2013, Cerebral cortex.

[61]  Andreea Ioana Sburlea,et al.  Intersession adaptation of the EEG-based detector of self-paced walking intention in stroke patients , 2015, 2015 37th Annual International Conference of the IEEE Engineering in Medicine and Biology Society (EMBC).

[62]  N. Hatsopoulos,et al.  Fast and Slow Oscillations in Human Primary Motor Cortex Predict Oncoming Behaviorally Relevant Cues , 2010, Neuron.

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

[64]  R. Chavarriaga,et al.  Single trial recognition of anticipatory slow cortical potentials: The role of spatio-spectral filtering , 2011, 2011 5th International IEEE/EMBS Conference on Neural Engineering.

[65]  Dario Farina,et al.  Movement related cortical potentials and sensory motor rhythms during self initiated and cued movements , 2014 .

[66]  C. Nam,et al.  Movement imagery-related lateralization of event-related (de)synchronization (ERD/ERS): Motor-imagery duration effects , 2011, Clinical Neurophysiology.

[67]  B. Hangya,et al.  Phase Entrainment of Human Delta Oscillations Can Mediate the Effects of Expectation on Reaction Speed , 2010, The Journal of Neuroscience.

[68]  R. VanRullen,et al.  The Phase of Ongoing EEG Oscillations Predicts Visual Perception , 2009, The Journal of Neuroscience.

[69]  Wei-Yen Hsu,et al.  Enhancing the Performance of Motor Imagery EEG Classification Using Phase Features , 2015, Clinical EEG and neuroscience.

[70]  M. Hallett,et al.  What is the Bereitschaftspotential? , 2006, Clinical Neurophysiology.

[71]  C. Neuper,et al.  Robot Assisted Walking Affects the Synchrony Between Premotor and Somatosensory Areas , 2013, Biomedizinische Technik. Biomedical engineering.

[72]  D. Farina,et al.  Detection of movement intention from single-trial movement-related cortical potentials , 2011, Journal of neural engineering.

[73]  Peter Desain,et al.  Feasibility of measuring event Related Desynchronization with electroencephalography during walking , 2012, 2012 Annual International Conference of the IEEE Engineering in Medicine and Biology Society.

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

[75]  M Congedo,et al.  A review of classification algorithms for EEG-based brain–computer interfaces , 2007, Journal of neural engineering.

[76]  G. Pfurtscheller,et al.  Evaluation of event-related desynchronization (ERD) preceding and following voluntary self-paced movement. , 1979, Electroencephalography and clinical neurophysiology.

[77]  Michael Voigt,et al.  Movement-related parameters modulate cortical activity during imaginary isometric plantar-flexions , 2006, Experimental Brain Research.

[78]  Peggy B. Nelson,et al.  Annual International Conference of the IEEE Engineering in Medicine and Biology - Proceedings , 2001 .

[79]  Andreea Ioana Sburlea,et al.  Continuous detection of the self-initiated walking pre-movement state from EEG correlates without session-to-session recalibration , 2015, Journal of neural engineering.