Space-time recurrences for functional connectivity evaluation and feature extraction in motor imagery brain-computer interfaces

AbstractThis work presents a classification performance comparison between different frameworks for functional connectivity evaluation and complex network feature extraction aiming to distinguish motor imagery classes in electroencephalography (EEG)-based brain-computer interfaces (BCIs). The analysis was performed in two online datasets: (1) a classical benchmark—the BCI competition IV dataset 2a—allowing a comparison with a representative set of strategies previously employed in this BCI paradigm and (2) a statistically representative dataset for signal processing technique comparisons over 52 subjects. Besides exploring three classical similarity measures—Pearson correlation, Spearman correlation, and mean phase coherence—this work also proposes a recurrence-based alternative for estimating EEG brain functional connectivity, which takes into account the recurrence density between pairwise electrodes over a time window. These strategies were followed by graph feature evaluation considering clustering coefficient, degree, betweenness centrality, and eigenvector centrality. The features were selected by Fisher’s discriminating ratio and classification was performed by a least squares classifier in agreement with classical and online BCI processing strategies. The results revealed that the recurrence-based approach for functional connectivity evaluation was significantly better than the other frameworks, which is probably associated with the use of higher order statistics underlying the electrode joint probability estimation and a higher capability of capturing nonlinear inter-relations. There were no significant differences in performance among the evaluated graph features, but the eigenvector centrality was the best feature regarding processing time. Finally, the best ranked graph-based attributes were found in classical EEG motor cortex positions for the subjects with best performances, relating functional organization and motor activity. Graphical AbstractEvaluating functional connectivity based on Space-Time Recurrence Counting for motor imagery classification in brain-computer interfaces. Recurrences are evaluated between electrodes over a time window, and, after a density threshold, the electrodes adjacency matrix is stablish, leading to a graph. Graph-based topological measures are used for motor imagery classification

[1]  Dennis Velakoulis,et al.  Striatal changes in Parkinson disease: An investigation of morphology, functional connectivity and their relationship to clinical symptoms , 2018, Psychiatry Research: Neuroimaging.

[2]  Sung-Jin Cho,et al.  Draft genome of the sea cucumber Apostichopus japonicus and genetic polymorphism among color variants , 2017, GigaScience.

[3]  A Giuliani,et al.  Elucidating protein secondary structures using alpha‐carbon recurrence quantifications , 2001, Proteins.

[4]  A. Strafella,et al.  Dynamic functional connectivity in Parkinson's disease patients with mild cognitive impairment and normal cognition , 2017, NeuroImage: Clinical.

[5]  Karl J. Friston,et al.  Clinical Applications of Stochastic Dynamic Models of the Brain, Part I: A Primer. , 2017, Biological psychiatry. Cognitive neuroscience and neuroimaging.

[6]  F. L. D. Silva,et al.  Event-related EEG/MEG synchronization and desynchronization: basic principles , 1999, Clinical Neurophysiology.

[7]  Yifan Hu,et al.  Efficient, High-Quality Force-Directed Graph Drawing , 2006 .

[8]  Gabriela Castellano,et al.  Effect of the combination of different numbers of flickering frequencies in an SSVEP-BCI for healthy volunteers and stroke patients , 2015, 2015 7th International IEEE/EMBS Conference on Neural Engineering (NER).

[9]  S. J. Roberts,et al.  Temporal and spatial complexity measures for electroencephalogram based brain-computer interfacing , 2006, Medical & Biological Engineering & Computing.

[10]  Jürgen Kurths,et al.  Recurrence plots for the analysis of complex systems , 2009 .

[11]  Lana Kambeitz-Ilankovic,et al.  The left frontal cortex supports reserve in aging by enhancing functional network efficiency , 2018, Alzheimer's Research & Therapy.

[12]  M Small,et al.  Complex network from pseudoperiodic time series: topology versus dynamics. , 2006, Physical review letters.

[13]  Karl J. Friston,et al.  Clinical Applications of Stochastic Dynamic Models of the Brain, Part II: A Review. , 2017, Biological psychiatry. Cognitive neuroscience and neuroimaging.

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

[15]  O. Sporns Networks of the Brain , 2010 .

[16]  Brian R. Tietz,et al.  Deciding Which Way to Go: How Do Insects Alter Movements to Negotiate Barriers? , 2012, Front. Neurosci..

[17]  Danielle S Bassett,et al.  Brain graphs: graphical models of the human brain connectome. , 2011, Annual review of clinical psychology.

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

[19]  Jie Yang,et al.  Different aberrant mentalizing networks in males and females with autism spectrum disorders: Evidence from resting-state functional magnetic resonance imaging , 2018, Autism : the international journal of research and practice.

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

[21]  Mahyar Hamedi,et al.  Motor imagery brain functional connectivity analysis via coherence , 2015, 2015 IEEE International Conference on Signal and Image Processing Applications (ICSIPA).

[22]  Keith A. Johnson,et al.  Preferential degradation of cognitive networks differentiates Alzheimer’s disease from ageing , 2018, Brain : a journal of neurology.

[23]  Gabriela Castellano,et al.  Can graph metrics be used for EEG-BCIs based on hand motor imagery? , 2018, Biomed. Signal Process. Control..

[24]  Robert Savit,et al.  Stationarity and nonstationarity in time series analysis , 1996 .

[25]  Gordon Cheng,et al.  Long-Term Training with a Brain-Machine Interface-Based Gait Protocol Induces Partial Neurological Recovery in Paraplegic Patients , 2016, Scientific Reports.

[26]  E. Bullmore,et al.  Functional Connectivity and Brain Networks in Schizophrenia , 2010, The Journal of Neuroscience.

[27]  Jonathan R. Wolpaw,et al.  Brain–Computer InterfacesPrinciples and Practice , 2012 .

[28]  Mahdi Jalili,et al.  Functional Brain Networks: Does the Choice of Dependency Estimator and Binarization Method Matter? , 2016, Scientific Reports.

[29]  J. Kurths,et al.  Complex network approach for recurrence analysis of time series , 2009, 0907.3368.

[30]  Andrea Petracca,et al.  A real-time classification algorithm for EEG-based BCI driven by self-induced emotions , 2015, Comput. Methods Programs Biomed..

[31]  Alessandro Giuliani,et al.  Model-free analysis of brain fMRI data by recurrence quantification , 2007, NeuroImage.

[32]  J R Wolpaw,et al.  Spatial filter selection for EEG-based communication. , 1997, Electroencephalography and clinical neurophysiology.

[33]  Kuncheng Li,et al.  Brain network alteration in patients with temporal lobe epilepsy with cognitive impairment , 2018, Epilepsy & Behavior.

[34]  Sung Chan Jun,et al.  EEG datasets for motor imagery brain–computer interface , 2017, GigaScience.

[35]  Kalyana Chakravarthy Veluvolu,et al.  Event-Related Functional Network Identification: Application to EEG Classification , 2016, IEEE Journal of Selected Topics in Signal Processing.

[36]  P. Grassberger,et al.  Measuring the Strangeness of Strange Attractors , 1983 .

[37]  Babak Mahmoudi,et al.  Electro-encephalogram based brain–computer interface: improved performance by mental practice and concentration skills , 2006, Medical and Biological Engineering and Computing.

[38]  Mahdi Jalili,et al.  EEG-based functional networks in schizophrenia , 2011, Comput. Biol. Medicine.

[39]  E. Basar,et al.  Abnormalities of resting-state functional cortical connectivity in patients with dementia due to Alzheimer's and Lewy body diseases: an EEG study , 2017, Neurobiology of Aging.

[40]  J. Pillai,et al.  Application of Resting State Functional MR Imaging to Presurgical Mapping: Language Mapping. , 2017, Neuroimaging clinics of North America.

[41]  Yoon Gi Chung,et al.  Analysis of correlated EEG activity during motor imagery for brain-computer interfaces , 2011, 2011 11th International Conference on Control, Automation and Systems.

[42]  Gabriela Castellano,et al.  A Recurrence-Based Approach for Feature Extraction in Brain-Computer Interface Systems , 2014 .

[43]  Romis de Faissol Attux,et al.  Comparative analysis of strategies for feature extraction and classification in SSVEP BCIs , 2015, Biomed. Signal Process. Control..

[44]  N. Marwan,et al.  Nonlinear analysis of bivariate data with cross recurrence plots , 2002, physics/0201061.

[45]  Weifeng Liu,et al.  Correntropy: A Localized Similarity Measure , 2006, The 2006 IEEE International Joint Conference on Neural Network Proceedings.

[46]  João Ricardo Sato,et al.  Abnormal Functional Resting-State Networks in ADHD: Graph Theory and Pattern Recognition Analysis of fMRI Data , 2014, BioMed research international.

[47]  Dario Farina,et al.  Classification of EEG signals to identify variations in attention during motor task execution , 2017, Journal of Neuroscience Methods.

[48]  Mahyar Hamedi,et al.  Electroencephalographic Motor Imagery Brain Connectivity Analysis for BCI: A Review , 2016, Neural Computation.

[49]  Helge B. D. Sørensen,et al.  BCI using imaginary movements: The simulator , 2013, Comput. Methods Programs Biomed..

[50]  Hui Yang,et al.  Self-organized topology of recurrence-based complex networks. , 2013, Chaos.

[51]  Malek Adjouadi,et al.  Functional connectivity network based on graph analysis of scalp EEG for epileptic classification , 2013, 2013 IEEE Signal Processing in Medicine and Biology Symposium (SPMB).

[52]  Muhammad Abd-El-Barr,et al.  Long-term Training With a Brain-Machine Interface-Based Gait Protocol Induces Partial Neurological Recovery in Paraplegic Patients. , 2016, Neurosurgery.

[53]  Giampaolo Brichetto,et al.  Resting‐state functional connectivity and motor imagery brain activation , 2016, Human brain mapping.

[54]  Olaf Sporns,et al.  Complex network measures of brain connectivity: Uses and interpretations , 2010, NeuroImage.

[55]  Alexander J. Barnett,et al.  Applications of Resting-State Functional MR Imaging to Epilepsy. , 2017, Neuroimaging clinics of North America.

[56]  Michael Small,et al.  Recurrence-based time series analysis by means of complex network methods , 2010, Int. J. Bifurc. Chaos.

[57]  Moritz Grosse-Wentrup,et al.  Understanding Brain Connectivity Patterns during Motor Imagery for Brain-Computer Interfacing , 2008, NIPS.

[58]  Ethan R. Buch,et al.  Parietofrontal integrity determines neural modulation associated with grasping imagery after stroke. , 2012, Brain : a journal of neurology.

[59]  Eric C Leuthardt,et al.  Resting-state Functional Magnetic Resonance Imaging in Presurgical Functional Mapping: Sensorimotor Localization. , 2017, Neuroimaging clinics of North America.

[60]  R. Turner,et al.  Eigenvector Centrality Mapping for Analyzing Connectivity Patterns in fMRI Data of the Human Brain , 2010, PloS one.

[61]  Panagiotis D. Bamidis,et al.  Investigating the Role of Alpha and Beta Rhythms in Functional Motor Networks , 2016, Neuroscience.

[62]  Angus W. MacDonald,et al.  Functional network changes and cognitive control in schizophrenia , 2017, NeuroImage: Clinical.

[63]  J. Wolpaw,et al.  Brain-Computer Interfaces: Principles and Practice , 2012 .

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

[65]  Matteo Fraschini,et al.  Brain network analysis of EEG functional connectivity during imagery hand movements. , 2013, Journal of integrative neuroscience.

[66]  Chang-Hwan Im,et al.  Evaluation of feature extraction methods for EEG-based brain–computer interfaces in terms of robustness to slight changes in electrode locations , 2012, Medical & Biological Engineering & Computing.

[67]  Ramaswamy Palaniappan,et al.  Multiresolution analysis over graphs for a motor imagery based online BCI game , 2016, Comput. Biol. Medicine.

[68]  G. de Marco,et al.  Assessment of brain interactivity in the motor cortex from the concept of functional connectivity and spectral analysis of fMRI data , 2008, Biological Cybernetics.

[69]  James Theiler,et al.  Generalized redundancies for time series analysis , 1995 .

[70]  Peng Xu,et al.  Efficient resting-state EEG network facilitates motor imagery performance , 2015, Journal of neural engineering.

[71]  Svitlana Zinger,et al.  Brain resting‐state networks in adolescents with high‐functioning autism: Analysis of spatial connectivity and temporal neurodynamics , 2018, Brain and behavior.

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

[73]  Weifeng Liu,et al.  Correntropy: Properties and Applications in Non-Gaussian Signal Processing , 2007, IEEE Transactions on Signal Processing.

[74]  Steve Horvath,et al.  Resting-State Quantitative Electroencephalography Reveals Increased Neurophysiologic Connectivity in Depression , 2012, PloS one.

[75]  David G. Stork,et al.  Pattern Classification , 1973 .

[76]  Graeme D. Jackson,et al.  Increased segregation of brain networks in focal epilepsy: An fMRI graph theory finding , 2015, NeuroImage: Clinical.

[77]  Julia M. Sheffield,et al.  Evidence for Accelerated Decline of Functional Brain Network Efficiency in Schizophrenia. , 2016, Schizophrenia bulletin.

[78]  Charles L. Webber,et al.  Recurrence Quantifications: Feature Extractions from Recurrence Plots , 2007, Int. J. Bifurc. Chaos.

[79]  Christopher James,et al.  Use of graph metrics to classify motor imagery based BCI , 2016, 2016 International Conference for Students on Applied Engineering (ICSAE).