Upper limb movements can be decoded from the time-domain of low-frequency EEG

How neural correlates of movements are represented in the human brain is of ongoing interest and has been researched with invasive and non-invasive methods. In this study, we analyzed the encoding of single upper limb movements in the time-domain of low-frequency electroencephalography (EEG) signals. Fifteen healthy subjects executed and imagined six different sustained upper limb movements. We classified these six movements and a rest class and obtained significant average classification accuracies of 55% (movement vs movement) and 87% (movement vs rest) for executed movements, and 27% and 73%, respectively, for imagined movements. Furthermore, we analyzed the classifier patterns in the source space and located the brain areas conveying discriminative movement information. The classifier patterns indicate that mainly premotor areas, primary motor cortex, somatosensory cortex and posterior parietal cortex convey discriminative movement information. The decoding of single upper limb movements is specially interesting in the context of a more natural non-invasive control of e.g., a motor neuroprosthesis or a robotic arm in highly motor disabled persons.

[1]  Stefan Haufe,et al.  On the interpretation of weight vectors of linear models in multivariate neuroimaging , 2014, NeuroImage.

[2]  A. Aertsen,et al.  The role of ECoG magnitude and phase in decoding position, velocity, and acceleration during continuous motor behavior , 2013, Front. Neurosci..

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

[4]  Thomas E. Nichols,et al.  Nonparametric permutation tests for functional neuroimaging: A primer with examples , 2002, Human brain mapping.

[5]  Francisco Sepulveda,et al.  Delta band contribution in cue based single trial classification of real and imaginary wrist movements , 2008, Medical & Biological Engineering & Computing.

[6]  R. Oostenveld,et al.  Nonparametric statistical testing of EEG- and MEG-data , 2007, Journal of Neuroscience Methods.

[7]  R. Kass,et al.  Decoding and cortical source localization for intended movement direction with MEG. , 2010, Journal of neurophysiology.

[8]  Bin He,et al.  Relationship between speed and EEG activity during imagined and executed hand movements , 2010, Journal of neural engineering.

[9]  Nicholas P. Szrama,et al.  Decoding three-dimensional reaching movements using electrocorticographic signals in humans , 2016, Journal of neural engineering.

[10]  Donald Eugene. Farrar,et al.  Multicollinearity in Regression Analysis; the Problem Revisited , 2011 .

[11]  N. Thakor,et al.  Electrocorticographic amplitude predicts finger positions during slow grasping motions of the hand , 2010, Journal of neural engineering.

[12]  Nitish V. Thakor,et al.  Coarse Electrocorticographic Decoding of Ipsilateral Reach in Patients with Brain Lesions , 2014, PloS one.

[13]  Dan Wu,et al.  Combining Spatial Filters for the Classification of Single-Trial EEG in a Finger Movement Task , 2007, IEEE Transactions on Biomedical Engineering.

[14]  R. Andersen,et al.  Decoding motor imagery from the posterior parietal cortex of a tetraplegic human , 2015, Science.

[15]  J. Wolpaw,et al.  Decoding two-dimensional movement trajectories using electrocorticographic signals in humans , 2007, Journal of neural engineering.

[16]  Jason Farquhar,et al.  Detection of event-related desynchronization during attempted and imagined movements in tetraplegics for brain switch control , 2012, 2012 Annual International Conference of the IEEE Engineering in Medicine and Biology Society.

[17]  Jon A. Mukand,et al.  Neuronal ensemble control of prosthetic devices by a human with tetraplegia , 2006, Nature.

[18]  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.

[19]  Bin He,et al.  EEG Source Imaging Enhances the Decoding of Complex Right-Hand Motor Imagery Tasks , 2016, IEEE Transactions on Biomedical Engineering.

[20]  C. Braun,et al.  Hand Movement Direction Decoded from MEG and EEG , 2008, The Journal of Neuroscience.

[21]  John Van Ness,et al.  The Use of Shrinkage Estimators in Linear Discriminant Analysis , 1982, IEEE Transactions on Pattern Analysis and Machine Intelligence.

[22]  R. Andersen,et al.  Multimodal representation of space in the posterior parietal cortex and its use in planning movements. , 1997, Annual review of neuroscience.

[23]  C. Mehring,et al.  Differential Representation of Arm Movement Direction in Relation to Cortical Anatomy and Function , 2008 .

[24]  Richard M. Leahy,et al.  Brainstorm: A User-Friendly Application for MEG/EEG Analysis , 2011, Comput. Intell. Neurosci..

[25]  Stefan Haufe,et al.  Single-trial analysis and classification of ERP components — A tutorial , 2011, NeuroImage.

[26]  Gernot R. Müller-Putz,et al.  Decoding of velocities and positions of 3D arm movement from EEG , 2012, 2012 Annual International Conference of the IEEE Engineering in Medicine and Biology Society.

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

[28]  Yasuharu Koike,et al.  Prediction of Muscle Activities from Electrocorticograms in Primary Motor Cortex of Primates , 2012, PloS one.

[29]  Aleksandra Vučković,et al.  A two-stage four-class BCI based on imaginary movements of the left and the right wrist. , 2012, Medical engineering & physics.

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

[31]  R D Pascual-Marqui,et al.  Standardized low-resolution brain electromagnetic tomography (sLORETA): technical details. , 2002, Methods and findings in experimental and clinical pharmacology.

[32]  Andrew Y. Paek,et al.  Global cortical activity predicts shape of hand during grasping , 2015, Front. Neurosci..

[33]  Trent J. Bradberry,et al.  Reconstructing Three-Dimensional Hand Movements from Noninvasive Electroencephalographic Signals , 2010, The Journal of Neuroscience.

[34]  M. Alexander,et al.  Principles of Neural Science , 1981 .

[35]  Gernot R. Müller-Putz,et al.  Using a Noninvasive Decoding Method to Classify Rhythmic Movement Imaginations of the Arm in Two Planes , 2015, IEEE Transactions on Biomedical Engineering.

[36]  Gernot R. Müller-Putz,et al.  Movement target decoding from EEG and the corresponding discriminative sources: A preliminary study , 2015, 2015 37th Annual International Conference of the IEEE Engineering in Medicine and Biology Society (EMBC).

[37]  M. Murray,et al.  EEG source imaging , 2004, Clinical Neurophysiology.

[38]  Carlo Menon,et al.  EEG Classification of Different Imaginary Movements within the Same Limb , 2015, PloS one.

[39]  Zhaohui Wu,et al.  The Convergence of Machine and Biological Intelligence , 2013, IEEE Intelligent Systems.

[40]  Vera Kaiser,et al.  Hybrid brain-computer interfaces and hybrid neuroprostheses for restoration of upper limb functions in individuals with high-level spinal cord injury , 2013, Artif. Intell. Medicine.

[41]  Dario Farina,et al.  Detecting and classifying movement-related cortical potentials associated with hand movements in healthy subjects and stroke patients from single-electrode, single-trial EEG , 2015, Journal of neural engineering.

[42]  Kojiro Matsushita,et al.  Common neural correlates of real and imagined movements contributing to the performance of brain–machine interfaces , 2016, Scientific Reports.

[43]  G. Pfurtscheller,et al.  EEG-based neuroprosthesis control: A step towards clinical practice , 2005, Neuroscience Letters.

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

[45]  Clemens Brunner,et al.  Better than random? A closer look on BCI results , 2008 .

[46]  K. Strimmer,et al.  Statistical Applications in Genetics and Molecular Biology A Shrinkage Approach to Large-Scale Covariance Matrix Estimation and Implications for Functional Genomics , 2011 .

[47]  Gernot R. Müller-Putz,et al.  Functional Rehabilitation of the Paralyzed Upper Extremity After Spinal Cord Injury by Noninvasive Hybrid Neuroprostheses , 2015, Proceedings of the IEEE.

[48]  Reinhold Scherer,et al.  EEG Oscillations Are Modulated in Different Behavior-Related Networks during Rhythmic Finger Movements , 2016, The Journal of Neuroscience.

[49]  R Rupp,et al.  Neuroprosthetics of the upper extremity--clinical application in spinal cord injury and challenges for the future. , 2007, Acta neurochirurgica. Supplement.

[50]  J L Pons,et al.  Detection of the onset of upper-limb movements based on the combined analysis of changes in the sensorimotor rhythms and slow cortical potentials , 2014, Journal of neural engineering.

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

[52]  G. Pfurtscheller,et al.  Imagery of motor actions: differential effects of kinesthetic and visual-motor mode of imagery in single-trial EEG. , 2005, Brain research. Cognitive brain research.

[53]  Michael G. Lacourse,et al.  Cortical potentials during imagined movements in individuals with chronic spinal cord injuries , 1999, Behavioural Brain Research.

[54]  Andreas Schulze-Bonhage,et al.  Prediction of arm movement trajectories from ECoG-recordings in humans , 2008, Journal of Neuroscience Methods.

[55]  B. Hjorth An on-line transformation of EEG scalp potentials into orthogonal source derivations. , 1975, Electroencephalography and clinical neurophysiology.

[56]  RP Dum,et al.  The origin of corticospinal projections from the premotor areas in the frontal lobe , 1991, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[57]  Dario Farina,et al.  Offline Identification of Imagined Speed of Wrist Movements in Paralyzed ALS Patients from Single-Trial EEG , 2009, Front. Neuropro..

[58]  Jonathan R Wolpaw,et al.  Control of a two-dimensional movement signal by a noninvasive brain-computer interface in humans. , 2004, Proceedings of the National Academy of Sciences of the United States of America.

[59]  A. Schwartz,et al.  High-performance neuroprosthetic control by an individual with tetraplegia , 2013, The Lancet.

[60]  Dario Farina,et al.  Single-trial discrimination of type and speed of wrist movements from EEG recordings , 2009, Clinical Neurophysiology.

[61]  M L Boninger,et al.  Ten-dimensional anthropomorphic arm control in a human brain−machine interface: difficulties, solutions, and limitations , 2015, Journal of neural engineering.

[62]  Christa Neuper,et al.  Distinct β Band Oscillatory Networks Subserving Motor and Cognitive Control during Gait Adaptation , 2016, The Journal of Neuroscience.

[63]  G. Pfurtscheller,et al.  ‘Thought’ – control of functional electrical stimulation to restore hand grasp in a patient with tetraplegia , 2003, Neuroscience Letters.

[64]  G. R. Muller,et al.  Brain oscillations control hand orthosis in a tetraplegic , 2000, Neuroscience Letters.

[65]  Nicolas Y. Masse,et al.  Reach and grasp by people with tetraplegia using a neurally controlled robotic arm , 2012, Nature.

[66]  Á. Gil-Agudo,et al.  Continuous decoding of movement intention of upper limb self-initiated analytic movements from pre-movement EEG correlates , 2014, Journal of NeuroEngineering and Rehabilitation.