High-resolution EEG techniques for brain–computer interface applications

High-resolution electroencephalographic (HREEG) techniques allow estimation of cortical activity based on non-invasive scalp potential measurements, using appropriate models of volume conduction and of neuroelectrical sources. In this study we propose an application of this body of technologies, originally developed to obtain functional images of the brain's electrical activity, in the context of brain-computer interfaces (BCI). Our working hypothesis predicted that, since HREEG pre-processing removes spatial correlation introduced by current conduction in the head structures, by providing the BCI with waveforms that are mostly due to the unmixed activity of a small cortical region, a more reliable classification would be obtained, at least when the activity to detect has a limited generator, which is the case in motor related tasks. HREEG techniques employed in this study rely on (i) individual head models derived from anatomical magnetic resonance images, (ii) distributed source model, composed of a layer of current dipoles, geometrically constrained to the cortical mantle, (iii) depth-weighted minimum L(2)-norm constraint and Tikhonov regularization for linear inverse problem solution and (iv) estimation of electrical activity in cortical regions of interest corresponding to relevant Brodmann areas. Six subjects were trained to learn self modulation of sensorimotor EEG rhythms, related to the imagination of limb movements. Off-line EEG data was used to estimate waveforms of cortical activity (cortical current density, CCD) on selected regions of interest. CCD waveforms were fed into the BCI computational pipeline as an alternative to raw EEG signals; spectral features are evaluated through statistical tests (r(2) analysis), to quantify their reliability for BCI control. These results are compared, within subjects, to analogous results obtained without HREEG techniques. The processing procedure was designed in such a way that computations could be split into a setup phase (which includes most of the computational burden) and the actual EEG processing phase, which was limited to a single matrix multiplication. This separation allowed to make the procedure suitable for on-line utilization, and a pilot experiment was performed. Results show that lateralization of electrical activity, which is expected to be contralateral to the imagined movement, is more evident on the estimated CCDs than in the scalp potentials. CCDs produce a pattern of relevant spectral features that is more spatially focused, and has a higher statistical significance (EEG: 0.20+/-0.114 S.D.; CCD: 0.55+/-0.16 S.D.; p=10(-5)). A pilot experiment showed that a trained subject could utilize voluntary modulation of estimated CCDs for accurate (eight targets) on-line control of a cursor. This study showed that it is practically feasible to utilize HREEG techniques for on-line operation of a BCI system; off-line analysis suggests that accuracy of BCI control is enhanced by the proposed method.

[1]  Febo Cincotti,et al.  Sub-second "temporal attention" modulates alpha rhythms. A high-resolution EEG study. , 2004, Brain research. Cognitive brain research.

[2]  A Urbano,et al.  Responses of human primary sensorimotor and supplementary motor areas to internally triggered unilateral and simultaneous bilateral one-digit movements. A high-resolution EEG study. , 1997, The European journal of neuroscience.

[3]  Jonathan R Wolpaw,et al.  Brain–computer interfaces as new brain output pathways , 2007, The Journal of physiology.

[4]  F. Babiloni,et al.  Estimation of the cortical functional connectivity with the multimodal integration of high-resolution EEG and fMRI data by directed transfer function , 2005, NeuroImage.

[5]  Anders M. Dale,et al.  Improved Localization of Cortical Activity By Combining EEG and MEG with MRI Cortical Surface Reconstruction , 2002 .

[6]  R Grave de Peralta Menendez,et al.  Imaging the electrical activity of the brain: ELECTRA , 2000, Human brain mapping.

[7]  L. Cohen,et al.  Brain–computer interfaces: communication and restoration of movement in paralysis , 2007, The Journal of physiology.

[8]  C. Uhl Analysis of neurophysiological brain functioning , 1999 .

[9]  José del R. Millán,et al.  Very high frequency oscillations (VHFO) as a predictor of movement intentions , 2006, NeuroImage.

[10]  A. Dale,et al.  Improved Localizadon of Cortical Activity by Combining EEG and MEG with MRI Cortical Surface Reconstruction: A Linear Approach , 1993, Journal of Cognitive Neuroscience.

[11]  J. Mourino,et al.  Asynchronous BCI and local neural classifiers: an overview of the adaptive brain interface project , 2003, IEEE Transactions on Neural Systems and Rehabilitation Engineering.

[12]  Febo Cincotti,et al.  Motor‐related cortical dynamics to intact movements in tetraplegics as revealed by high‐resolution EEG , 2006, Human brain mapping.

[13]  Jonathan R. Wolpaw,et al.  Brain-computer interfaces (BCIs) for communication and control , 2007, Assets '07.

[14]  F Cincotti,et al.  EEG Deblurring Techniques in a Clinical Context , 2004, Methods of Information in Medicine.

[15]  G. Pfurtscheller,et al.  Brain-Computer Interfaces for Communication and Control. , 2011, Communications of the ACM.

[16]  P. Hansen Numerical tools for analysis and solution of Fredholm integral equations of the first kind , 1992 .

[17]  E. Halgren,et al.  Dynamic Statistical Parametric Mapping Combining fMRI and MEG for High-Resolution Imaging of Cortical Activity , 2000, Neuron.

[18]  José del R. Millán,et al.  Noninvasive brain-actuated control of a mobile robot by human EEG , 2004, IEEE Transactions on Biomedical Engineering.

[19]  W. J. Nowack Neocortical Dynamics and Human EEG Rhythms , 1995, Neurology.

[20]  S. G. Andino,et al.  Distributed Source Models: Standard Solutions and New Developments , 1999 .

[21]  P. Strick,et al.  Imaging the premotor areas , 2001, Current Opinion in Neurobiology.

[22]  F. Cincotti,et al.  The use of EEG modifications due to motor imagery for brain-computer interfaces , 2003, IEEE Transactions on Neural Systems and Rehabilitation Engineering.

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

[24]  Thom F. Oostendorp,et al.  The conductivity of the human skull: results of in vivo and in vitro measurements , 2000, IEEE Transactions on Biomedical Engineering.

[25]  Febo Cincotti,et al.  Human Cortical Electroencephalography (EEG) Rhythms during the Observation of Simple Aimless Movements: A High-Resolution EEG Study , 2002, NeuroImage.

[26]  Jukka Heikkonen,et al.  A local neural classifier for the recognition of EEG patterns associated to mental tasks , 2002, IEEE Trans. Neural Networks.

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

[28]  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.

[29]  M. Fuchs,et al.  Development of Volume Conductor and Source Models to Localize Epileptic Foci , 2007, Journal of clinical neurophysiology : official publication of the American Electroencephalographic Society.

[30]  D J McFarland,et al.  An EEG-based brain-computer interface for cursor control. , 1991, Electroencephalography and clinical neurophysiology.

[31]  Per Christian Hansen,et al.  Analysis of Discrete Ill-Posed Problems by Means of the L-Curve , 1992, SIAM Rev..

[32]  F Babiloni,et al.  Classification of EEG Mental Patterns by Using Two Scalp Electrodes and Mahalanobis Distance-Based Classifiers , 2002, Methods of Information in Medicine.

[33]  P. Rossini,et al.  High-resolution electro-encephalogram: source estimates of Laplacian-transformed somatosensory-evoked potentials using a realistic subject head model constructed from magnetic resonance images , 2000, Medical and Biological Engineering and Computing.

[34]  S. Rossi,et al.  Human cortical responses during one-bit short-term memory. A high-resolution EEG study on delayed choice reaction time tasks , 2004, Clinical Neurophysiology.

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