Pre-Stimulus Sensorimotor Rhythms Influence Brain–Computer Interface Classification Performance

The influence of pre-stimulus ongoing brain activity on post-stimulus task performance has recently been analyzed in several studies. While pre-stimulus activity in the parieto-occipital area has been exhaustively investigated with congruent results, less is known about the sensorimotor areas, for which studies reported inconsistent findings. In this work, the topic is addressed in a brain-computer interface (BCI) setting based on modulations of sensorimotor rhythms (SMR). The goal is to assess whether and how pre-stimulus SMR activity influences the successive task execution quality and consequently the classification performance. Grand average data of 23 participants performing right and left hand motor imagery were analyzed. Trials were separated into two groups depending on the SMR amplitude in the 1000 ms interval preceding the cue, and classification by common spatial patterns (CSPs) preprocessing and linear discriminant analysis (LDA) was carried out in the post-stimulus time interval, i.e., during the task execution. The correlation between trial group and classification performance was assessed by an analysis of variance. As a result of this analysis, trials with higher SMR amplitude in the 1000 ms interval preceding the cue yielded significantly better classification performance than trials with lower amplitude. A further investigation of brain activity patterns revealed that this increase in accuracy is mainly due to the persistence of a higher SMR amplitude over the ipsilateral hemisphere. Our findings support the idea that exploiting information about the ongoing SMR might be the key to boosting performance in future SMR-BCI experiments and motor related tasks in general.

[1]  Dennis J. McFarland,et al.  Design and operation of an EEG-based brain-computer interface with digital signal processing technology , 1997 .

[2]  Benjamin Blankertz,et al.  A Note on Brain Actuated Spelling with the Berlin Brain-Computer Interface , 2007, HCI.

[3]  G. Pfurtscheller,et al.  EEG-based discrimination between imagination of right and left hand movement. , 1997, Electroencephalography and clinical neurophysiology.

[4]  S. Kosslyn,et al.  Reactivity of magnetic parieto-occipital alpha rhythm during visual imagery. , 1995, Electroencephalography and clinical neurophysiology.

[5]  R. Hari,et al.  Spatiotemporal characteristics of sensorimotor neuromagnetic rhythms related to thumb movement , 1994, Neuroscience.

[6]  Simon Hanslmayr,et al.  Prestimulus oscillations predict visual perception performance between and within subjects , 2007, NeuroImage.

[7]  G. Pfurtscheller,et al.  Evidence for distinct beta resonance frequencies in human EEG related to specific sensorimotor cortical areas , 2001, Clinical Neurophysiology.

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

[9]  J. Gross,et al.  On the Role of Prestimulus Alpha Rhythms over Occipito-Parietal Areas in Visual Input Regulation: Correlation or Causation? , 2010, The Journal of Neuroscience.

[10]  J. Schoffelen,et al.  Prestimulus Oscillatory Activity in the Alpha Band Predicts Visual Discrimination Ability , 2008, The Journal of Neuroscience.

[11]  Klaus-Robert Müller,et al.  Machine-Learning-Based Coadaptive Calibration for Brain-Computer Interfaces , 2011, Neural Computation.

[12]  C. Herrmann,et al.  Prestimulus EEG alpha activity reflects prestimulus top-down processing , 2007, Neuroscience Letters.

[13]  Christa Neuper,et al.  Post-movement synchronization of beta rhythms in the EEG over the cortical foot area in man , 1996, Neuroscience Letters.

[14]  Matthias J. Wieser,et al.  Distinct effects of attention and affect on pain perception and somatosensory evoked potentials , 2008, Biological Psychology.

[15]  S. Cochin,et al.  Perception of motion and qEEG activity in human adults. , 1998, Electroencephalography and clinical neurophysiology.

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

[17]  Klaus-Robert Müller,et al.  Neurophysiological predictor of SMR-based BCI performance , 2010, NeuroImage.

[18]  P. Sajda,et al.  Spatiotemporal Linear Decoding of Brain State , 2008, IEEE Signal Processing Magazine.

[19]  H. Jasper,et al.  Electrocorticograms in man: Effect of voluntary movement upon the electrical activity of the precentral gyrus , 1949 .

[20]  K. Linkenkaer-Hansen,et al.  Prestimulus Oscillations Enhance Psychophysical Performance in Humans , 2004, The Journal of Neuroscience.

[21]  D J McFarland,et al.  Brain-computer interface research at the Wadsworth Center. , 2000, IEEE transactions on rehabilitation engineering : a publication of the IEEE Engineering in Medicine and Biology Society.

[22]  Dominique L. Pritchett,et al.  Cued Spatial Attention Drives Functionally Relevant Modulation of the Mu Rhythm in Primary Somatosensory Cortex , 2010, The Journal of Neuroscience.

[23]  Klaus-Robert Müller,et al.  The Berlin Brain-Computer Interface , 2008, WCCI.

[24]  J. Lange,et al.  Fluctuations of prestimulus oscillatory power predict subjective perception of tactile simultaneity. , 2012, Cerebral cortex.

[25]  C. Gerloff,et al.  Enhancing cognitive performance with repetitive transcranial magnetic stimulation at human individual alpha frequency , 2003, The European journal of neuroscience.

[26]  Yan Zhang,et al.  Detection of a Weak Somatosensory Stimulus: Role of the Prestimulus Mu Rhythm and Its Top–Down Modulation , 2010, Journal of Cognitive Neuroscience.

[27]  G. Pfurtscheller,et al.  Functional dissociation of lower and upper frequency mu rhythms in relation to voluntary limb movement , 2000, Clinical Neurophysiology.

[28]  G. Pfurtscheller,et al.  Motor imagery activates primary sensorimotor area in humans , 1997, Neuroscience Letters.

[29]  Hermann Ackermann,et al.  The role of the unaffected hemisphere in motor recovery after stroke , 2010, Human brain mapping.

[30]  Arno Villringer,et al.  Oscillatory brain states interact with late cognitive components of the somatosensory evoked potential , 2009, Journal of Neuroscience Methods.

[31]  R. Hari,et al.  Human cortical oscillations: a neuromagnetic view through the skull , 1997, Trends in Neurosciences.

[32]  C. Braun,et al.  Somatosensory event-related potentials to painful and non-painful stimuli: effects of attention , 1989, Pain.

[33]  Stefan Haufe,et al.  Parieto-occipital alpha power indexes distraction during simulated car driving , 2008 .

[34]  B. Allison,et al.  The effects of self-movement, observation, and imagination on mu rhythms and readiness potentials (RP's): toward a brain-computer interface (BCI). , 2000, IEEE transactions on rehabilitation engineering : a publication of the IEEE Engineering in Medicine and Biology Society.

[35]  Klaus-Robert Müller,et al.  The non-invasive Berlin Brain–Computer Interface: Fast acquisition of effective performance in untrained subjects , 2007, NeuroImage.

[36]  K. Müller,et al.  Psychological predictors of SMR-BCI performance , 2012, Biological Psychology.

[37]  J. Conradia,et al.  Brain-Computer Interfacing in Tetraplegic Patients with High Spinal Cord Injury , 2009 .

[38]  Klaus Linkenkaer-Hansen,et al.  Dynamics of mu-rhythm suppression caused by median nerve stimulation: a magnetoencephalographic study in human subjects , 2000, Neuroscience Letters.

[39]  G. Pfurtscheller,et al.  Enhancement of left-right sensorimotor EEG differences during feedback-regulated motor imagery. , 1999, Journal of clinical neurophysiology : official publication of the American Electroencephalographic Society.

[40]  Klaus-Robert Müller,et al.  Machine-Learning Based Co-adaptive Calibration : Towards a Cure for BCI illiteracy , 2010 .

[41]  W. A. Sarnacki,et al.  Electroencephalographic (EEG) control of three-dimensional movement , 2010, Journal of neural engineering.

[42]  R. Hari,et al.  Functional Segregation of Movement-Related Rhythmic Activity in the Human Brain , 1995, NeuroImage.

[43]  J. Wolpaw,et al.  Patients with ALS can use sensorimotor rhythms to operate a brain-computer interface , 2005, Neurology.

[44]  F. L. D. Silva,et al.  Beta rebound after different types of motor imagery in man , 2005, Neuroscience Letters.

[45]  J. Wolpaw,et al.  Mu and Beta Rhythm Topographies During Motor Imagery and Actual Movements , 2004, Brain Topography.

[46]  G Pfurtscheller,et al.  Computational model of thalamo-cortical networks: dynamical control of alpha rhythms in relation to focal attention. , 2001, International journal of psychophysiology : official journal of the International Organization of Psychophysiology.

[47]  G. Pfurtscheller,et al.  Event-related dynamics of cortical rhythms: frequency-specific features and functional correlates. , 2001, International journal of psychophysiology : official journal of the International Organization of Psychophysiology.

[48]  Diane M. Beck,et al.  To See or Not to See: Prestimulus α Phase Predicts Visual Awareness , 2009, The Journal of Neuroscience.

[49]  Wolfgang Klimesch,et al.  The Functional Significance of Absolute Power with Respect to Event-Related Desynchronization , 2004, Brain Topography.

[50]  Yan Zhang,et al.  Prestimulus Cortical Activity is Correlated with Speed of Visuomotor Processing , 2008, Journal of Cognitive Neuroscience.

[51]  G. Pfurtscheller,et al.  Post-movement beta synchronization. A correlate of an idling motor area? , 1996, Electroencephalography and clinical neurophysiology.

[52]  Gert Pfurtscheller,et al.  Walking from thought , 2006, Brain Research.

[53]  Manuel Schabus,et al.  Increasing Individual Upper Alpha Power by Neurofeedback Improves Cognitive Performance in Human Subjects , 2005, Applied psychophysiology and biofeedback.

[54]  Ethan R. Buch,et al.  Think to Move: a Neuromagnetic Brain-Computer Interface (BCI) System for Chronic Stroke , 2008, Stroke.

[55]  Dragan F. Dimitrov,et al.  Cortical Representation of Ipsilateral Arm Movements in Monkey and Man , 2009, The Journal of Neuroscience.

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

[57]  G. Pfurtscheller,et al.  Optimal spatial filtering of single trial EEG during imagined hand movement. , 2000, IEEE transactions on rehabilitation engineering : a publication of the IEEE Engineering in Medicine and Biology Society.

[58]  R. Harper,et al.  Somatomotor and visceromotor correlates of operantly conditioned 12-14 C-SEC sensorimotor cortical activity. , 1971, Electroencephalography and clinical neurophysiology.

[59]  Claudio Del Percio,et al.  Pre-stimulus alpha rhythms are correlated with post-stimulus sensorimotor performance in athletes and non-athletes: A high-resolution EEG study , 2007, Clinical Neurophysiology.

[60]  Wolfgang Klimesch,et al.  Interindividual Differences in Alpha and Theta Power Reflect Memory Performance. , 1999 .

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

[62]  W. Klimesch,et al.  Visual discrimination performance is related to decreased alpha amplitude but increased phase locking , 2005, Neuroscience Letters.

[63]  A. Haig,et al.  Prestimulus EEG alpha phase synchronicity influences N100 amplitude and reaction time. , 1998, Psychophysiology.

[64]  O. Jensen,et al.  Prestimulus alpha and mu activity predicts failure to inhibit motor responses , 2009, Human brain mapping.

[65]  M Doppelmayr,et al.  High-frequency components in the alpha band and memory performance. , 1998, Journal of clinical neurophysiology : official publication of the American Electroencephalographic Society.

[66]  T. Ergenoğlu,et al.  Alpha rhythm of the EEG modulates visual detection performance in humans. , 2004, Brain research. Cognitive brain research.

[67]  G. Pfurtscheller,et al.  Brain motor system function in a patient with complete spinal cord injury following extensive brain–computer interface training , 2008, Experimental Brain Research.

[68]  V. Jousmäki,et al.  Involvement of Primary Motor Cortex in Motor Imagery: A Neuromagnetic Study , 1997, NeuroImage.

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

[70]  Benjamin Blankertz,et al.  Designing for uncertain, asymmetric control: Interaction design for brain-computer interfaces , 2009, Int. J. Hum. Comput. Stud..

[71]  K.-R. Muller,et al.  Optimizing Spatial filters for Robust EEG Single-Trial Analysis , 2008, IEEE Signal Processing Magazine.