Decoding the Attentional Demands of Gait through EEG Gamma Band Features

Rehabilitation techniques are evolving focused on improving their performance in terms of duration and level of recovery. Current studies encourage the patient’s involvement in their rehabilitation. Brain-Computer Interfaces are capable of decoding the cognitive state of users to provide feedback to an external device. On this paper, cortical information obtained from the scalp is acquired with the goal of studying the cognitive mechanisms related to the users’ attention to the gait. Data from 10 healthy users and 3 incomplete Spinal Cord Injury patients are acquired during treadmill walking. During gait, users are asked to perform 4 attentional tasks. Data obtained are treated to reduce movement artifacts. Features from δ(1 − 4Hz), θ(4 − 8Hz), α(8 − 12Hz), β(12 − 30Hz), γlow(30 − 50Hz), γhigh(50 − 90Hz) frequency bands are extracted and analyzed to find which ones provide more information related to attention. The selected bands are tested with 5 classifiers to distinguish between tasks. Classification results are also compared with chance levels to evaluate performance. Results show success rates of ∼67% for healthy users and ∼59% for patients. These values are obtained using features from γ band suggesting that the attention mechanisms are related to selective attention mechanisms, meaning that, while the attention on gait decreases the level of attention on the environment and external visual information increases. Linear Discriminant Analysis, K-Nearest Neighbors and Support Vector Machine classifiers provide the best results for all users. Results from patients are slightly lower, but significantly different, than those obtained from healthy users supporting the idea that the patients pay more attention to gait during non-attentional tasks due to the inherent difficulties they have during normal gait. This study provides evidence of the existence of classifiable cortical information related to the attention level on the gait. This fact could allow the development of a real-time system that obtains the attention level during lower limb rehabilitation. This information could be used as feedback to adapt the rehabilitation strategy.

[1]  郑肇葆,et al.  基于Naive Bayes Classifiers的航空影像纹理分类 , 2006 .

[2]  T. Shakespeare,et al.  Editorial , 2011, Disability and rehabilitation.

[3]  D. Yao,et al.  A method to standardize a reference of scalp EEG recordings to a point at infinity , 2001, Physiological measurement.

[4]  T. Kailath The Divergence and Bhattacharyya Distance Measures in Signal Selection , 1967 .

[5]  W J Ray,et al.  EEG activity during cognitive processing: influence of attentional factors. , 1985, International journal of psychophysiology : official journal of the International Organization of Psychophysiology.

[6]  M. Woollacott,et al.  Attention and the control of posture and gait: a review of an emerging area of research. , 2002, Gait & posture.

[7]  G. J. Daniell,et al.  μSR frequency spectra using the maximum entropy method , 1994 .

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

[9]  G. Steinbeck,et al.  Frequency analysis of the electrocardiogram with maximum entropy method for identification of patients with sustained ventricular tachycardia , 1991, IEEE Transactions on Biomedical Engineering.

[10]  N. Westgren,et al.  Quality of life and traumatic spinal cord injury. , 1998, Archives of physical medicine and rehabilitation.

[11]  Klaas Postema,et al.  Improving rehabilitation treatment in a local setting: a case study of prosthetic rehabilitation , 2009, Clinical rehabilitation.

[12]  Chung-Hung Hsieh,et al.  A Kinect-Based System for Physical Rehabilitation: Utilizing Tai Chi Exercises to Improve Movement Disorders in Patients with Balance Ability , 2013, 2013 7th Asia Modelling Symposium.

[13]  K. Cicerone,et al.  Attention deficits and dual task demands after mild traumatic brain injury. , 1996, Brain injury.

[14]  Jeffrey M. Hausdorff,et al.  The role of executive function and attention in gait , 2008, Movement disorders : official journal of the Movement Disorder Society.

[15]  W. Klimesch,et al.  Induced alpha band power changes in the human EEG and attention , 1998, Neuroscience Letters.

[16]  Alexa B. Roggeveen,et al.  Large-scale gamma-band phase synchronization and selective attention. , 2008, Cerebral cortex.

[17]  A Curt,et al.  How does the human brain deal with a spinal cord injury? , 1998, The European journal of neuroscience.

[18]  W. Ray,et al.  EEG alpha activity reflects attentional demands, and beta activity reflects emotional and cognitive processes. , 1985, Science.

[19]  R. Riener,et al.  Virtual environments increase participation of children with cerebral palsy in robot-aided treadmill training , 2008, 2008 Virtual Rehabilitation.

[20]  Elizabeth D. Kay,et al.  Improving Rehabilitation Services in Developing Nations: The proposed role of physiotherapists , 1994 .

[21]  P. Fries,et al.  Is synchronized neuronal gamma activity relevant for selective attention? , 2003, Brain Research Reviews.

[22]  G. L. Tangonan,et al.  A study on ocular and facial muscle artifacts in EEG signals for BCI applications , 2012, TENCON 2012 IEEE Region 10 Conference.

[23]  G. Chaudhuri,et al.  Bhattacharyya distance based linear discriminant function for stationary time series , 1991 .

[24]  Lalit Kalra,et al.  Improving Stroke Rehabilitation: A Controlled Study , 1993, Stroke.

[25]  Sarah Jane Delany k-Nearest Neighbour Classifiers , 2007 .

[26]  A. Genz,et al.  Numerical evaluation of singular multivariate normal distributions , 2000 .

[27]  T. Gasser,et al.  The transfer of EOG activity into the EEG for eyes open and closed. , 1985, Electroencephalography and clinical neurophysiology.

[28]  Matthias M. Müller,et al.  Modulation of induced gamma band activity in the human EEG by attention and visual information processing. , 2000, International journal of psychophysiology : official journal of the International Organization of Psychophysiology.

[29]  Matthias M. Müller,et al.  Selective visual-spatial attention alters induced gamma band responses in the human EEG , 1999, Clinical Neurophysiology.

[30]  Richard Stephenson,et al.  A review of neuroplasticity: some implications for physiotherapy in the treatment of lesions of the brain , 1993 .

[31]  Wojciech Samek,et al.  Transferring Subspaces Between Subjects in Brain--Computer Interfacing , 2012, IEEE Transactions on Biomedical Engineering.

[32]  J Holsheimer,et al.  Volume conduction and EEG measurements within the brain: a quantitative approach to the influence of electrical spread on the linear relationship of activity measured at different locations. , 1977, Electroencephalography and clinical neurophysiology.

[33]  J. Wolpaw,et al.  Brain–computer interfaces in neurological rehabilitation , 2008, The Lancet Neurology.

[34]  A. Thomé SVM Classifiers – Concepts and Applications to Character Recognition , 2012 .

[35]  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.

[36]  Li-Shan Chou,et al.  The effect of divided attention on gait stability following concussion. , 2005, Clinical biomechanics.

[37]  Richard B. Reilly,et al.  Measurement of attention during movement: Acquisition of ambulatory EEG and cognitive performance from healthy young adults , 2013, 2013 35th Annual International Conference of the IEEE Engineering in Medicine and Biology Society (EMBC).

[38]  B. Dobkin Brain–computer interface technology as a tool to augment plasticity and outcomes for neurological rehabilitation , 2007, The Journal of physiology.

[39]  F. L. D. Silva,et al.  EEG signal processing , 2000, Clinical Neurophysiology.

[40]  Jeffrey M. Hausdorff,et al.  Dual‐tasking effects on gait variability: The role of aging, falls, and executive function , 2006, Movement disorders : official journal of the Movement Disorder Society.

[41]  J. A. Stevens,et al.  Using motor imagery in the rehabilitation of hemiparesis. , 2003, Archives of physical medicine and rehabilitation.

[42]  L. Cohen,et al.  Neuroplasticity in the context of motor rehabilitation after stroke , 2011, Nature Reviews Neurology.

[43]  J. Polich,et al.  Attention, probability, and task demands as determinants of P300 latency from auditory stimuli. , 1986, Electroencephalography and clinical neurophysiology.

[44]  Leigh Blizzard,et al.  Cognitive function, gait, and gait variability in older people: a population-based study. , 2013, The journals of gerontology. Series A, Biological sciences and medical sciences.

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

[46]  Daniel P Ferris,et al.  Isolating gait-related movement artifacts in electroencephalography during human walking , 2015, Journal of neural engineering.

[47]  H. Gray,et al.  P300 as an index of attention to self-relevant stimuli , 2004 .

[48]  David A. Landgrebe,et al.  A survey of decision tree classifier methodology , 1991, IEEE Trans. Syst. Man Cybern..

[49]  Robert Riener,et al.  Virtual reality and gait rehabilitation Augmented feedback for the Lokomat , 2009, 2009 Virtual Rehabilitation International Conference.

[50]  R. Karandikar,et al.  Sankhyā, The Indian Journal of Statistics , 2006 .

[51]  M. Diamond,et al.  Primary Motor and Sensory Cortex Activation during Motor Performance and Motor Imagery: A Functional Magnetic Resonance Imaging Study , 1996, The Journal of Neuroscience.

[52]  B. Scholkopf,et al.  Fisher discriminant analysis with kernels , 1999, Neural Networks for Signal Processing IX: Proceedings of the 1999 IEEE Signal Processing Society Workshop (Cat. No.98TH8468).

[53]  W. Frontera The world report on disability. , 2012, American journal of physical medicine & rehabilitation.

[54]  Haim Ring,et al.  Rehabilitation outcome of elderly patients after a first stroke: effect of cognitive status at admission on the functional outcome. , 2002, Archives of physical medicine and rehabilitation.

[55]  Guorong Xuan,et al.  Bhattacharyya distance feature selection , 1996, ICPR.

[56]  Jan K. Buitelaar,et al.  The increase in theta/beta ratio on resting-state EEG in boys with attention-deficit/hyperactivity disorder is mediated by slow alpha peak frequency , 2011, Progress in Neuro-Psychopharmacology and Biological Psychiatry.

[57]  P. Brown,et al.  EEG–EMG, MEG–EMG and EMG–EMG frequency analysis: physiological principles and clinical applications , 2002, Clinical Neurophysiology.

[58]  Cuntai Guan,et al.  A clinical study of motor imagery-based brain-computer interface for upper limb robotic rehabilitation , 2009, 2009 Annual International Conference of the IEEE Engineering in Medicine and Biology Society.

[59]  L Garnero,et al.  Spatial extension of brain activity fools the single‐channel reconstruction of EEG dynamics , 1997, Human brain mapping.

[60]  Andrés Úbeda,et al.  Development of a Low-cost SVM-based Spontaneous Brain-computer Interface , 2011, IJCCI.

[61]  László Györfi,et al.  Lower Bounds for Bayes Error Estimation , 1999, IEEE Trans. Pattern Anal. Mach. Intell..

[62]  Chulhee Lee,et al.  Feature extraction based on the Bhattacharyya distance , 2003, Pattern Recognit..

[63]  Kilseop Ryu,et al.  Evaluation of mental workload with a combined measure based on physiological indices during a dual task of tracking and mental arithmetic , 2005 .

[64]  Ronald C Petersen,et al.  Assessing the temporal relationship between cognition and gait: slow gait predicts cognitive decline in the Mayo Clinic Study of Aging. , 2013, The journals of gerontology. Series A, Biological sciences and medical sciences.

[65]  Cuntai Guan,et al.  Spatially Regularized Common Spatial Patterns for EEG Classification , 2010, 2010 20th International Conference on Pattern Recognition.