Neural decoding of robot-assisted gait during rehabilitation after stroke

Objective·. Recent advances in robot-assisted gait rehabilitation and brain-machine interfaces (BMI) promise to increase the quality of life of people with deficits in bipedal locomotion such as in stroke survivors. Moreover, BMI systems may enhance stroke neurorehabilitation by engaging the user while providing valuable information about cortical adaptations and neural plasticity resulting from robot use. However, the feasibility of decoding walking from brain activity of stroke survivors during robot-assisted gait therapy is unknown. To address this gap, we designed a study to investigate the feasibility of decoding gait kinematics from chronic stroke patients undergoing gait rehabilitation based on a lower extremity gait system (H2 NeuroExo) integrated with a noninvasive neural interface based on electroencephalography (EEG).

[1]  J. Borg,et al.  Gait training early after stroke with a new exoskeleton – the hybrid assistive limb: a study of safety and feasibility , 2014, Journal of NeuroEngineering and Rehabilitation.

[2]  T. Demott,et al.  Enhanced Gait-Related Improvements After Therapist- Versus Robotic-Assisted Locomotor Training in Subjects With Chronic Stroke: A Randomized Controlled Study , 2008, Stroke.

[3]  A. Bastian Understanding sensorimotor adaptation and learning for rehabilitation , 2008, Current opinion in neurology.

[4]  Bram Koopman,et al.  Selective control of gait subtasks in robotic gait training: foot clearance support in stroke survivors with a powered exoskeleton , 2013, Journal of NeuroEngineering and Rehabilitation.

[5]  Daniel P. Ferris,et al.  Electrocortical activity is coupled to gait cycle phase during treadmill walking , 2011, NeuroImage.

[6]  Christa Neuper,et al.  Level of participation in robotic-assisted treadmill walking modulates midline sensorimotor EEG rhythms in able-bodied subjects , 2012, NeuroImage.

[7]  Jeremy C. Rietschel,et al.  Increased reward in ankle robotics training enhances motor control and cortical efficiency in stroke. , 2014, Journal of rehabilitation research and development.

[8]  D. Farina,et al.  Precise temporal association between cortical potentials evoked by motor imagination and afference induces cortical plasticity , 2012, The Journal of physiology.

[9]  J. Moreno,et al.  The H2 robotic exoskeleton for gait rehabilitation after stroke: early findings from a clinical study , 2015, Journal of NeuroEngineering and Rehabilitation.

[10]  Atilla Kilicarslan,et al.  A robust adaptive denoising framework for real-time artifact removal in scalp EEG measurements , 2016, Journal of neural engineering.

[11]  Pamela W Duncan,et al.  Management of Adult Stroke Rehabilitation Care: a clinical practice guideline. , 2005, Stroke.

[12]  D. Farina,et al.  A brain–computer interface for single-trial detection of gait initiation from movement related cortical potentials , 2015, Clinical Neurophysiology.

[13]  D. Lefeber,et al.  Human-Robot Interaction: Does Robotic Guidance Force Affect Gait-Related Brain Dynamics during Robot-Assisted Treadmill Walking? , 2015, PloS one.

[14]  I. Tarkka,et al.  The effectiveness of body weight-supported gait training and floor walking in patients with chronic stroke. , 2005, Archives of physical medicine and rehabilitation.

[15]  J. Wolpaw,et al.  EMG contamination of EEG: spectral and topographical characteristics , 2003, Clinical Neurophysiology.

[16]  M. Nicolelis,et al.  Unscented Kalman Filter for Brain-Machine Interfaces , 2009, PloS one.

[17]  I. Schwartz,et al.  The Effectiveness of Locomotor Therapy Using Robotic‐Assisted Gait Training in Subacute Stroke Patients: A Randomized Controlled Trial , 2009, PM & R : the journal of injury, function, and rehabilitation.

[18]  Daniel P. Ferris,et al.  Removal of movement artifact from high-density EEG recorded during walking and running. , 2010, Journal of neurophysiology.

[19]  Cordula Werner,et al.  Electromechanical-assisted training for walking after stroke. , 2017, The Cochrane database of systematic reviews.

[20]  Bram Koopman,et al.  The effect of impedance-controlled robotic gait training on walking ability and quality in individuals with chronic incomplete spinal cord injury: an explorative study , 2014, Journal of NeuroEngineering and Rehabilitation.

[21]  Reinhold Scherer,et al.  EEG beta suppression and low gamma modulation are different elements of human upright walking , 2014, Front. Hum. Neurosci..

[22]  Yoshiyuki Sankai,et al.  Pilot study of locomotion improvement using hybrid assistive limb in chronic stroke patients , 2013, BMC Neurology.

[23]  Tzyy-Ping Jung,et al.  Real-time modeling and 3D visualization of source dynamics and connectivity using wearable EEG , 2013, 2013 35th Annual International Conference of the IEEE Engineering in Medicine and Biology Society (EMBC).

[24]  F. Müller,et al.  Effects of Locomotion Training With Assistance of a Robot-Driven Gait Orthosis in Hemiparetic Patients After Stroke: A Randomized Controlled Pilot Study , 2007, Stroke.

[25]  R. Tong,et al.  Effectiveness of gait training using an electromechanical gait trainer, with and without functional electric stimulation, in subacute stroke: a randomized controlled trial. , 2006, Archives of physical medicine and rehabilitation.

[26]  Chris Beck,et al.  An integrated neuro-robotic interface for stroke rehabilitation using the NASA X1 powered lower limb exoskeleton , 2014, 2014 36th Annual International Conference of the IEEE Engineering in Medicine and Biology Society.

[27]  M. Molinari,et al.  Rehabilitation of gait after stroke: a review towards a top-down approach , 2011, Journal of NeuroEngineering and Rehabilitation.

[28]  José Luis Pons Rovira,et al.  A Closed-Loop Brain–Computer Interface Triggering an Active Ankle–Foot Orthosis for Inducing Cortical Neural Plasticity , 2014, IEEE Transactions on Biomedical Engineering.

[29]  H. Thieme Enhanced Gait-Related Improvements After Therapist- versus Robotic-Assisted Locomotor Training in Subjects with Chronic Stroke: A Randomized Controlled Study , 2008 .

[30]  C. Neuper,et al.  It's how you get there: walking down a virtual alley activates premotor and parietal areas , 2014, Front. Hum. Neurosci..

[31]  BrittaHusemann,et al.  Effects of Locomotion Training With Assistance of a Robot-Driven Gait Orthosis in Hemiparetic Patients After Stroke , 2007 .

[32]  J. Contreras-Vidal,et al.  Applications of Brain–Machine Interface Systems in Stroke Recovery and Rehabilitation , 2014, Current Physical Medicine and Rehabilitation Reports.

[33]  A. Mayr,et al.  Prospective, Blinded, Randomized Crossover Study of Gait Rehabilitation in Stroke Patients Using the Lokomat Gait Orthosis , 2007, Neurorehabilitation and neural repair.

[34]  R. Rosenfeld Patients , 2012, Otolaryngology--head and neck surgery : official journal of American Academy of Otolaryngology-Head and Neck Surgery.

[35]  Gregory S Sawicki,et al.  A neuromechanics-based powered ankle exoskeleton to assist walking post-stroke: a feasibility study , 2015, Journal of NeuroEngineering and Rehabilitation.

[36]  Gernot R. Müller-Putz,et al.  High and low gamma EEG oscillations in central sensorimotor areas are conversely modulated during the human gait cycle , 2015, NeuroImage.

[37]  P. Schwenkreis,et al.  Voluntary driven exoskeleton as a new tool for rehabilitation in chronic spinal cord injury: a pilot study. , 2014, The spine journal : official journal of the North American Spine Society.

[38]  Greg Welch,et al.  Welch & Bishop , An Introduction to the Kalman Filter 2 1 The Discrete Kalman Filter In 1960 , 1994 .

[39]  Ronald N. Goodman,et al.  Neural decoding of treadmill walking from noninvasive electroencephalographic signals. , 2011, Journal of neurophysiology.

[40]  Michael Voigt,et al.  Influence of directional orientations during gait initiation and stepping on movement-related cortical potentials , 2005, Behavioural Brain Research.

[41]  Joseph Hidler,et al.  Role of Robotics in Neurorehabilitation. , 2011, Topics in spinal cord injury rehabilitation.

[42]  Rob Labruyère,et al.  Strength training versus robot-assisted gait training after incomplete spinal cord injury: a randomized pilot study in patients depending on walking assistance , 2014, Journal of NeuroEngineering and Rehabilitation.

[43]  Y. Sankai,et al.  Effectiveness of Acute Phase Hybrid Assistive Limb Rehabilitation in Stroke Patients Classified by Paralysis Severity , 2015, Neurologia medico-chirurgica.

[44]  Kelly P Westlake,et al.  Pilot study of Lokomat versus manual-assisted treadmill training for locomotor recovery post-stroke , 2009, Journal of NeuroEngineering and Rehabilitation.

[45]  Atilla Kilicarslan,et al.  High accuracy decoding of user intentions using EEG to control a lower-body exoskeleton , 2013, 2013 35th Annual International Conference of the IEEE Engineering in Medicine and Biology Society (EMBC).

[46]  V. Feigin,et al.  Worldwide stroke incidence and early case fatality reported in 56 population-based studies: a systematic review , 2009, The Lancet Neurology.

[47]  Gernot R. Müller-Putz,et al.  Reconstructing gait cycle patterns from non-invasive recorded low gamma modulations , 2014 .

[48]  S. Hesse,et al.  Treadmill Training With Partial Body Weight Support and an Electromechanical Gait Trainer for Restoration of Gait in Subacute Stroke Patients: A Randomized Crossover Study , 2002, Stroke.

[49]  J. Contreras-Vidal,et al.  Decoding Intra-Limb and Inter-Limb Kinematics During Treadmill Walking From Scalp Electroencephalographic (EEG) Signals , 2012, IEEE Transactions on Neural Systems and Rehabilitation Engineering.

[50]  Jose L. Contreras-Vidal,et al.  Negligible Motion Artifacts in Scalp Electroencephalography (EEG) During Treadmill Walking , 2016, Front. Hum. Neurosci..

[51]  J. Hidler,et al.  Multicenter Randomized Clinical Trial Evaluating the Effectiveness of the Lokomat in Subacute Stroke , 2009, Neurorehabilitation and neural repair.

[52]  Amy L Shortal Recovery of Walking Function in Stroke Patients: The Copenhagen Stroke Study , 1996 .

[53]  Jose L. Contreras-Vidal,et al.  Sitting and standing intention can be decoded from scalp EEG recorded prior to movement execution , 2014, Front. Neurosci..