Rehabilitation of hand in subacute tetraplegic patients based on brain computer interface and functional electrical stimulation: a randomised pilot study

OBJECTIVE To compare neurological and functional outcomes between two groups of hospitalised patients with subacute tetraplegia. APPROACH Seven patients received 20 sessions of brain computer interface (BCI) controlled functional electrical stimulation (FES) while five patients received the same number of sessions of passive FES for both hands. The neurological assessment measures were event related desynchronization (ERD) during movement attempt, Somatosensory evoked potential (SSEP) of the ulnar and median nerve; assessment of hand function involved the range of motion (ROM) of wrist and manual muscle test. MAIN RESULTS Patients in both groups initially had intense ERD during movement attempt that was not restricted to the sensory-motor cortex. Following the treatment, ERD cortical activity restored towards the activity in able-bodied people in BCI-FES group only, remaining wide-spread in FES group. Likewise, SSEP returned in 3 patients in BCI-FES group, having no changes in FES group. The ROM of the wrist improved in both groups. Muscle strength significantly improved for both hands in BCI-FES group. For FES group, a significant improvement was noticed for right hand flexor muscles only. SIGNIFICANCE Combined BCI-FES therapy results in better neurological recovery and better improvement of muscle strength than FES alone. For spinal cord injured patients, BCI-FES should be considered as a therapeutic tool rather than solely a long-term assistive device for the restoration of a lost function.

[1]  Valer Jurcak,et al.  10/20, 10/10, and 10/5 systems revisited: Their validity as relative head-surface-based positioning systems , 2007, NeuroImage.

[2]  J B Green,et al.  Cortical sensorimotor reorganization after spinal cord injury , 1998, Neurology.

[3]  Aleksandra Vuckovic,et al.  Influence of motor imagination on cortical activation during functional electrical stimulation , 2015, Clinical Neurophysiology.

[4]  A. Pavlovic,et al.  Efficient neuroplasticity induction in chronic stroke patients by an associative brain-computer interface. , 2016, Journal of neurophysiology.

[5]  Jayme Knutson,et al.  Neuromuscular Electrical Stimulation for Motor Restoration in Hemiplegia , 2008, Topics in stroke rehabilitation.

[6]  Fei Meng,et al.  A Minimal Set of Electrodes for Motor Imagery BCI to Control an Assistive Device in Chronic Stroke Subjects: A Multi-Session Study , 2011, IEEE Transactions on Neural Systems and Rehabilitation Engineering.

[7]  Steven C Cramer,et al.  Cortical Plasticity Following Motor Skill Learning During Mental Practice in Stroke , 2009, Neurorehabilitation and neural repair.

[8]  Cuntai Guan,et al.  EEG controlled neuromuscular electrical stimulation of the upper limb for stroke patients , 2011 .

[9]  M. Schubert,et al.  Evolution of tibial SSEP after traumatic spinal cord injury: Baseline for clinical trials , 2008, Clinical Neurophysiology.

[10]  Carmen Vidaurre,et al.  BioSig: The Free and Open Source Software Library for Biomedical Signal Processing , 2011, Comput. Intell. Neurosci..

[11]  Aleksandra Vučković,et al.  Hybrid Brain-Computer Interface and Functional Electrical Stimulation for Sensorimotor Training in Participants With Tetraplegia: A Proof-of-Concept Study , 2015, Journal of neurologic physical therapy : JNPT.

[12]  Keinosuke Fukunaga,et al.  Introduction to statistical pattern recognition (2nd ed.) , 1990 .

[13]  S. Page,et al.  Mental Practice in Chronic Stroke: Results of a Randomized, Placebo-Controlled Trial , 2007, Stroke.

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

[15]  Suk-Tak Chan,et al.  BCI-FES training system design and implementation for rehabilitation of stroke patients , 2008, 2008 IEEE International Joint Conference on Neural Networks (IEEE World Congress on Computational Intelligence).

[16]  Akio Kimura,et al.  Efficacy of brain-computer interface-driven neuromuscular electrical stimulation for chronic paresis after stroke. , 2014, Journal of rehabilitation medicine.

[17]  R. Rupp.  Challenges in clinical applications of brain computer interfaces in individuals with spinal cord injury , 2014, Front. Neuroeng..

[18]  D. Allan,et al.  BCI-FES hand therapy for patients with sub-acute tetraplegia , 2014 .

[19]  Aleksandra Vuckovic,et al.  Dynamic Oscillatory Signatures of Central Neuropathic Pain in Spinal Cord Injury , 2014, The journal of pain : official journal of the American Pain Society.

[20]  John Chae,et al.  Neuromuscular Electrical Stimulation for Motor Restoration in Hemiplegia. , 2015, Physical medicine and rehabilitation clinics of North America.

[21]  S. Makeig.  Auditory event-related dynamics of the EEG spectrum and effects of exposure to tones. , 1993, Electroencephalography and clinical neurophysiology.

[22]  Vivek Prabhakaran,et al.  Case report: post-stroke interventional BCI rehabilitation in an individual with preexisting sensorineural disability , 2014, Front. Neuroeng..

[23]  G. Pfurtscheller,et al.  Event-related beta EEG-changes during passive and attempted foot movements in paraplegic patients , 2007, Brain Research.

[24]  B. J. Norton,et al.  Clinical reliability of manual muscle testing. Middle trapezius and gluteus medius muscles. , 1987, Physical therapy.

[25]  Mark E. Dohring,et al.  Feasibility of a New Application of Noninvasive Brain Computer Interface (BCI): A Case Study of Training for Recovery of Volitional Motor Control After Stroke , 2009, Journal of neurologic physical therapy : JNPT.

[26]  Yi Wu,et al.  Neurophysiological substrates of stroke patients with motor imagery-based brain-computer interface training , 2014, The International journal of neuroscience.

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

[28]  P. M. Rossini,et al.  Recommendations for the clinical use of somatosensory-evoked potentials , 2008, Clinical Neurophysiology.

[29]  Shun-Hwa Wei,et al.  Investigating the Effects of Peripheral Electrical Stimulation on Corticomuscular Functional Connectivity Stroke Survivors , 2016, Topics in stroke rehabilitation.

[30]  Erkki Oja,et al.  Independent component analysis: algorithms and applications , 2000, Neural Networks.

[31]  Nicole Krämer,et al.  Time Domain Parameters as a feature for EEG-based Brain-Computer Interfaces , 2009, Neural Networks.

[32]  Aleksandra Vuckovic,et al.  Feasibility of using time-domain parameters as online therapeutic BCI features , 2014 .

[33]  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.

[34]  S. Holm.  A Simple Sequentially Rejective Multiple Test Procedure , 1979 .

[35]  D. Gater,et al.  Functional electrical stimulation therapies after spinal cord injury. , 2011, NeuroRehabilitation.

[36]  Johannes Sarnthein,et al.  High thalamocortical theta coherence in patients with neurogenic pain , 2008, NeuroImage.

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

[38]  S. C. Gandevia,et al.  Neuropathic pain and primary somatosensory cortex reorganization following spinal cord injury , 2009, PAIN®.

[39]  Milos R Popovic,et al.  Short‐Term Neuroplastic Effects of Brain‐Controlled and Muscle‐Controlled Electrical Stimulation , 2015, Neuromodulation : journal of the International Neuromodulation Society.

[40]  Taehoon Kim,et al.  Effects of Action Observational Training Plus Brain-Computer Interface-Based Functional Electrical Stimulation on Paretic Arm Motor Recovery in Patient with Stroke: A Randomized Controlled Trial. , 2016, Occupational therapy international.

[41]  W. Donovan,et al.  International Standards For Neurological Classification Of Spinal Cord Injury , 2003, The journal of spinal cord medicine.

[42]  R. Chabot,et al.  SOMATOSENSORY EVOKED POTENTIALS , 1990, International anesthesiology clinics.

[43]  A Curt,et al.  Electrophysiological recordings in patients with spinal cord injury: significance for predicting outcome , 1999, Spinal Cord.