Abstract
Brain-machine interface-controlled (BMI) neurofeedback training aims to modulate cortical physiology and is applied during neurorehabilitation to increase the responsiveness of the brain to subsequent physiotherapy. In a parallel line of research, robotic exoskeletons are used in goal-oriented rehabilitation exercises for patients with severe motor impairment to extend their range of motion (ROM) and the intensity of training. Furthermore, neuromuscular electrical stimulation (NMES) is applied in neurologically impaired patients to restore muscle strength by closing the sensorimotor loop. In this proof-of-principle study, we explored an integrated approach for providing assistance as needed to amplify the task-related ROM and the movement-related brain modulation during rehabilitation exercises of severely impaired patients. For this purpose, we combined these three approaches (BMI, NMES, and exoskeleton) in an integrated neuroprosthesis and studied the feasibility of this device in seven severely affected chronic stroke patients who performed wrist flexion and extension exercises while receiving feedback via a virtual environment. They were assisted by a gravity-compensating, seven degree-of-freedom exoskeleton which was attached to the paretic arm. NMES was applied to the wrist extensor and flexor muscles during the exercises and was controlled by a hybrid BMI based on both sensorimotor cortical desynchronization (ERD) and electromyography (EMG) activity. The stimulation intensity was individualized for each targeted muscle and remained subthreshold, i.e., induced no overt support. The hybrid BMI controlled the stimulation significantly better than the offline analyzed ERD (p = 0.028) or EMG (p = 0.021) modality alone. Neuromuscular stimulation could be well integrated into the exoskeleton-based training and amplified both the task-related ROM (p = 0.009) and the movement-related brain modulation (p = 0.019). Combining a hybrid BMI with neuromuscular stimulation and antigravity assistance augments upper limb function and brain activity during rehabilitation exercises and may thus provide a novel restorative framework for severely affected stroke patients.
Highlights
Standard of care leaves the majority of stroke survivors with a dysfunctional upper extremity and, with a long-term dependency on others for activities of daily living (Jørgensen et al, 1999; Dobkin, 2005; Feigin et al, 2008)
Subthreshold neuromuscular electrical stimulation (NMES) could be well integrated into the exoskeleton-based training; the effects on range of motion (ROM) and event-related desynchronization (ERD) were bigger when using Brain-machine interface-controlled (BMI)+NMES than the exoskeleton alone
By achieving a mean classification accuracy of 66 ± 9.6% compared to 55 ± 6.4% and 55 ± 4.6%, the hybrid BMI controlled the stimulation significantly better than either the EEG (p = 0.028) or the EMG (p = 0.021) modality
Summary
Standard of care leaves the majority of stroke survivors with a dysfunctional upper extremity and, with a long-term dependency on others for activities of daily living (Jørgensen et al, 1999; Dobkin, 2005; Feigin et al, 2008). Attempts to improve recovery in this patient group are numerous and embrace advanced rehabilitation technology for motor relearning such as brain-interface based neurofeedback training (Ang et al, 2015; Morone et al, 2015; Pichiorri et al, 2015), robot-assisted rehabilitation devices (Lo et al, 2010; KlamrothMarganska et al, 2014) and activity-dependent neuromuscular stimulation techniques (Thrasher et al, 2008; Oujamaa et al, 2009; Mann et al, 2011) Recent approaches combine these different methods in a bid to maximize the overall benefits (Meadmore et al, 2014; Brauchle et al, 2015; Hortal et al, 2015; Grimm and Gharabaghi, 2016). There is still a critical need in the rehabilitation community to provide options for stroke patients with chronic impairments In this context, movement-related desynchronization (ERD) in the contralateral sensorimotor cortex has been shown to be compromised in stroke patients compared to healthy controls; notably, the more severe the patient’s motor impairment, the less beta-band ERD (Rossiter et al, 2014). Increasing this oscillatory modulation range again would provide a therapeutic target for a restorative training approach
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