Long-term Training With a Brain-Machine Interface-Based Gait Protocol Induces Partial Neurological Recovery in Paraplegic Patients

摘要

Spinal cord injury (SCI) rehabilitation remains a major clinical challenge, especially in cases involving chronic, complete injury. Existing interventions for assisting patients with SCI in walking, including body weight support systems, robotic assistance, and functional electrostimulation of the legs, have not shown evidence of generating significant clinical improvement in somatosensory function below the level of the injury. In the past 2 decades, brain-machine interfaces (BMIs) have become popular tools for restoring limb function in paralyzed patients, although no study has suggested that long-term training with BMI-based paradigms and physical training could trigger neurological recovery, particularly in patients with complete SCI.1 However, the prospect of neurological recovery is supported by postmortem anatomical studies that have shown that 60% to 80% of patients with “complete” SCI show viable axons crossing the level of the SCI. In this study, Donati et al2 show partial neurological and clinical improvement in patients with SCI subjected to long-term training with a multistage BMI-based gait protocol called the Walk Again Neurorehabilitation protocol (WA-NR). Donati et al implemented WA-NR in 8 patients with chronic (> 1 year) paraplegic SCI. Seven patients had complete SCI (American Spinal Injury Association Impairment Scale A), and 1 patient had partial SCI (American Spinal Injury Association Impairment Scale B). The 6-component protocol of WA-NR (Figure, A) started with seated virtual reality and progressed to gait training with a brain-controlled exoskeleton.Figure: A, the Walk Again Neurorehabilitation protocol (WA-NR): (1) Seated patient uses his/her brain activity, recorded via EEG, to control the movements of a human body avatar in an immersive virtual reality (VR) environment while receiving visuo-tactile feedback; (2) the same as phase 1 but the patient is upright, supported by a stand-in-table device; (3) training on a robotic body weight support (BWS) gait system on a treadmill; (4) training with a BWS gait system fixed on an over-ground track; (5) training with a brain-controlled robotic BWS gait system on a treadmill; and (6) gait training with a brain-controlled, sensorized robotic exoskeleton. B, functional assessment of autonomy in walking given by the Walking Index for Spinal Cord Injury (WISCI) scale. All patients improved in functional walking ability after 12 months of WA-NR. BMI, brain-machine interface; EEG, electroencephalography; EMG, electromyography. Adapted from Donati ARC, Shokur S, Morya E, et al. Long-term training with a brain-machine interface-based gait protocol induces partial neurological recovery in paraplegic patients. Sci Rep. 2016;6:30383 used under CC BY 4.0.Although the original goal of the study was to explore how much such a long-term BMI-based protocol could help patients with SCI regain their ability to walk autonomously using the brain-controlled exoskeleton, the scientists realized after the first 12 months of training that all patients experienced a significant clinical improvement in their ability to perceive somatic sensations and to exert voluntary motor control below the original SCI. Sensory recovery was more vigorous and consistent for nociceptive perception (>5 dermatomes on average) than for tactile, vibration, or proprioception (1-2 dermatomes) and temperature (no significant improvement). Improvements were clinically significant after 7 months, peaking at the 10th month of training. Figure, B summarizes improvements in walking ability as measured by the Walking Index Spinal Cord Injury. The authors propose that even in SCI up to 27% of the total area of spinal cord white matter may be preserved. Direct brain control of virtual or robotic legs and a continuous stream of tactile stimulation feedback from the legs and robotic actuators may induce plasticity through activation of central pattern generators and cortical afferents in patients with SCI. The full