Abstract

Brain-machine interfaces (BMIs) provide a new assistive strategy aimed at restoring mobility in severely paralyzed patients. Yet, no study in animals or in human subjects has indicated that long-term BMI training could induce any type of clinical recovery. Eight chronic (3–13 years) spinal cord injury (SCI) paraplegics were subjected to long-term training (12 months) with a multi-stage BMI-based gait neurorehabilitation paradigm aimed at restoring locomotion. This paradigm combined intense immersive virtual reality training, enriched visual-tactile feedback, and walking with two EEG-controlled robotic actuators, including a custom-designed lower limb exoskeleton capable of delivering tactile feedback to subjects. Following 12 months of training with this paradigm, all eight patients experienced neurological improvements in somatic sensation (pain localization, fine/crude touch, and proprioceptive sensing) in multiple dermatomes. Patients also regained voluntary motor control in key muscles below the SCI level, as measured by EMGs, resulting in marked improvement in their walking index. As a result, 50% of these patients were upgraded to an incomplete paraplegia classification. Neurological recovery was paralleled by the reemergence of lower limb motor imagery at cortical level. We hypothesize that this unprecedented neurological recovery results from both cortical and spinal cord plasticity triggered by long-term BMI usage.

Highlights

  • Since the first experimental demonstrations in rats[9], monkeys[10,11], and the subsequent clinical reports in humans[12,13,14], brain-machine interfaces (BMIs) have emerged as potential options to restore mobility in patients who are severely paralyzed as a result of spinal cord injuries (SCIs) or neurodegenerative disorders[15]

  • EEG analysis revealed clear signs of cortical functional plasticity, at the level of the primary somatosensory and motor cortical areas, during the same period. These findings suggest, for the first time, that long-term exposure to BMI-based protocols enriched with tactile feedback and combined with robotic gait training may induce cortical and subcortical plasticity capable of triggering partial neurological recovery even in patients originally diagnosed with a chronic complete spinal cord injury

  • We measured the extent of the Zone of Partial Preservation (ZPP), i.e. the dermatomes and myotomes caudal to the neurological level of injury that remain partially innervated[23]

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Summary

Introduction

Since the first experimental demonstrations in rats[9], monkeys[10,11], and the subsequent clinical reports in humans[12,13,14], brain-machine interfaces (BMIs) have emerged as potential options to restore mobility in patients who are severely paralyzed as a result of spinal cord injuries (SCIs) or neurodegenerative disorders[15]. Our central goal was to explore how much such a long-term BMI-based protocol could help SCI patients regain their ability to walk autonomously using our brain-controlled exoskeleton Among other innovations, this device provides tactile feedback to subjects through the combination of multiple force-sensors, applied to key locations of the exoskeleton, such as the plantar surface of the feet, and a multi-channel haptic display, applied to the patient’s forearm skin surface. EEG analysis revealed clear signs of cortical functional plasticity, at the level of the primary somatosensory and motor cortical areas, during the same period These findings suggest, for the first time, that long-term exposure to BMI-based protocols enriched with tactile feedback and combined with robotic gait training may induce cortical and subcortical plasticity capable of triggering partial neurological recovery even in patients originally diagnosed with a chronic complete spinal cord injury

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