Brain-Machine Neurofeedback: Robotics or Electrical Stimulation?

Robert Guggenberger,Monika Heringhaus,Alireza Gharabaghi

doi:10.3389/fbioe.2020.00639

Robert Guggenberger, Monika Heringhaus + Show 1 more

Open Access

https://doi.org/10.3389/fbioe.2020.00639

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Abstract

Neurotechnology such as brain-machine interfaces (BMI) are currently being investigated as training devices for neurorehabilitation, when active movements are no longer possible. When the hand is paralyzed following a stroke for example, a robotic orthosis, functional electrical stimulation (FES) or their combination may provide movement assistance; i.e., the corresponding sensory and proprioceptive neurofeedback is given contingent to the movement intention or imagination, thereby closing the sensorimotor loop. Controlling these devices may be challenging or even frustrating. Direct comparisons between these two feedback modalities (robotics vs. FES) with regard to the workload they pose for the user are, however, missing. Twenty healthy subjects controlled a BMI by kinesthetic motor imagery of finger extension. Motor imagery-related sensorimotor desynchronization in the EEG beta frequency-band (17–21 Hz) was turned into passive opening of the contralateral hand by a robotic orthosis or FES in a randomized, cross-over block design. Mental demand, physical demand, temporal demand, performance, effort, and frustration level were captured with the NASA Task Load Index (NASA-TLX) questionnaire by comparing these workload components to each other (weights), evaluating them individually (ratings), and estimating the respective combinations (adjusted workload ratings). The findings were compared to the task-related aspects of active hand movement with EMG feedback. Furthermore, both feedback modalities were compared with regard to their BMI performance. Robotic and FES feedback had similar workloads when weighting and rating the different components. For both robotics and FES, mental demand was the most relevant component, and higher than during active movement with EMG feedback. The FES task led to significantly more physical (p = 0.0368) and less temporal demand (p = 0.0403) than the robotic task in the adjusted workload ratings. Notably, the FES task showed a physical demand 2.67 times closer to the EMG task, but a mental demand 6.79 times closer to the robotic task. On average, significantly more onsets were reached during the robotic as compared to the FES task (17.22 onsets, SD = 3.02 vs. 16.46, SD = 2.94 out of 20 opportunities; p = 0.016), even though there were no significant differences between the BMI classification accuracies of the conditions (p = 0.806; CI = −0.027 to −0.034). These findings may inform the design of neurorehabilitation interfaces toward human-centered hardware for a more natural bidirectional interaction and acceptance by the user.

Highlights

About half of all severely affected stroke survivors remain with persistent motor deficits in the chronic disease stage despite therapeutic interventions on the basis of the current standard of care (Winters et al, 2015)
Since these patients cannot use the affected hand for activities of daily living, novel interventions investigate different neurotechnological devices to facilitate upper limb motor rehabilitation, such as brain-machine interfaces (BMI), robotic orthoses, neuromuscular functional electrical stimulation (FES), and brain stimulation (Coscia et al, 2019)
Recent research has taken a refined and rather mechanistic approach, e.g., by targeting physiologically grounded and clinically relevant biomarkers with BMI neurofeedback; this has led to the conceptional differentiation between restorative therapeutic BMIs on the one side and classical assistive BMIs on the other side like those applied to control devices such as wheel-chairs (Gharabaghi, 2016): While assistive BMIs intend to maximize the decoding accuracy, restorative BMIs want to enhance behaviorally relevant biomarkers

Summary

Introduction

About half of all severely affected stroke survivors remain with persistent motor deficits in the chronic disease stage despite therapeutic interventions on the basis of the current standard of care (Winters et al, 2015) Since these patients cannot use the affected hand for activities of daily living, novel interventions investigate different neurotechnological devices to facilitate upper limb motor rehabilitation, such as brain-machine interfaces (BMI), robotic orthoses, neuromuscular functional electrical stimulation (FES), and brain stimulation (Coscia et al, 2019). It is hypothesized that this approach will lead to reorganization of the corticospinal network through repetitive practice, and might restore the lost motor function (Naros and Gharabaghi, 2015, 2017; Belardinelli et al, 2017; Guggenberger et al, 2018) These novel approaches often result in no relevant clinical improvements in severe chronic stroke patients yet (Coscia et al, 2019). Brain oscillations in the beta frequency band have been suggested as potential candidate markers and therapeutic targets for technology-assisted stroke rehabilitation with restorative BMIs (Naros and Gharabaghi, 2015, 2017; Belardinelli et al, 2017), since they are known to enhance signal propagation in the motor system and to determine the input-output ratio of corticospinal excitability in a frequency- and phase-specific way (Raco et al, 2016; Khademi et al, 2018, 2019; Naros et al, 2019)

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