Attentional state-synchronous peripheral electrical stimulation during action observation induced distinct modulation of corticospinal plasticity after stroke.

Introduction: Brain computer interface-based action observation (BCI-AO) is a promising technique in detecting the user's cortical state of visual attention and providing feedback to assist rehabilitation. Peripheral nerve electrical stimulation (PES) is a conventional method used to enhance outcomes in upper extremity function by increasing activation in the motor cortex. In this study, we examined the effects of different pairings of peripheral nerve electrical stimulation (PES) during BCI-AO tasks and their impact on corticospinal plasticity. Materials and methods: Our innovative BCI-AO interventions decoded user's attentive watching during task completion. This process involved providing rewarding visual cues while simultaneously activating afferent pathways through PES. Fifteen stroke patients were included in the analysis. All patients underwent a 15 min BCI-AO program under four different experimental conditions: BCI-AO without PES, BCI-AO with continuous PES, BCI-AO with triggered PES, and BCI-AO with reverse PES application. PES was applied at the ulnar nerve of the wrist at an intensity equivalent to 120% of the sensory threshold and a frequency of 50 Hz. The experiment was conducted randomly at least 3 days apart. To assess corticospinal and peripheral nerve excitability, we compared pre and post-task (post 0, post 20 min) parameters of motor evoked potential and F waves under the four conditions in the muscle of the affected hand. Results: The findings indicated that corticospinal excitability in the affected hemisphere was higher when PES was synchronously applied with AO training, using BCI during a state of attentive watching. In contrast, there was no effect on corticospinal activation when PES was applied continuously or in the reverse manner. This paradigm promoted corticospinal plasticity for up to 20 min after task completion. Importantly, the effect was more evident in patients over 65 years of age. Conclusion: The results showed that task-driven corticospinal plasticity was higher when PES was applied synchronously with a highly attentive brain state during the action observation task, compared to continuous or asynchronous application. This study provides insight into how optimized BCI technologies dependent on brain state used in conjunction with other rehabilitation training could enhance treatment-induced neural plasticity.

Effect of immersive virtual mirror visual feedback on Mu suppression and coherence in motor and parietal cortex in stroke.

We investigated the activation pattern of the motor cortex (M1) and parietal cortex during immersive virtual reality (VR)-based mirror visual feedback (MVF) of the upper limb in 14 patients with chronic stroke and severe upper limb hemiparesis and in 21 healthy controls. Participants performed wrist extension with unaffected wrists (dominant side in controls). In the MVF condition, movement of the affected hand was synchronized with that of the unaffected hand. In the no-MVF condition, only the movement of unaffected hand was shown. Mu suppression in bilateral M1 and parietal cortex and mu coherence were analyzed. In patients with stroke, MVF induced significant mu suppression in both the ipsilesional M1 and parietal lobes (p = 0.006 and p = 0.009, respectively), while mu suppression was observed in the bilateral M1 (p = 0.003 for ipsilesional and p = 0.041 for contralesional M1, respectively) and contralesional parietal lobes in the controls (p = 0.036). The ipsilesional mu coherence between the M1 and parietal cortex in patients with stroke was stronger than controls, regardless of MVF condition (p < 0.001), while mu coherence between interhemispheric M1 cortices was significantly weaker in patients with stroke (p = 0.032). Our findings provide evidence of the neural mechanism of MVF using immersive VR in patients with stroke.

Attentional State-Dependent Peripheral Electrical Stimulation During Action Observation Enhances Cortical Activations in Stroke Patients.

Brain-computer interface (BCI) is a promising technique that enables patients' interaction with computers or machines by analyzing specific brain signal patterns and provides patients with brain state-dependent feedback to assist in their rehabilitation. Action observation (AO) and peripheral electrical stimulation (PES) are conventional methods used to enhance rehabilitation outcomes by promoting neural plasticity. In this study, we assessed the effects of attentional state-dependent feedback in the combined application of BCI-AO with PES on sensorimotor cortical activation in patients after stroke. Our approach involved showing the participants a video with repetitive grasping actions under four different tasks. A mu band suppression (8-13 Hz) corresponding to each task was computed. A topographical representation showed that mu suppression of the dominant (healthy) and affected hemispheres (stroke) gradually became prominent during the tasks. There were significant differences in mu suppression in the affected motor and frontal cortices of the stroke patients. The involvement of both frontal and motor cortices became prominent in the BCI-AO+triggered PES task, in which feedback was given to the patients according to their attentive watching. Our findings suggest that synchronous stimulation according to patient attention is important for neurorehabilitation of stroke patients, which can be achieved with the combination of BCI-AO feedback with PES. BCI-AO feedback combined with PES could be effective in facilitating sensorimotor cortical activation in the affected hemispheres of stroke patients.

Brain-computer interface-based action observation combined with peripheral electrical stimulation enhances corticospinal excitability in healthy subjects and stroke patients.

Objective.Action observation (AO) combined with brain-computer interface (BCI) technology enhances cortical activation. Peripheral electrical stimulation (PES) increases corticospinal excitability, thereby activating brain plasticity. To maximize motor recovery, we assessed the effects of BCI-AO combined with PES on corticospinal plasticity.Approach.Seventeen patients with chronic hemiplegic stroke and 17 healthy subjects were recruited. The participants watched a video of repetitive grasping actions with four different tasks for 15 min: (A) AO alone; (B) AO + PES; (C) BCI-AO + continuous PES; and (D) BCI-AO + triggered PES. PES was applied at the ulnar nerve of the wrist. The tasks were performed in a random order at least three days apart. We assessed the latency and amplitude of motor evoked potentials (MEPs). We examined changes in MEP parameters pre-and post-exercise across the four tasks in the first dorsal interosseous muscle of the dominant hand (healthy subjects) and affected hand (stroke patients).Main results.The decrease in MEP latency and increase in MEP amplitude after the four tasks were significant in both groups. The increase in MEP amplitude was sustained for 20 min after tasks B, C, and D in both groups. The increase in MEP amplitude was significant between tasks A vs. B, B vs. C, and C vs. D. The estimated mean difference in MEP amplitude post-exercise was the highest for A and D in both groups.Significance.The results indicate that BCI-AO combined with PES is superior to AO alone or AO + PES for facilitating corticospinal plasticity in both healthy subjects and patients with stroke. Furthermore, this study supports the idea that synchronized activation of cortical and peripheral networks can enhance neuroplasticity after stroke. We suggest that the BCI-AO paradigm and PES could provide a novel neurorehabilitation strategy for patients with stroke.

Distraction Classification During Target Tracking Tasks Involving Target and Cursor Flickering Using EEGNet.

Keeping patients from being distracted while performing motor rehabilitation is important. An EEG-based biofeedback strategy has been introduced to help encourage participants to focus their attention on rehabilitation tasks. Here, we suggest a BCI-based monitoring method using a flickering cursor and target that can evoke a steady-state visually evoked potential (SSVEP) using the fact that the SSVEP is modulated by a patient's attention. Fifteen healthy individuals performed a tracking task where the target and cursor flickered. There were two tracking sessions, one with and one without flickering stimuli, and each session had four conditions in which each had no distractor (non-D), a visual (vis-D) or cognitive distractor (cog-D), and both distractors (both-D). An EEGNet was trained as a classifier using only non-D and both-D conditions to classify whether it was distracted and validated with a leave-one-subject-out scheme. The results reveal that the proposed classifier demonstrates superior performance when using data from the task with the flickering stimuli compared to the case without the flickering stimuli. Furthermore, the observed classification likelihood was between those corresponding to the non-D and both-D when using the trained EEGNet. This suggests that the classifier trained for the two conditions could also be used to measure the level of distraction by windowing and averaging the outcomes. Therefore, the proposed method is advantageous because it can reveal a robust and continuous level of patient distraction. This facilitates its successful application to the rehabilitation systems that use computerized technology, such as virtual reality to encourage patient engagement.

Superior Facilitation of an Action Observation Network by Congruent Character Movements in Brain-Computer Interface Action-Observation Games.

Action observation (AO) is a promising strategy for promoting motor function in neural rehabilitation. Recently, brain-computer interface (BCI)-AO game rehabilitation, which combines AO therapy with BCI technology, has been introduced to improve the effectiveness of rehabilitation. This approach can improve motor learning by providing feedback, which can be interactive in an observation task, and the game contents of the BCI-AO game paradigm can affect rehabilitation. In this study, the effects of congruent rather than incongruent feedback in a BCI-AO game on mirror neurons were investigated. Specifically, the mu suppression with congruent and incongruent BCI-AO games was measured in 17 healthy adults. The mu suppression in the central motor cortex was significantly higher with the congruent BCI-AO game than with the incongruent one. In addition, the satisfaction evaluation results were excellent for the congruent case. These results support the fact that providing feedback congruent with the motion of an action video facilitates mirror neuron activity and can offer useful guidelines for the design of BCI-AO games for rehabilitation.

Transcranial Direct Current Stimulation Effect on Virtual Hand Illusion.

Virtual reality (VR) is effectively used to evoke the mirror illusion, and transcranial direct current stimulation (tDCS) synergistically facilitates this illusion. This study investigated whether a mirror virtual hand illusion (MVHI) induced by an immersive, first-person-perspective, virtual mirror system could be modulated by tDCS of the primary motor cortex. Fourteen healthy adults (average age 21.86 years ±0.47, seven men and seven women) participated in this study, and they experienced VR with and without tDCS-the tDCS and sham conditions, each of which takes ∼30 minutes-on separate days to allow the washout of the tDCS effect. While experiencing VR, the movements of the virtual left hand reflected the flexion and extension of the real right hand. Subsequently, electroencephalogram was recorded, the magnitude of the proprioceptive shift was measured, and the participants provided responses to a questionnaire regarding hand ownership. A significant difference in the proprioceptive shift was observed between the tDCS and sham conditions. In addition, there was significant suppression of the mu power in Pz, and augmentation of the beta power in the Pz, P4, O1, and O2 channels. The difference in proprioceptive deviation between the two conditions showed significant negative correlation with mu suppression over the left frontal lobe in the tDCS condition. Finally, the question "I felt that the virtual hand was my own hand" received a significantly higher score under the tDCS condition. In short, applying tDCS over the motor cortex facilitates the MVHI by activating the attentional network over the parietal and frontal lobes such that the MVHI induces more proprioceptive drift, which suggests that the combination of VR and tDCS can enhance the immersive effect in VR. This result provides better support for the use of the MVHI paradigm in combination with tDCS for recovery from illnesses such as stroke.

Development of a flickering action video based steady state visual evoked potential triggered brain computer interface-functional electrical stimulation for a rehabilitative action observation game.

BACKGROUND: This study focused on developing an upper limb rehabilitation program. In this regard, a steady state visual evoked potential (SSVEP) triggered brain computer interface (BCI)-functional electrical stimulation (FES) based action observation game featuring a flickering action video was designed. OBJECTIVE: In particular, the synergetic effect of the game was investigated by combining the action observation paradigm with BCI based FES. METHODS: The BCI-FES system was contrasted under two conditions: with flickering action video and flickering noise video. In this regard, 11 right-handed subjects aged between 22-27 years were recruited. The differences in brain activation in response to the two conditions were examined. RESULTS: The results indicate that T3 and P3 channels exhibited greater Mu suppression in 8-13 Hz for the action video than the noise video. Furthermore, T4, C4, and P4 channels indicated augmented high beta (21-30 Hz) for the action in contrast to the noise video. Finally, T4 indicated suppressed low beta (14-20 Hz) for the action video in contrast to the noise video. CONCLUSION: The flickering action video based BCI-FES system induced a more synergetic effect on cortical activation than the flickering noise based system.

Multiple-command single-frequency SSVEP-based BCI system using flickering action video.

BACKGROUND: The number of commands in a brain-computer interface (BCI) system is important. This study proposes a new BCI technique to increase the number of commands in a single BCI system without loss of accuracy. NEW METHOD: We expected that a flickering action video with left and right elbow movements could simultaneously activate the different pattern of event-related desynchronization (ERD) according to the video contents (e.g., left or right) and steady-state visually evoked potential (SSVEP). The classification accuracy to discriminate left, right, and rest states was compared under the three following feature combinations: SSVEP power (19-21 Hz), Mu power (8-13 Hz), and simultaneous SSVEP and Mu power. RESULTS: The SSVEP feature could discriminate the stimulus condition, regardless of left or right, from the rest condition, while the Mu feature discriminated left or right, but was relatively poor in discriminating stimulus from rest. However, combining the SSVEP and Mu features, which were evoked by the stimulus with a single frequency, showed superior performance for discriminating all the stimuli among rest, left, or right. COMPARISON WITH THE EXISTING METHOD: The video contents could activate the ERD differently, and the flickering component increased its accuracy, such that it revealed a better performance to discriminate when considering together. CONCLUSIONS: This paradigm showed possibility of increasing performance in terms of accuracy and number of commands with a single frequency by applying flickering action video paradigm and applicability to rehabilitation systems used by patients to facilitate their mirror neuron systems while training.

A Brain-Computer Interface-Based Action Observation Game That Enhances Mu Suppression.

Action observation training based on the theory of activation of the mirror-neuron system has been used for the rehabilitation of patients with stroke. In this paper, we sought to assess whether a brain-computer interface (BCI)-based action observation rehabilitation game, using a flickering action video, could preferentially activate the mirror-neuron system. Feedback of stimulus observation, evoked by the flickering action video, was provided using steady state visually evoked potential and event-related desynchronization. Fifteen healthy subjects have experienced the game with BCI interaction (game and interaction), without BCI interaction (game without interaction), observed non-flickering stimuli, and flickering stimuli without the game background (stimuli only) in a counter-balanced order. The game and interface condition was resulted in significantly stronger activation of the mirror-neuron system than did the other three conditions. In addition, the amount of mirror-neuron system activation is gradually decreased in the game without interface, non-flickering stimuli, and stimuli only conditions in a time-dependent manner; however, in the game and interface condition, the amount of mirror-neuron system activation was maintained until the end of the training. Taken together, these data suggest that the proposed game paradigm, which integrates the action observation paradigm with BCI technology, could provide interactive responses for whether watching video clips can engage patients and enhance rehabilitation.

Flickering exercise video produces mirror neuron system (MNS) activation and steady state visually evoked potentials (SSVEPs).

The action of observing can be used as an effective rehabilitation paradigm, because it activates the mirror neuron system. However, it is difficult to fully use this paradigm because it is difficult to get patients to engage in watching video clips of exercise. In this study, we proposed a steady state visually evoked potential (SSVEP) based paradigm that could be used in a Brain Computer Interface, and examined its feasibility by investigating whether flickering video could activate the mirror neuron system and evoke SSVEPs at the same time. Twenty subjects were recruited and asked to watch the flickering videos at a rate of 20 Hz of upper limb motion and visual white noise, while an EEG signal was recorded. The mu rhythm (8-13 Hz) suppression and the SSVEP (19-21 Hz) evocation were analyzed from recorded EEG. The results showed that SSVEPs, evoked by the flickering stimulus, was observed in both conditions on O1 and O2, but the mu rhythm suppression on C3 and C4 was observed only in the exercise video condition. These results could signify that the flickering video is applicable for the BCI rehabilitation game, activating the mirror neuron system at the same time.

Mobile game-based virtual reality rehabilitation program for upper limb dysfunction after ischemic stroke.

BACKGROUND: Virtual reality (VR) has the potential to provide intensive, repetitive, and task-oriented training, and game-based therapy can enhance patients' motivation and enjoyment. OBJECTIVE: The objective of the present study was to develop a mobile game-based upper extremity VR program for patients who have experienced stroke, and to evaluate the feasibility and effectiveness of the program. METHODS: This randomized, double-blind, controlled trial included 24 patients with ischemic stroke. The intervention group (n = 12) received 30 min of conventional occupational therapy (OT) and 30 min of the mobile upper extremity rehabilitation program using a smartphone and a tablet PC (MoU-Rehab). The controls (n = 12) received conventional OT alone for 1 h per day. Rehabilitation consisted of 10 sessions of therapy, 5 days per week, for 2 weeks. The outcome measures (Fugl-Meyer Assessment of the upper extremity [FMA-UE], Brunnström stage [B-stage] for the arm and the hand, manual muscle testing [MMT], modified Barthel index [MBI], EuroQol-5 Dimension [EQ-5D], and Beck Depression Inventory [BDI]) were assessed at the beginning and end of treatment, and at 1 month. User satisfaction was evaluated by a questionnaire. RESULTS: A greater improvement in the FMA-UE, B-stage, and MMT was found after treatment with the MoU-Rehab than with conventional therapy. The extent of improvements in the MBI, EQ-5D, and BDI was not significantly different between the two groups. Patients in the experimental group completed the 2-weeks treatment without adverse effects, and they were generally satisfied with MoU-Rehab. CONCLUSION: This mobile game-based VR rehabilitation program appears to be feasible and effective for promoting upper limb recovery after ischemic stroke.