|
 
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| REVIEW |
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| Year : 2022 | Volume
: 1
| Issue : 2 | Page : 80-87 |
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A review on electroencephalography (EEG)-controlled upper limb exoskeletons towards stroke rehabilitation
Xin Gao, Robert Clarke, Dingguo Zhang
Centre for Autonomous Robotics (CENTAUR), University of Bath, Bath, UK
| Date of Submission | 06-Jun-2022 |
| Date of Decision | 08-Jun-2022 |
| Date of Acceptance | 15-Jun-2022 |
| Date of Web Publication | 29-Jun-2022 |
Correspondence Address:
Dingguo Zhang
Centre for Autonomous Robotics (CENTAUR), University of Bath
UK
 Source of Support: None, Conflict of Interest: None
DOI: 10.4103/2773-2398.348253
Stroke is a significant cause of disability in both developing and developed countries. This can cause a severe financial burden on families and society. With the development of robotics and brain-computer interfaces (BCIs), robotic exoskeletons and BCIs have received increasing clinical attention on stroke rehabilitation. Electroencephalography (EEG) is a method of recording brain signals non-invasively, which can be used as a BCI to control exoskeletons. This review focuses on rehabilitation systems of EEG-controlled upper limb exoskeletons, including the newest research progress and clinical evaluation in recent years. From the review, we find EEG-controlled exoskeletons can positively contribute to stroke rehabilitation. However, there are some issues that should be well investigated. More efforts are needed on EEG signal decoding algorithms such as deep learning methods in the clinical context. Practical applications must also bridge the gap between offline experiment and online control. In addition, this review also discusses the impact and significance of shared control, virtual reality/augmented reality, and other ways of human-computer interaction to improve EEG-controlled exoskeletons.
Keywords: brain-computer interface; electroencephalography; exoskeleton; stroke rehabilitation; upper limb
How to cite this article:
Gao X, Clarke R, Zhang D. A review on electroencephalography (EEG)-controlled upper limb exoskeletons towards stroke rehabilitation. Brain Netw Modulation 2022;1:80-7 |
How to cite this URL:
Gao X, Clarke R, Zhang D. A review on electroencephalography (EEG)-controlled upper limb exoskeletons towards stroke rehabilitation. Brain Netw Modulation [serial online] 2022 [cited 2023 Sep 22];1:80-7. Available from: http://www.bnmjournal.com/text.asp?2022/1/2/80/348253 |
| Introduction | |  |
Currently, the number of people whose daily lives are affected by stroke is considerable. According to incomplete statistics from the World Stroke Organization (Lindsay et al., 2019), about 185.01 in every 100,000 people per year have a stroke for the first time globally. Among people over the age of 25 years, about a quarter will have a stroke in their lifetime. When a stroke occurs, part of the brain will lose the ability to control specific functional areas of the human body. This will affect the daily life of stroke survivors, and neurological complications such as convulsions and phantom pain will occur in those affected functional areas (American Stroke Association, 2021).
According to the studies of humans and animals on learning adaptations (Gupta et al., 1993; Mattson et al., 2018; Price and Duman, 2020), the activation of experience-based neuronal plasticity enhanced functional recovery after stroke. Neuronal plasticity is generally defined as the ability of the brain to change its neuron connections and pathways in response to a given goal for humans or animals (Zimerman and Hummel, 2014). The stroke rehabilitation of the upper limb is considered a vital direction to improve patients’ quality of daily life. Functional training, graded repetitive arm supplementary program, active and weighted exercise are the most comment upper limb stroke rehabilitation therapies (Stockley et al., 2019). Although the adjuvant therapy for stroke with human intervention has proven to be effective, it has two major shortcomings. One is that the rehabilitation therapy conducted by therapists cannot fully match the patient’s exercise intention; the other is that there is a lack of qualified therapists (Mohd Nordin et al., 2014).
There are already therapies that use robotic exoskeletons as an aid. However, rehabilitation using exoskeletons solely does not allow patients to be actively engaged. The patient’s intent is not well linked to the motion of the exoskeleton, which hinders efficient motor rehabilitation. Brain-computer interfaces (BCIs) are emerging technologies that can provide a link between brain and computer systems. BCIs can recognize human motion intention through a user’s brain signals and be used to control exoskeletons. These have been shown to solve the aforementioned limitations of rehabilitation purely based on exoskeletons (Chen et al., 2013; Iqbal and Baizid, 2015; Louie and Eng, 2016). The exoskeleton will operate according to the command signals from the BCI, helping stroke patients accomplish the training exercise that matches their own intention.
BCIs can bypass the damaged pathway between the central nervous system and peripheral nerves. Electroencephalography (EEG) measures the electrical signals of the brain via electrodes placed on a person’s scalp. EEG is widely used as a non-invasive method of brain-computer interfacing. There are many paradigms for BCIs, most notably, motor imagery (MI) and steady-state visual evoked potentials (Zhu et al., 2010; Liu et al., 2014; Hong and Qin, 2021). During a paradigm, the participant performs enough trials in the same category to facilitate the training and testing of the decoding algorithms. The EEG signals are recorded in these trials. After the EEG data is collected, the EEG signals are preprocessed, and features are extracted using various methods. Following, decoding algorithms are used to classify the EEG data and recognize human motion intention.
Independently, EEG-based BCIs can be used for stroke rehabilitation (Silvoni et al., 2011; Subramanya et al., 2012; Ang and Guan, 2017; Al-Quraishi et al., 2018). However, combining BCIs with exoskeletons can further improve rehabilitation performance. This paper will review the clinical achievements and development trends of EEG-controlled exoskeletons for upper limb rehabilitation in recent years. Lower limb rehabilitation is not in the scope of this paper. Regarding the upper limb, we consider the arm and hand separately. The strategy used for this review was to search for publications with terms related to the keywords “BCI,” “upper limb,” “EEG controlled exoskeleton,” and “stroke rehabilitation” in the past 10 years. We qualitatively analyzed the advantages and disadvantages of the research and proposed the research gap. The search engines used were Google Scholar and Web of Science. Some early studies did not set a control group. The typical studies are summarized in [Table 1].
| Electroencephalography-Controlled Arm Exoskeletons | | |
Frolov et al. (2017) invited 74 stroke survivors with paralysis of upper limbs to participate in a randomized controlled trial to determine the effectiveness of EEG-controlled exoskeleton therapy in stroke rehabilitation. The trials used four classes of MI tasks to control the exoskeleton (MI states for the left hand, right hand, and relation in each). However, the study reported a relatively low average accuracy of 51.9% in the signal decoding, and the simple rehabilitation exercise parameters in the experimental design may limit the actual effectiveness of rehabilitation. This is as the exercise was for a pinch and grip movement, controlled by the exoskeleton.
Bhagat et al. (2014) recruited 160 first-time subacute and chronic upper limb hemiplegic stroke patients. After filtering, 10 participants completed the experiment. The study used a one degree-of-freedom exoskeleton robot to assist participants with EEG-controlled movements. The EEG signal processing method uses a support vector machine based on mutual information. The study used a systematic study protocol, using the Fugl-Meyer Assessment Stroke (FMA) of motor recovery after stroke (Gladstone et al., 2002) and the Action Research Arm Test (Yozbatiran et al., 2008) metrics to compare participants before and after the rehabilitation sessions. The results showed that the FMA and Action Research Arm Test scores of the participants’ upper limbs improved by an average of 3.92 ± 3.73 and 5.35 ± 4.62 respectively after rehabilitation. According to the results of kinematic measures, it was shown that the participants’ movement speed fluency was faster and more fluent on average than before. This study invited a sufficiently convincing subject population and used quantitative indicators to compare rehabilitation effects objectively. These findings demonstrate the positive effects of EEG-controlled exoskeleton devices for stroke rehabilitation. However, the one-degree of freedom exoskeleton device used in this study may have reduced the rehabilitation effect, and there is still much room for improvement in EEG signal decoding.
Ang et al. (2015) recruited 26 post-stroke hemiplegic subjects to participate in a randomized controlled trial using BCI controlled exoskeletons. They used the upper limb FMA score as an indicator of rehabilitation efficacy. The MIT-Manus shoulder and elbow robot was used in the experiment. A band-pass filter and filter bank common spatial pattern algorithm were used as EEG signal processing methods. After 4 weeks of rehabilitative training, 71.4% of the participants had significantly improved FMA scores. The BCI group performed worse than the group only using the robotic arm assistance. One reason may be the longer task execution delay in the BCI group, which reduces the fitting level between the mental task and the actual movement. On the other hand, the participants could complete fewer rehabilitation tasks in a limited amount of time compared with those with pure exoskeleton assistance. Improving algorithm decoding accuracy and real-time performance is the key to solving this defect. Additionally, this clinical study also showed fascinating information that the robot group could bring noticeable improvement in motor function to the patients in the early stage of rehabilitation exercise. Still, as the rehabilitation progressed, the performance of the BCI group became better. In the actual rehabilitation treatment, it may be possible to consider only robotic exoskeletons in the early stage and the use of BCI-exoskeletons solution in the later periods to maximize the rehabilitation effect.
Another study by Chen et al. (2020) recruited 14 subacute stroke participants for a randomized controlled trial. These participants were divided into two groups (n = 7 per group) for the BCI and control groups and underwent 4 weeks of training. The results showed that stroke rehabilitation using BCI technology could more effectively recover the patient’s exercise ability than the exoskeleton-based rehabilitation therapy without a BCI. The study also showed that the participants who made significant improvements within their chosen rehabilitation indicators also improved event-related desynchronization strength. However, from the description of the BCI part of the study, Chen et al. (2020) only applied two exercise modes for rehabilitation training, which is minimal compared to therapist conducted rehabilitation. The study employed the power spectral density method to extract data features, and a random forest machine learning model was used for classification.
Bhagat et al. (2014) proposed an EEG controlled exoskeleton rehabilitation system, recruiting three healthy individuals and one stroke patient to evaluate the system. For stroke patients, the FMA for upper-extremities was performed to assess the degree of upper limb injury. The exoskeleton used had four active degrees of freedom. Rehabilitation training was divided into three modes: passive, triggered and active which represented the participants using an autonomous exoskeleton, the EEG-based BCI exoskeleton, and the patient themselves, respectively. In terms of EEG-based exoskeleton control, a band-pass filter and surface Laplacian were used as a preprocessing method, with EEG-based spatial averages used as features and a support vector machine used as a classifier. The trial results showed that stroke patients and healthy participants had high classification accuracy in the EEG-controlled mode. However, this study failed to mention any quantitative analysis of patients in upper limb rehabilitation using indicators such as FMA.
Nann et al. (2021) proposed a stroke rehabilitation system combining both shoulder and hand exoskeletons, which were integrated with a wheelchair to allow mobile usage. The arm exoskeleton structure included four tandem elastic drive units, which could assist the patient by providing considerable torque, assisting rehabilitation movements in an extensive range. In terms of the control system, the scheme used EEG and electrooculography, and the data was preprocessed by a band-pass filter and surface Laplacian. EEG decoding used the power method (Pfurtscheller and Lopes da Silva, 1999). A total of five post-stroke patients with severe hemiplegia participated in the experiment. Results showed that more than 75% of the subtasks were completed within three seconds. The system proposed in this study has high user-friendliness and satisfaction. However, although the experiment mentioned that stroke survivors could use the system to restore activities of daily living, the experiment did not use quantitative measures to compare the participants’ motor function changes before and after the application of the system. Alongside this, the EEG decoding algorithm used in this study was proposed in 1999, and we believe more recent algorithms with better performance may enhance the system’s overall rehabilitation efficacy.
In recent years, Frolov et al. (2018) and Wu et al. (2019) reported some evidence of the mechanism for cortical plasticity induced by intervention in functional and structural neuronal reorganization. Furthermore, a study from Ramos-Murguialday et al. (2019) also reported a significant increase in FMA score after BCI robot intervention in subjects with chronic stroke. A six-month follow-up showed that patients retained their FMA score. In addition to the above research, Barsotti et al. (2015), Bhagat et al. (2016), Nann et al. (2021) and Xiao et al. (2014) have also demonstrated statistically significant outcomes in stroke patients using BCIs.
| Electroencephalography-Controlled Hand Exoskeletons | | |
In addition to the arm exoskeletons, hand exoskeletons or robotic gloves are also considered essential for assisting upper limb rehabilitation.
Araujo et al. (2021) used an EEG-based stroke rehabilitation system fused with a flexible exoskeleton glove. Made with three-dimensional printing technology, this system is lightweight, portable, and low-cost. This study used a scheme combining the common spatial pattern feature extraction algorithm and linear discriminant analysis classifier for EEG signal decoding. The exoskeleton glove solution had a complete engineering design. However, the study showed no subject-related quantitative comparisons. Nonetheless, the advantages of this superior design and low cost are worth learning.
Another study was presented by Khan et al. (2021), which used an integrated forearm and wrist exoskeleton to assist movements. For EEG decoding, the study selected the C3, Cz and C4 channels most associated with sensorimotor rhythms. The interquartile range, median absolute deviation and energy were used as signals to classify the identified features. Finally, the feature data were classified under the linear discriminant analysis classifier. Although this study proposed a complete system, further clinical trials are needed to ensure the impact of this system on various aspects of rehabilitation.
Cheng et al. (2020) proposed a BCI-controlled exoskeleton glove to aid stroke patients’ rehabilitation. The experiment was designed with six activities of daily living, with the experimental subjects divided into a “BCI intervention group” and a “no BCI group,” with five participants in each. The non-BCI group only used exoskeleton gloves in rehabilitation. Although FMA and Action Research Arm Test did not differ significantly compared to before and after the rehabilitation exercise, subjects in the BCI group all reported a sense of movement in the upper limbs. The control group did not have this reaction, which illustrates the effectiveness of BCI on rehabilitation with possible effects in the motor region. The experiment used six types of MI tasks to assist patients in rehabilitation. Compared to having only two classification tasks, a device such as this would be more suitable to have rehabilitation activities of daily living. However, the study used the FBCSP algorithm to extract features from the data and used linear discriminant analysis as the classifier. There are stronger-performing algorithms available that may be able to achieve better results.
| Discussion | | |
So far, some EEG-controlled exoskeleton systems have been clinically tested on stroke patients to demonstrate their positive implications in practical therapies. Exoskeletons are also developing to be more lightweight, friendly, and ergonomic. It is a big topic regarding design and control of exoskeletons (Gopura and Kiguchi, 2009; Gopura et al., 2016; Gull et al., 2020; Shen et al., 2020), which is not in the scope of this review. BCI-based stroke rehabilitation therapy mainly has problems that need to be paid attention to in terms of decoding algorithms, offline algorithms versus online control, shared control, and user interactions.
Decoding algorithms
In the clinical studies reviewed above, although a lot of signal processing methods are used in EEG decoding, there are almost no deep learning decoding schemes. In recent years, deep learning has been getting more attention. Some deep learning models designed for EEG decoding have been proposed. EEGNet is the most popular one that directly uses the original EEG signals as input for classification (Lawhern et al., 2018). Time-frequency features are used for an image-based deep learning model that transfers the EEG signal into the time-frequency domain and uses the feature images for classification (Xu et al., 2019; Li et al., 2020; Aslan and Akin, 2022). Long short-term memory is another popular deep learning method that is based on temporal information for decoding (Khademi et al., 2022). Similar to long short-term memory, recurrent neural networks also use temporal information for decoding, for example, these studies adopt the recurrent neural network structures to make better use of the time domain information of EEG signals (Lu et al., 2020; Tortora et al., 2020). The deep learning algorithms essentially use neuron nodes with variable weights simulated on the computer to fit the input and output data. As the number of layers of neuron nodes increases, the neural network will appear complex and have valuable characteristics for decoding. Due to the non-stationarity of the EEG signal (Pardey et al., 1996; Gonen and Tcheslavski, 2012; Ang and Guan, 2017), deep learning is considered a technique that can effectively do the entire decoding process. However, no clinical studies were found to use a deep learning decoder. The reason may be that the EEG control scenarios are very different in offline and online control; more about this topic will be discussed in the next section. Another reason may be that the EEG decoding algorithm based on deep learning has high computational time, which may delay the response (Faust et al., 2018; Rivera et al., 2022). However, decoding algorithms based on deep learning still have many advantages over traditional feature extraction schemes for clinical treatment.
Offline algorithms versus online control
Some advanced algorithms have shown high decoding accuracy for EEG signal decoding in offline data set tests recently (Hou et al., 2020; Singh Malan and Sharma, 2021; Khademi et al., 2022). However, in online scenarios, the accuracy and information transmission rate of algorithms are often lower than the results described in their paper. Part of the reason is that the algorithm may overfit the dataset. Another cause may be that the online and offline scenarios are quite different. In an online scenario, a trigger is needed to initiate decoding of the collected EEG signals with the signal decoding algorithm. Some use a continuous discriminator with a sliding window (Li et al., 2016) to achieve this effect. The advantage of this implementation is that it can distinguish between a task more often. However, the disadvantage is also apparent, which leads to a significant computational burden and misclassification of the idle state as an MI state. Another implementation method is to use electrooculography (Nakanishi et al., 2012; Jiang et al., 2014) or a physical trigger to prompt the system to enter the EEG-decoding and control state, which may present a better application effect. However, there are still a lot of engineering and theoretical problems to be faced if the BCI system is triggered to analyze the acquired signal while the ideal system would be able to automatically decode the mental state.
EEG signals
The most significant defect of the EEG signal is its low signal-noise ratio. As a non-stationary signal, it is difficult to extract the obvious and robust features that can be directly used for pattern recognition from EEG signals.
Additionally, EEG signals may exhibit significant changes over time in response to specific mental tasks. Therefore, EEG signal-based control efforts in the clinic may require periodic re-acquisition of the training data. Since the EEG signal is collected from the skin of the participant’s skull, the signal passes through the cerebral cortex, pia mater, dura mater, skull and scalp. While the electrodes receive the signal on the EEG cap, the obtained signal is already mixed with some noise. In addition to EEG, intracranial brain signals such as electrocorticography with less noise may also be considered for acquiring and identifying brain-related physiological signals, and electrocorticography-based BCI has just been applied to control exoskeletons (Benabid et al., 2019). This requires a trade-off between signal quality and participant acceptability.
Shared control
Due to the low signal-to-noise ratio of EEG signals, the performance of EEG-based BCI is limited. Robotic control technologies may compensate for this deficiency and a shared control strategy is a feasible solution. In the BCI field, shared control generally uses BCI control as the high-level controller of intent, with computer vision or autonomous control as the detailed implementation layer. Using the shared control strategy can improve task completion efficiency with the limited human intentions provided by EEG decoding algorithms. Millan et al. (2004) used BCI system controlled small cars by applying the shared control strategy. With the assistance of shared control, the efficiency of the car to complete the task has been improved. This idea has now been extended further in rehabilitation research on robotic arms/exoskeletons controlled by BCI (Xu et al., 2019b; Quere et al., 2020; Cao et al., 2021).
In the simultaneous sharing control mode, humans and robots can complete tasks synchronously and collaboratively, which can effectively increase the success rate of tasks while ensuring the user’s sense of participation and also significantly improve patients’ confidence in rehabilitation (Philips et al., 2007; Mane et al., 2020). Sharing strategy is the core issue in shared control and the most critical case to be considered in current related research. For example, the control system needs to judge when to use the machine vision automation system, when to use the BCI control, determine the trigger signal between the BCI control and the autonomous control, etc. The optimization of these problems will bring a better rehabilitation experience and rehabilitation effects to patients.
Virtual reality/augmented reality-based user interaction
It is important to enhance the user’s participation and make EEG-controlled exoskeleton systems interesting. The use of interaction systems such as virtual reality, augmented reality and video games in stroke rehabilitation has been studied in recent years (Alimanova et al., 2017; Zheng et al., 2018; Bouteraa et al., 2019). These human-computer interactions can increase patient engagement, immersion, and motivation (Mubin et al., 2019). Gauthier et al. (2018) and Petrie (2018) investigated how to use gamification to increase repetition, engagement, and care coverage in the context of rehabilitation.
In addition to improving a patient’s focus on rehabilitation, games also positively reduce patient stress (Jannink et al., 2008). According to the study by Pittenger and Duman (2008), neuroplasticity may be disrupted in animal models of emotional disorders and stress, and games can significantly relieve patient stress. This effect is positive for recovery. For more information on the impact of virtual reality, augmented reality, and video games on stroke rehabilitation, please refer to these review papers (Saleh et al., 2017; Mubin et al., 2019; Huygelier et al., 2021). We think it is a promising direction to introduce augmented reality/virtual reality technologies into EEG-controlled exoskeleton rehabilitation training.
| Conclusions | | |
This paper reviewed the progress of EEG-controlled upper limb exoskeletons in stroke rehabilitation over recent years. The typical studies are introduced and summarized. The current challenges are analyzed, and the future directions are discussed. We believe EEG-controlled exoskeletons are a cutting-edge technology with great potential to shine in the field of stroke rehabilitation in the future. However, this requires close collaboration and continuous effort from researchers, developers, and therapists in related fields.
Author contributions
XG drafted the paper. RC and DZ reviewed and revised the paper. DZ conceived of this study. All authors approved the final version for publication.
Conflicts of interest
There are no conflicts of interest.
Editor note: DZ is an Editorial Board member of Brain Network and Modulation. He was blinded from reviewing or making decisions on the manuscript. The article was subject to the journal’s standard procedures, with peer review handled independently of this Editorial Board member and his research group.
Open access statement
This is an open access journal, and articles are distributed under the terms of the Creative Commons AttributionNonCommercial-ShareAlike 4.0 License, which allows others to remix, tweak, and build upon the work non-commercially, as long as appropriate credit is given and the new creations are licensed under the identical terms.
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[Table 1]
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