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1.  EEG Control of a Virtual Helicopter in 3-Dimensional Space Using Intelligent Control Strategies 
Films like Firefox, Surrogates, and Avatar have explored the possibilities of using brain-computer interfaces (BCIs) to control machines and replacement bodies with only thought. Real world BCIs have made great progress toward that end. Invasive BCIs have enabled monkeys to fully explore 3-dimensional (3D) space using neuroprosthetics. However, non-invasive BCIs have not been able to demonstrate such mastery of 3D space. Here, we report our work, which demonstrates that human subjects can use a non-invasive BCI to fly a virtual helicopter to any point in a 3D world. Through use of intelligent control strategies, we have facilitated the realization of controlled flight in 3D space. We accomplished this through a reductionist approach that assigns subject-specific control signals to the crucial components of 3D flight. Subject control of the helicopter was comparable when using either the BCI or a keyboard. By using intelligent control strategies, the strengths of both the user and the BCI system were leveraged and accentuated. Intelligent control strategies in BCI systems such as those presented here may prove to be the foundation for complex BCIs capable of doing more than we ever imagined.
PMCID: PMC3037732  PMID: 20876032
BCI; Brain-Computer Interface; EEG; 3D
2.  Visuo-motor coordination ability predicts performance with brain-computer interfaces controlled by modulation of sensorimotor rhythms (SMR) 
Modulation of sensorimotor rhythms (SMR) was suggested as a control signal for brain-computer interfaces (BCI). Yet, there is a population of users estimated between 10 to 50% not able to achieve reliable control and only about 20% of users achieve high (80–100%) performance. Predicting performance prior to BCI use would facilitate selection of the most feasible system for an individual, thus constitute a practical benefit for the user, and increase our knowledge about the correlates of BCI control. In a recent study, we predicted SMR-BCI performance from psychological variables that were assessed prior to the BCI sessions and BCI control was supported with machine-learning techniques. We described two significant psychological predictors, namely the visuo-motor coordination ability and the ability to concentrate on the task. The purpose of the current study was to replicate these results thereby validating these predictors within a neurofeedback based SMR-BCI that involved no machine learning.Thirty-three healthy BCI novices participated in a calibration session and three further neurofeedback training sessions. Two variables were related with mean SMR-BCI performance: (1) a measure for the accuracy of fine motor skills, i.e., a trade for a person’s visuo-motor control ability; and (2) subject’s “attentional impulsivity”. In a linear regression they accounted for almost 20% in variance of SMR-BCI performance, but predictor (1) failed significance. Nevertheless, on the basis of our prior regression model for sensorimotor control ability we could predict current SMR-BCI performance with an average prediction error of M = 12.07%. In more than 50% of the participants, the prediction error was smaller than 10%. Hence, psychological variables played a moderate role in predicting SMR-BCI performance in a neurofeedback approach that involved no machine learning. Future studies are needed to further consolidate (or reject) the present predictors.
PMCID: PMC4123785  PMID: 25147518
brain-computer interfaces; sensorimotor rhythms; predictors; visuo-motor coordination abilities; attentional impulsivity
3.  Proprioceptive Feedback and Brain Computer Interface (BCI) Based Neuroprostheses 
PLoS ONE  2012;7(10):e47048.
Brain computer interface (BCI) technology has been proposed for motor neurorehabilitation, motor replacement and assistive technologies. It is an open question whether proprioceptive feedback affects the regulation of brain oscillations and therefore BCI control. We developed a BCI coupled on-line with a robotic hand exoskeleton for flexing and extending the fingers. 24 healthy participants performed five different tasks of closing and opening the hand: (1) motor imagery of the hand movement without any overt movement and without feedback, (2) motor imagery with movement as online feedback (participants see and feel their hand, with the exoskeleton moving according to their brain signals, (3) passive (the orthosis passively opens and closes the hand without imagery) and (4) active (overt) movement of the hand and rest. Performance was defined as the difference in power of the sensorimotor rhythm during motor task and rest and calculated offline for different tasks. Participants were divided in three groups depending on the feedback receiving during task 2 (the other tasks were the same for all participants). Group 1 (n = 9) received contingent positive feedback (participants' sensorimotor rhythm (SMR) desynchronization was directly linked to hand orthosis movements), group 2 (n = 8) contingent “negative” feedback (participants' sensorimotor rhythm synchronization was directly linked to hand orthosis movements) and group 3 (n = 7) sham feedback (no link between brain oscillations and orthosis movements). We observed that proprioceptive feedback (feeling and seeing hand movements) improved BCI performance significantly. Furthermore, in the contingent positive group only a significant motor learning effect was observed enhancing SMR desynchronization during motor imagery without feedback in time. Furthermore, we observed a significantly stronger SMR desynchronization in the contingent positive group compared to the other groups during active and passive movements. To summarize, we demonstrated that the use of contingent positive proprioceptive feedback BCI enhanced SMR desynchronization during motor tasks.
PMCID: PMC3465309  PMID: 23071707
4.  EEG-Based BCI System Using Adaptive Features Extraction and Classification Procedures 
Motor imagery is a common control strategy in EEG-based brain-computer interfaces (BCIs). However, voluntary control of sensorimotor (SMR) rhythms by imagining a movement can be skilful and unintuitive and usually requires a varying amount of user training. To boost the training process, a whole class of BCI systems have been proposed, providing feedback as early as possible while continuously adapting the underlying classifier model. The present work describes a cue-paced, EEG-based BCI system using motor imagery that falls within the category of the previously mentioned ones. Specifically, our adaptive strategy includes a simple scheme based on a common spatial pattern (CSP) method and support vector machine (SVM) classification. The system's efficacy was proved by online testing on 10 healthy participants. In addition, we suggest some features we implemented to improve a system's “flexibility” and “customizability,” namely, (i) a flexible training session, (ii) an unbalancing in the training conditions, and (iii) the use of adaptive thresholds when giving feedback.
PMCID: PMC5011245  PMID: 27635129
5.  Large-Scale Assessment of a Fully Automatic Co-Adaptive Motor Imagery-Based Brain Computer Interface 
PLoS ONE  2016;11(2):e0148886.
In the last years Brain Computer Interface (BCI) technology has benefited from the development of sophisticated machine leaning methods that let the user operate the BCI after a few trials of calibration. One remarkable example is the recent development of co-adaptive techniques that proved to extend the use of BCIs also to people not able to achieve successful control with the standard BCI procedure. Especially for BCIs based on the modulation of the Sensorimotor Rhythm (SMR) these improvements are essential, since a not negligible percentage of users is unable to operate SMR-BCIs efficiently. In this study we evaluated for the first time a fully automatic co-adaptive BCI system on a large scale. A pool of 168 participants naive to BCIs operated the co-adaptive SMR-BCI in one single session. Different psychological interventions were performed prior the BCI session in order to investigate how motor coordination training and relaxation could influence BCI performance. A neurophysiological indicator based on the Power Spectral Density (PSD) was extracted by the recording of few minutes of resting state brain activity and tested as predictor of BCI performances. Results show that high accuracies in operating the BCI could be reached by the majority of the participants before the end of the session. BCI performances could be significantly predicted by the neurophysiological indicator, consolidating the validity of the model previously developed. Anyway, we still found about 22% of users with performance significantly lower than the threshold of efficient BCI control at the end of the session. Being the inter-subject variability still the major problem of BCI technology, we pointed out crucial issues for those who did not achieve sufficient control. Finally, we propose valid developments to move a step forward to the applicability of the promising co-adaptive methods.
PMCID: PMC4758702  PMID: 26891350
6.  Towards a User-Friendly Brain-Computer Interface: Initial Tests in ALS and PLS Patients 
Patients usually require long-term training for effective EEG-based brain-computer interface (BCI) control due to fatigue caused by the demands for focused attention during prolonged BCI operation. We intended to develop a user-friendly BCI requiring minimal training and less mental load.
Testing of BCI performance was investigated in three patients with amyotrophic lateral sclerosis (ALS) and three patients with primary lateral sclerosis (PLS), who had no previous BCI experience. All patients performed binary control of cursor movement. One ALS patient and one PLS patient performed four-directional cursor control in a two-dimensional domain under a BCI paradigm associated with human natural motor behavior using motor execution and motor imagery. Subjects practiced for 5-10 minutes and then participated in a multi-session study of either binary control or four-directional control including online BCI game over 1.5 – 2 hours in a single visit.
Event-related desynchronization and event-related synchronization in the beta band were observed in all patients during the production of voluntary movement either by motor execution or motor imagery. The online binary control of cursor movement was achieved with an average accuracy about 82.1±8.2% with motor execution and about 80% with motor imagery, whereas offline accuracy was achieved with 91.4±3.4% with motor execution and 83.3±8.9% with motor imagery after optimization. In addition, four-directional cursor control was achieved with an accuracy of 50-60% with motor execution and motor imagery.
Patients with ALS or PLS may achieve BCI control without extended training, and fatigue might be reduced during operation of a BCI associated with human natural motor behavior.
The development of a user-friendly BCI will promote practical BCI applications in paralyzed patients.
PMCID: PMC2895010  PMID: 20347612
EEG; brain-computer interface (BCI); event-related desynchronization (ERD); event-related synchronization (ERS); user-friendly; amyotrophic lateral sclerosis (ALS); primary lateral sclerosis (PLS); motor control
7.  Quadcopter control in three-dimensional space using a noninvasive motor imagery based brain-computer interface 
Journal of neural engineering  2013;10(4):10.1088/1741-2560/10/4/046003.
At the balanced intersection of human and machine adaptation is found the optimally functioning brain-computer interface (BCI). In this study, we report a novel experiment of BCI controlling a robotic quadcopter in three-dimensional physical space using noninvasive scalp EEG in human subjects. We then quantify the performance of this system using metrics suitable for asynchronous BCI. Lastly, we examine the impact that operation of a real world device has on subjects’ control with comparison to a two-dimensional virtual cursor task.
Five human subjects were trained to modulate their sensorimotor rhythms to control an AR Drone navigating a three-dimensional physical space. Visual feedback was provided via a forward facing camera on the hull of the drone. Individual subjects were able to accurately acquire up to 90.5% of all valid targets presented while travelling at an average straight-line speed of 0.69 m/s.
Freely exploring and interacting with the world around us is a crucial element of autonomy that is lost in the context of neurodegenerative disease. Brain-computer interfaces are systems that aim to restore or enhance a user’s ability to interact with the environment via a computer and through the use of only thought. We demonstrate for the first time the ability to control a flying robot in the three-dimensional physical space using noninvasive scalp recorded EEG in humans. Our work indicates the potential of noninvasive EEG based BCI systems to accomplish complex control in three-dimensional physical space. The present study may serve as a framework for the investigation of multidimensional non-invasive brain-computer interface control in a physical environment using telepresence robotics.
PMCID: PMC3839680  PMID: 23735712
Brain-Computer Interface; BCI; EEG; 3D control; motor imagery; telepresence robotics
Journal of neural engineering  2012;10(1):016002.
Sensorimotor rhythms (SMRs) are 8–30 Hz oscillations in the EEG recorded from the scalp over sensorimotor cortex that change with movement and/or movement imagery. Many brain-computer interface (BCI) studies have shown that people can learn to control SMR amplitudes and can use that control to move cursors and other objects in one, two, or three dimensions. At the same time, if SMR-based BCIs are to be useful for people with neuromuscular disabilities, their accuracy and reliability must be improved substantially. These BCIs often use spatial filtering methods such as common average reference (CAR), Laplacian (LAP) filter or common spatial pattern (CSP) filter to enhance the signal-to-ratio of EEG. Here we test the hypothesis that a new filter design, called an “adaptive Laplacian (ALAP) filter,” can provide better performance for SMR-based BCIs.
An ALAP filter employs a Gaussian kernel to construct a smooth spatial gradient of channel weights, and then simultaneously seeks the optimal kernel radius of this spatial filter and the regularization parameter of linear ridge regression. This optimization is based on minimizing leave-one-out cross-validation error through a gradient descent method, and is computationally feasible.
Main results
Using a variety of kinds of BCI data from a total of 22 individuals, we compare the performances of ALAP filter to CAR, small LAP, large LAP and CSP filter. With a large number of channels and limited data, ALAP performs significantly better than CSP, CAR, small LAP and large LAP both in classification accuracy as well as in mean squared error. Using fewer channels restricted to motor areas, ALAP is still superior to CAR, small LAP and large LAP, but equally matched to CSP.
Thus, ALAP may help to improve the accuracy and robustness of SMR-based BCIs.
PMCID: PMC3602341  PMID: 23220879
Brain computer interface (BCI); brain-machine interface (BMI); spatial filter; electroencephalogram (EEG); leave-one-out (LOO) cross-validation; assistive communication
9.  A brain-computer interface with vibrotactile biofeedback for haptic information 
It has been suggested that Brain-Computer Interfaces (BCI) may one day be suitable for controlling a neuroprosthesis. For closed-loop operation of BCI, a tactile feedback channel that is compatible with neuroprosthetic applications is desired. Operation of an EEG-based BCI using only vibrotactile feedback, a commonly used method to convey haptic senses of contact and pressure, is demonstrated with a high level of accuracy.
A Mu-rhythm based BCI using a motor imagery paradigm was used to control the position of a virtual cursor. The cursor position was shown visually as well as transmitted haptically by modulating the intensity of a vibrotactile stimulus to the upper limb. A total of six subjects operated the BCI in a two-stage targeting task, receiving only vibrotactile biofeedback of performance. The location of the vibration was also systematically varied between the left and right arms to investigate location-dependent effects on performance.
Results and Conclusion
Subjects are able to control the BCI using only vibrotactile feedback with an average accuracy of 56% and as high as 72%. These accuracies are significantly higher than the 15% predicted by random chance if the subject had no voluntary control of their Mu-rhythm. The results of this study demonstrate that vibrotactile feedback is an effective biofeedback modality to operate a BCI using motor imagery. In addition, the study shows that placement of the vibrotactile stimulation on the biceps ipsilateral or contralateral to the motor imagery introduces a significant bias in the BCI accuracy. This bias is consistent with a drop in performance generated by stimulation of the contralateral limb. Users demonstrated the capability to overcome this bias with training.
PMCID: PMC2104531  PMID: 17941986
10.  Change in brain activity through virtual reality-based brain-machine communication in a chronic tetraplegic subject with muscular dystrophy 
BMC Neuroscience  2010;11:117.
For severely paralyzed people, a brain-computer interface (BCI) provides a way of re-establishing communication. Although subjects with muscular dystrophy (MD) appear to be potential BCI users, the actual long-term effects of BCI use on brain activities in MD subjects have yet to be clarified. To investigate these effects, we followed BCI use by a chronic tetraplegic subject with MD over 5 months. The topographic changes in an electroencephalogram (EEG) after long-term use of the virtual reality (VR)-based BCI were also assessed. Our originally developed BCI system was used to classify an EEG recorded over the sensorimotor cortex in real time and estimate the user's motor intention (MI) in 3 different limb movements: feet, left hand, and right hand. An avatar in the internet-based VR was controlled in accordance with the results of the EEG classification by the BCI. The subject was trained to control his avatar via the BCI by strolling in the VR for 1 hour a day and then continued the same training twice a month at his home.
After the training, the error rate of the EEG classification decreased from 40% to 28%. The subject successfully walked around in the VR using only his MI and chatted with other users through a voice-chat function embedded in the internet-based VR. With this improvement in BCI control, event-related desynchronization (ERD) following MI was significantly enhanced (p < 0.01) for feet MI (from -29% to -55%), left-hand MI (from -23% to -42%), and right-hand MI (from -22% to -51%).
These results show that our subject with severe MD was able to learn to control his EEG signal and communicate with other users through use of VR navigation and suggest that an internet-based VR has the potential to provide paralyzed people with the opportunity for easy communication.
PMCID: PMC2949766  PMID: 20846418
11.  Motor priming in virtual reality can augment motor-imagery training efficacy in restorative brain-computer interaction: a within-subject analysis 
The use of Brain–Computer Interface (BCI) technology in neurorehabilitation provides new strategies to overcome stroke-related motor limitations. Recent studies demonstrated the brain's capacity for functional and structural plasticity through BCI. However, it is not fully clear how we can take full advantage of the neurobiological mechanisms underlying recovery and how to maximize restoration through BCI. In this study we investigate the role of multimodal virtual reality (VR) simulations and motor priming (MP) in an upper limb motor-imagery BCI task in order to maximize the engagement of sensory-motor networks in a broad range of patients who can benefit from virtual rehabilitation training.
In order to investigate how different BCI paradigms impact brain activation, we designed 3 experimental conditions in a within-subject design, including an immersive Multimodal Virtual Reality with Motor Priming (VRMP) condition where users had to perform motor-execution before BCI training, an immersive Multimodal VR condition, and a control condition with standard 2D feedback. Further, these were also compared to overt motor-execution. Finally, a set of questionnaires were used to gather subjective data on Workload, Kinesthetic Imagery and Presence.
Our findings show increased capacity to modulate and enhance brain activity patterns in all extracted EEG rhythms matching more closely those present during motor-execution and also a strong relationship between electrophysiological data and subjective experience.
Our data suggest that both VR and particularly MP can enhance the activation of brain patterns present during overt motor-execution. Further, we show changes in the interhemispheric EEG balance, which might play an important role in the promotion of neural activation and neuroplastic changes in stroke patients in a motor-imagery neurofeedback paradigm. In addition, electrophysiological correlates of psychophysiological responses provide us with valuable information about the motor and affective state of the user that has the potential to be used to predict MI-BCI training outcome based on user’s profile. Finally, we propose a BCI paradigm in VR, which gives the possibility of motor priming for patients with low level of motor control.
PMCID: PMC4977849  PMID: 27503007
Stroke rehabilitation; Brain-computer interfaces; Virtual reality; Motor priming; Motor imagery; Neurofeedback; EEG
12.  EEG oscillatory patterns and classification of sequential compound limb motor imagery 
A number of studies have been done on movement imagination of motor sequences with a single limb. However, brain oscillatory patterns induced by movement imagination of motor sequences involving multiple limbs have not been reported in recent years. The goal of the present study was to verify the feasibility of application of motor sequences involving multiple limbs to brain-computer interface (BCI) systems based on motor imagery (MI). The changes of EEG patterns and the inter-influence between movements associated with the imagination of motor sequences were also investigated.
The experiment, where 12 healthy subjects participated, involved one motor sequence with a single limb and three kinds of motor sequences with two or three limbs. The activity involved mental simulation, imagining playing drums with two conditions (60 and 30 beats per minute for the first and second conditions, respectively).
Movement imagination of different limbs in the sequence contributed to time-variant event-related desynchronization (ERD) patterns within both mu and beta rhythms, which was more obvious for the second condition compared with the first condition. The ERD values of left/right hand imagery with prior hand imagery were significantly larger than those with prior foot imagery, while the phase locking values (PLVs) between central electrodes and the mesial frontocentral electrode of non-initial movement were significantly larger than those of the initial movement during imagination of motor sequences for both conditions. Classification results showed that the power spectral density (PSD) based method outperformed the multi-class common spatial patterns (multi-CSP) based method: The highest accuracies were 82.86 % and 91.43 %, and the mean values were 65 % and 74.14 % for the first and second conditions, respectively.
This work implies that motor sequences involving multiple limbs can be utilized to build a multimodal classification paradigm in MI-based BCI systems, and that prior movement imagination can result in the changes of neural activities in motor areas during subsequent movement imagination in the process of limb switching.
PMCID: PMC4731999  PMID: 26822435
Sequential compound limb motor imagery; Event-related desynchronization; Phase locking value; Brain-computer interface; Support vector machine
13.  A Co-Adaptive Brain-Computer Interface for End Users with Severe Motor Impairment 
PLoS ONE  2014;9(7):e101168.
Co-adaptive training paradigms for event-related desynchronization (ERD) based brain-computer interfaces (BCI) have proven effective for healthy users. As of yet, it is not clear whether co-adaptive training paradigms can also benefit users with severe motor impairment. The primary goal of our paper was to evaluate a novel cue-guided, co-adaptive BCI training paradigm with severely impaired volunteers. The co-adaptive BCI supports a non-control state, which is an important step toward intuitive, self-paced control. A secondary aim was to have the same participants operate a specifically designed self-paced BCI training paradigm based on the auto-calibrated classifier. The co-adaptive BCI analyzed the electroencephalogram from three bipolar derivations (C3, Cz, and C4) online, while the 22 end users alternately performed right hand movement imagery (MI), left hand MI and relax with eyes open (non-control state). After less than five minutes, the BCI auto-calibrated and proceeded to provide visual feedback for the MI task that could be classified better against the non-control state. The BCI continued to regularly recalibrate. In every calibration step, the system performed trial-based outlier rejection and trained a linear discriminant analysis classifier based on one auto-selected logarithmic band-power feature. In 24 minutes of training, the co-adaptive BCI worked significantly (p = 0.01) better than chance for 18 of 22 end users. The self-paced BCI training paradigm worked significantly (p = 0.01) better than chance in 11 of 20 end users. The presented co-adaptive BCI complements existing approaches in that it supports a non-control state, requires very little setup time, requires no BCI expert and works online based on only two electrodes. The preliminary results from the self-paced BCI paradigm compare favorably to previous studies and the collected data will allow to further improve self-paced BCI systems for disabled users.
PMCID: PMC4094431  PMID: 25014055
14.  Factors of Influence on the Performance of a Short-Latency Non-Invasive Brain Switch: Evidence in Healthy Individuals and Implication for Motor Function Rehabilitation 
Brain-computer interfacing (BCI) has recently been applied as a rehabilitation approach for patients with motor disorders, such as stroke. In these closed-loop applications, a brain switch detects the motor intention from brain signals, e.g., scalp EEG, and triggers a neuroprosthetic device, either to deliver sensory feedback or to mimic real movements, thus re-establishing the compromised sensory-motor control loop and promoting neural plasticity. In this context, single trial detection of motor intention with short latency is a prerequisite. The performance of the event detection from EEG recordings is mainly determined by three factors: the type of motor imagery (e.g., repetitive, ballistic), the frequency band (or signal modality) used for discrimination (e.g., alpha, beta, gamma, and MRCP, i.e., movement-related cortical potential), and the processing technique (e.g., time-series analysis, sub-band power estimation). In this study, we investigated single trial EEG traces during movement imagination on healthy individuals, and provided a comprehensive analysis of the performance of a short-latency brain switch when varying these three factors. The morphological investigation showed a cross-subject consistency of a prolonged negative phase in MRCP, and a delayed beta rebound in sensory-motor rhythms during repetitive tasks. The detection performance had the greatest accuracy when using ballistic MRCP with time-series analysis. In this case, the true positive rate (TPR) was ~70% for a detection latency of ~200 ms. The results presented here are of practical relevance for designing BCI systems for motor function rehabilitation.
PMCID: PMC4720791  PMID: 26834551
brain-computer interface; motor intention detection; ballistic and repetitive task; movement-related cortical potential; sensory-motor rhythm
15.  EEG feature comparison and classification of simple and compound limb motor imagery 
Motor imagery can elicit brain oscillations in Rolandic mu rhythm and central beta rhythm, both originating in the sensorimotor cortex. In contrast with simple limb motor imagery, less work was reported about compound limb motor imagery which involves several parts of limbs. The goal of this study was to investigate the differences of the EEG patterns between simple limb motor imagery and compound limb motor imagery, and discuss the separability of multiple types of mental tasks.
Ten subjects participated in the experiment involving three tasks of simple limb motor imagery (left hand, right hand, feet), three tasks of compound limb motor imagery (both hands, left hand combined with right foot, right hand combined with left foot) and rest state. Event-related spectral perturbation (ERSP), power spectral entropy (PSE) and spatial distribution coefficient were adopted to analyze these seven EEG patterns. Then three algorithms of modified multi-class common spatial patterns (CSP) were used for feature extraction and classification was implemented by support vector machine (SVM).
The induced event-related desynchronization (ERD) affects more components within both alpha and beta bands resulting in more broad ERD bands at electrode positions C3, Cz and C4 during left/right hand combined with contralateral foot imagery, whose PSE values are significant higher than that of simple limb motor imagery. From the topographical distribution, simultaneous imagination of upper limb and contralateral lower limb certainly contributes to the activation of more areas on cerebral cortex. Classification result shows that multi-class stationary Tikhonov regularized CSP (Multi-sTRCSP) outperforms other two multi-class CSP methods, with the highest accuracy of 84% and mean accuracy of 70%.
The work implies that there exist the separable differences between simple limb motor imagery and compound limb motor imagery, which can be utilized to build a multimodal classification paradigm in motor imagery based brain-computer interface (BCI) systems.
PMCID: PMC3853015  PMID: 24119261
Compound limb motor imagery; Event-related desynchronization; Event-related spectral perturbation; Power spectral entropy; Spatial distribution coefficient; Common spatial patterns; Support vector machine
16.  Applying a brain-computer interface to support motor imagery practice in people with stroke for upper limb recovery: a feasibility study 
There is now sufficient evidence that using a rehabilitation protocol involving motor imagery (MI) practice in conjunction with physical practice (PP) of goal-directed rehabilitation tasks leads to enhanced functional recovery of paralyzed limbs among stroke sufferers. It is however difficult to confirm patient engagement during an MI in the absence of any on-line measure. Fortunately an EEG-based brain-computer interface (BCI) can provide an on-line measure of MI activity as a neurofeedback for the BCI user to help him/her focus better on the MI task. However initial performance of novice BCI users may be quite moderate and may cause frustration. This paper reports a pilot study in which a BCI system is used to provide a computer game-based neurofeedback to stroke participants during the MI part of a protocol.
The participants included five chronic hemiplegic stroke sufferers. Participants received up to twelve 30-minute MI practice sessions (in conjunction with PP sessions of the same duration) on 2 days a week for 6 weeks. The BCI neurofeedback performance was evaluated based on the MI task classification accuracy (CA) rate. A set of outcome measures including action research arm test (ARAT) and grip strength (GS), was made use of in assessing the upper limb functional recovery. In addition, since stroke sufferers often experience physical tiredness, which may influence the protocol effectiveness, their fatigue and mood levels were assessed regularly.
Positive improvement in at least one of the outcome measures was observed in all the participants, while improvements approached a minimal clinically important difference (MCID) for the ARAT. The on-line CA of MI induced sensorimotor rhythm (SMR) modulation patterns in the form of lateralized event-related desynchronization (ERD) and event-related synchronization (ERS) effects, for novice participants was in a moderate range of 60-75% within the limited 12 training sessions. The ERD/ERS change from the first to the last session was statistically significant for only two participants.
Overall the crucial observation is that the moderate BCI classification performance did not impede the positive rehabilitation trends as quantified with the rehabilitation outcome measures adopted in this study. Therefore it can be concluded that the BCI supported MI is a feasible intervention as part of a post-stroke rehabilitation protocol combining both PP and MI practice of rehabilitation tasks. Although these findings are promising, the scope of the final conclusions is limited by the small sample size and the lack of a control group.
PMCID: PMC3017056  PMID: 21156054
17.  MEG-based neurofeedback for hand rehabilitation 
Providing neurofeedback (NF) of motor-related brain activity in a biologically-relevant and intuitive way could maximize the utility of a brain-computer interface (BCI) for promoting therapeutic plasticity. We present a BCI capable of providing intuitive and direct control of a video-based grasp.
Utilizing magnetoencephalography’s (MEG) high temporal and spatial resolution, we recorded sensorimotor rhythms (SMR) that were modulated by grasp or rest intentions. SMR modulation controlled the grasp aperture of a stop motion video of a human hand. The displayed hand grasp position was driven incrementally towards a closed or opened state and subjects were required to hold the targeted position for a time that was adjusted to change the task difficulty.
We demonstrated that three individuals with complete hand paralysis due to spinal cord injury (SCI) were able to maintain brain-control of closing and opening a virtual hand with an average of 63 % success which was significantly above the average chance rate of 19 %. This level of performance was achieved without pre-training and less than 4 min of calibration. In addition, successful grasp targets were reached in 1.96 ± 0.15 s. Subjects performed 200 brain-controlled trials in approximately 30 min excluding breaks. Two of the three participants showed a significant improvement in SMR indicating that they had learned to change their brain activity within a single session of NF.
This study demonstrated the utility of a MEG-based BCI system to provide realistic, efficient, and focused NF to individuals with paralysis with the goal of using NF to induce neuroplasticity.
PMCID: PMC4578759  PMID: 26392353
Brain-Computer Interface; Neurofeedback; Spinal Cord Injury; Magnetoencephalography; Neuroplasticity; Rehabilitation
18.  Effects of Training Pre-Movement Sensorimotor Rhythms on Behavioral Performance: A Pilot Study 
Journal of neural engineering  2015;12(6):066021.
Brain–computer interface (BCI) technology might contribute to rehabilitation of motor function. This speculation is based on the premise that modifying the EEG will modify behavior, a proposition for which there is limited empirical data. The present study asked whether learned modulation of pre-motor sensorimotor rhythm (SMR) activity can affect motor performance in normal human subjects.
Eight individuals first performed a joystick-based cursor-movement task with variable warning periods. Targets appeared randomly on a video monitor and subjects moved the cursor to the target and pressed a select button within 2 sec. SMR features in the pre-movement EEG that correlated with performance speed and accuracy were identified. The subjects then learned to increase or decrease these features to control a two-target BCI task. Following successful BCI training, they were asked to increase or decrease SMR amplitude in order to initiate the joystick task.
After BCI training, pre-movement SMR amplitude was correlated with performance in subjects with initial poor performance: lower amplitude was associated with faster and more accurate movement. The beneficial effect on performance of lower SMR amplitude was greater in subjects with lower initial performance levels. These results indicate that BCI-based SMR training can affect a standard motor behavior. They provide a rationale for studies that integrate such training into rehabilitation protocols and examine its capacity to enhance restoration of useful motor function.
PMCID: PMC4843806  PMID: 26529119
19.  Towards a Cure for BCI Illiteracy 
Brain Topography  2009;23(2):194-198.
Brain–Computer Interfaces (BCIs) allow a user to control a computer application by brain activity as acquired, e.g., by EEG. One of the biggest challenges in BCI research is to understand and solve the problem of “BCI Illiteracy”, which is that BCI control does not work for a non-negligible portion of users (estimated 15 to 30%). Here, we investigate the illiteracy problem in BCI systems which are based on the modulation of sensorimotor rhythms. In this paper, a sophisticated adaptation scheme is presented which guides the user from an initial subject-independent classifier that operates on simple features to a subject-optimized state-of-the-art classifier within one session while the user interacts the whole time with the same feedback application. While initial runs use supervised adaptation methods for robust co-adaptive learning of user and machine, final runs use unsupervised adaptation and therefore provide an unbiased measure of BCI performance. Using this approach, which does not involve any offline calibration measurement, good performance was obtained by good BCI participants (also one novice) after 3–6 min of adaptation. More importantly, the use of machine learning techniques allowed users who were unable to achieve successful feedback before to gain significant control over the BCI system. In particular, one participant had no peak of the sensory motor idle rhythm in the beginning of the experiment, but could develop such peak during the course of the session (and use voluntary modulation of its amplitude to control the feedback application).
PMCID: PMC2874052  PMID: 19946737
Co-adaptive learning; Brain–computer interfaces; BCI illiteracy problem
20.  A novel channel selection method for optimal classification in different motor imagery BCI paradigms 
For sensorimotor rhythms based brain-computer interface (BCI) systems, classification of different motor imageries (MIs) remains a crucial problem. An important aspect is how many scalp electrodes (channels) should be used in order to reach optimal performance classifying motor imaginations. While the previous researches on channel selection mainly focus on MI tasks paradigms without feedback, the present work aims to investigate the optimal channel selection in MI tasks paradigms with real-time feedback (two-class control and four-class control paradigms).
In the present study, three datasets respectively recorded from MI tasks experiment, two-class control and four-class control experiments were analyzed offline. Multiple frequency-spatial synthesized features were comprehensively extracted from every channel, and a new enhanced method IterRelCen was proposed to perform channel selection. IterRelCen was constructed based on Relief algorithm, but was enhanced from two aspects: change of target sample selection strategy and adoption of the idea of iterative computation, and thus performed more robust in feature selection. Finally, a multiclass support vector machine was applied as the classifier. The least number of channels that yield the best classification accuracy were considered as the optimal channels. One-way ANOVA was employed to test the significance of performance improvement among using optimal channels, all the channels and three typical MI channels (C3, C4, Cz).
The results show that the proposed method outperformed other channel selection methods by achieving average classification accuracies of 85.2, 94.1, and 83.2 % for the three datasets, respectively. Moreover, the channel selection results reveal that the average numbers of optimal channels were significantly different among the three MI paradigms.
It is demonstrated that IterRelCen has a strong ability for feature selection. In addition, the results have shown that the numbers of optimal channels in the three different motor imagery BCI paradigms are distinct. From a MI task paradigm, to a two-class control paradigm, and to a four-class control paradigm, the number of required channels for optimizing the classification accuracy increased. These findings may provide useful information to optimize EEG based BCI systems, and further improve the performance of noninvasive BCI.
PMCID: PMC4618360  PMID: 26489759
EEG; Brain-computer interface (BCI); Motor imagery (MI); Relief; IterRelCen; Channel selection
21.  The Importance of Visual Feedback Design in BCIs; from Embodiment to Motor Imagery Learning 
PLoS ONE  2016;11(9):e0161945.
Brain computer interfaces (BCIs) have been developed and implemented in many areas as a new communication channel between the human brain and external devices. Despite their rapid growth and broad popularity, the inaccurate performance and cost of user-training are yet the main issues that prevent their application out of the research and clinical environment. We previously introduced a BCI system for the control of a very humanlike android that could raise a sense of embodiment and agency in the operators only by imagining a movement (motor imagery) and watching the robot perform it. Also using the same setup, we further discovered that the positive bias of subjects’ performance both increased their sensation of embodiment and improved their motor imagery skills in a short period. In this work, we studied the shared mechanism between the experience of embodiment and motor imagery. We compared the trend of motor imagery learning when two groups of subjects BCI-operated different looking robots, a very humanlike android’s hands and a pair of metallic gripper. Although our experiments did not show a significant change of learning between the two groups immediately during one session, the android group revealed better motor imagery skills in the follow up session when both groups repeated the task using the non-humanlike gripper. This result shows that motor imagery skills learnt during the BCI-operation of humanlike hands are more robust to time and visual feedback changes. We discuss the role of embodiment and mirror neuron system in such outcome and propose the application of androids for efficient BCI training.
PMCID: PMC5012560  PMID: 27598310
22.  Trained Modulation of Sensorimotor Rhythms Can Affect Reaction Time 
Brain-computer interface (BCI) technology might be useful for rehabilitation of motor function. This speculation is based on the premise that modifying the EEG will modify behavior, a proposition for which there is limited empirical data. The present study examined the possibility that voluntary modulation of sensorimotor rhythm (SMR) can affect motor behavior in normal human subjects.
Six individuals performed a cued-reaction task with variable warning periods. A typical variable foreperiod effect was associated with SMR desynchronization. SMR features that correlated with reaction times were then used to control a two-target cursor movement BCI task. Following successful BCI training, the reaction time task was embedded within the cursor movement task.
Voluntarily increasing SMR beta rhythms was associated with longer reaction times and decreasing SMR beta rhythms with shorter reaction times.
Voluntary modulation of EEG SMR can affect motor behavior.
These results encourage studies that integrate BCI training into rehabilitation protocols and examine its capacity to augment restoration of useful motor function.
PMCID: PMC3132832  PMID: 21411366
reaction time; EEG; brain-computer interface
23.  An MEG-based Brain-Computer Interface (BCI) 
NeuroImage  2007;36(3):581-593.
Brain-Computer Interfaces (BCIs) allow for communicating intentions by mere brain activity, not involving muscles. Thus, BCIs may offer patients who have lost all voluntary muscle control the only possible way to communicate. Many recent studies have demonstrated that BCIs based on electroencephalography (EEG) can allow healthy and severely paralyzed individuals to communicate. While this approach is safe and inexpensive, communication is slow. Magnetoencephalography (MEG) provides signals with higher spatiotemporal resolution than EEG, and could thus be used to explore whether these improved signal properties translate into increased BCI communication speed. In this study, we investigated the utility of an MEG-based BCI that uses voluntary amplitude modulation of sensorimotor μ and β rhythms. To increase the signal-to-noise ratio, we present a simple spatial filtering method that takes the geometric properties of signal propagation in MEG into account, and we present methods that can process artifacts specifically encountered in an MEG-based BCI. Exemplarily, six participants were successfully trained to communicate binary decisions by imagery of limb movements using a feedback paradigm. Participants achieved significant μ-rhythm self control within 32 minutes of feedback training. For a subgroup of three participants, we localized the origin of the amplitude modulated signal to the motor cortex. Our results suggest that an MEG-based BCI is feasible and efficient in terms of user training.
PMCID: PMC2017111  PMID: 17475511
Brain-computer interface; Magnetoencephalography; Real-time feedback; Mu rhythm; Source localization
24.  The Self-Paced Graz Brain-Computer Interface: Methods and Applications 
We present the self-paced 3-class Graz brain-computer interface (BCI) which is based on the detection of sensorimotor electroencephalogram (EEG) rhythms induced by motor imagery. Self-paced operation means that the BCI is able to determine whether the ongoing brain activity is intended as control signal (intentional control) or not (non-control state). The presented system is able to automatically reduce electrooculogram (EOG) artifacts, to detect electromyographic (EMG) activity, and uses only three bipolar EEG channels. Two applications are presented: the freeSpace virtual environment (VE) and the Brainloop interface. The freeSpace is a computer-game-like application where subjects have to navigate through the environment and collect coins by autonomously selecting navigation commands. Three subjects participated in these feedback experiments and each learned to navigate through the VE and collect coins. Two out of the three succeeded in collecting all three coins. The Brainloop interface provides an interface between the Graz-BCI and Google Earth.
PMCID: PMC2266812  PMID: 18350133
25.  The Influence of Psychological State and Motivation on Brain–Computer Interface Performance in Patients with Amyotrophic Lateral Sclerosis – a Longitudinal Study 
The current study investigated the effects of psychological well-being measured as quality of life (QoL), depression, current mood and motivation on brain–computer interface (BCI) performance in amyotrophic lateral sclerosis (ALS). Six participants with most advanced ALS were trained either for a block of 20 sessions with a BCI based on sensorimotor rhythms (SMR) or a block of 10 sessions with a BCI based on event-related potentials, or both. Questionnaires assessed QoL and severity of depressive symptoms before each training block and mood and motivation before each training session. The SMR-BCI required more training than the P300-BCI. The information transfer rate was higher with the P300-BCI (3.25 bits/min) than with the SMR-BCI (1.16 bits/min). Mood and motivation were related to the number of BCI sessions. Motivational factors, specifically challenge and mastery confidence, were positively related to BCI performance (controlled for the number of sessions) in tow participants, while incompetence fear was negatively related with performance in one participant. BCI performance was not related to motivational factors in three other participants nor to mood in any of the six participants. We conclude that motivational factors may be related to BCI performance in individual subjects and suggest that motivational factors and well-being should be assessed in standard BCI protocols. We also recommend using P300-based BCI as first choice in severely paralyzed patients who present with a P300 evoked potential.
PMCID: PMC2916671  PMID: 20700521
amyotrophic lateral sclerosis; brain–computer interface; motivation; mood; sensorimotor rhythms; P300 event-related potential

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