An exploration of BCI performance variations in people with amyotrophic lateral sclerosis using longitudinal EEG data.

OBJECTIVE: Brain-computer interface (BCI) technology enables people to use direct measures of brain activity for communication and control. The National Center for Adaptive Neurotechnologies and Helen Hayes Hospital are studying long-term independent home use of P300-based BCIs by people with amyotrophic lateral sclerosis (ALS). This BCI use takes place without technical oversight, and users can encounter substantial variation in their day-to-day BCI performance. The purpose of this study is to identify and evaluate features in the electroencephalogram (EEG) that correlate with successful BCI performance during home use with the goal of improving BCI for people with neuromuscular disorders. APPROACH: Nine people with ALS used a P300-based BCI at home over several months for communication and computer control. Sessions from a routine calibration task were categorized as successful ([Formula: see text]70%) or unsuccessful (<70%) BCI performance. The correlation of temporal and spectral EEG features with BCI performance was then evaluated. MAIN RESULTS: BCI performance was positively correlated with an increase in alpha-band (8-14 Hz) activity at locations PO8, P3, Pz, and P4; and beta-band (15-30 Hz) activity at occipital locations. In addition, performance was significantly positively correlated with a positive deflection in EEG amplitude around 220 ms at frontal mid-line locations (i.e. Fz and Cz). BCI performance was negatively correlated with delta-band (1-3 Hz) activity recorded from occipital locations. SIGNIFICANCE: These results highlight the variability found in the EEG and describe EEG features that correlate with successful BCI performance during day-to-day use of a P300-based BCI by people with ALS. These results should inform studies focused on improved BCI reliability for people with neuromuscular disorders.

Controlling pre-movement sensorimotor rhythm can improve finger extension after stroke.

OBJECTIVE: Brain-computer interface (BCI) technology is attracting increasing interest as a tool for enhancing recovery of motor function after stroke, yet the optimal way to apply this technology is unknown. Here, we studied the immediate and therapeutic effects of BCI-based training to control pre-movement sensorimotor rhythm (SMR) amplitude on robot-assisted finger extension in people with stroke. APPROACH: Eight people with moderate to severe hand impairment due to chronic stroke completed a four-week three-phase protocol during which they practiced finger extension with assistance from the FINGER robotic exoskeleton. In Phase 1, we identified spatiospectral SMR features for each person that correlated with the intent to extend the index and/or middle finger(s). In Phase 2, the participants learned to increase or decrease SMR features given visual feedback, without movement. In Phase 3, the participants were cued to increase or decrease their SMR features, and when successful, were then cued to immediately attempt to extend the finger(s) with robot assistance. MAIN RESULTS: Of the four participants that achieved SMR control in Phase 2, three initiated finger extensions with a reduced reaction time after decreasing (versus increasing) pre-movement SMR amplitude during Phase 3. Two also extended at least one of their fingers more forcefully after decreasing pre-movement SMR amplitude. Hand function, measured by the box and block test (BBT), improved by 7.3 ± 7.5 blocks versus 3.5 ± 3.1 blocks in those with and without SMR control, respectively. Higher BBT scores at baseline correlated with a larger change in BBT score. SIGNIFICANCE: These results suggest that learning to control person-specific pre-movement SMR features associated with finger extension can improve finger extension ability after stroke for some individuals. These results merit further investigation in a rehabilitation context.

EEG-Based Brain-Computer Interfaces.

Brain-Computer Interfaces (BCIs) are real-time computer-based systems that translate brain signals into useful commands. To date most applications have been demonstrations of proof-of-principle; widespread use by people who could benefit from this technology requires further development. Improvements in current EEG recording technology are needed. Better sensors would be easier to apply, more confortable for the user, and produce higher quality and more stable signals. Although considerable effort has been devoted to evaluating classifiers using public datasets, more attention to real-time signal processing issues and to optimizing the mutually adaptive interaction between the brain and the BCI are essential for improving BCI performance. Further development of applications is also needed, particularly applications of BCI technology to rehabilitation. The design of rehabilitation applications hinges on the nature of BCI control and how it might be used to induce and guide beneficial plasticity in the brain.

Trained modulation of sensorimotor rhythms can affect reaction time.

OBJECTIVE: 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. METHODS: 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, an uncued reaction time task was embedded within the cursor movement task. RESULTS: Voluntarily increasing SMR beta rhythms was associated with longer reaction times than decreasing SMR beta rhythms. CONCLUSIONS: Voluntary modulation of EEG SMR can affect motor behavior. SIGNIFICANCE: These results encourage studies that integrate BCI training into rehabilitation protocols and examine its capacity to augment restoration of useful motor function.

Does the 'P300' speller depend on eye gaze?

Many people affected by debilitating neuromuscular disorders such as amyotrophic lateral sclerosis, brainstem stroke or spinal cord injury are impaired in their ability to, or are even unable to, communicate. A brain-computer interface (BCI) uses brain signals, rather than muscles, to re-establish communication with the outside world. One particular BCI approach is the so-called 'P300 matrix speller' that was first described by Farwell and Donchin (1988 Electroencephalogr. Clin. Neurophysiol. 70 510-23). It has been widely assumed that this method does not depend on the ability to focus on the desired character, because it was thought that it relies primarily on the P300-evoked potential and minimally, if at all, on other EEG features such as the visual-evoked potential (VEP). This issue is highly relevant for the clinical application of this BCI method, because eye movements may be impaired or lost in the relevant user population. This study investigated the extent to which the performance in a 'P300' speller BCI depends on eye gaze. We evaluated the performance of 17 healthy subjects using a 'P300' matrix speller under two conditions. Under one condition ('letter'), the subjects focused their eye gaze on the intended letter, while under the second condition ('center'), the subjects focused their eye gaze on a fixation cross that was located in the center of the matrix. The results show that the performance of the 'P300' matrix speller in normal subjects depends in considerable measure on gaze direction. They thereby disprove a widespread assumption in BCI research, and suggest that this BCI might function more effectively for people who retain some eye-movement control. The applicability of these findings to people with severe neuromuscular disabilities (particularly in eye-movements) remains to be determined.

A novel P300-based brain-computer interface stimulus presentation paradigm: moving beyond rows and columns.

OBJECTIVE: An electroencephalographic brain-computer interface (BCI) can provide a non-muscular means of communication for people with amyotrophic lateral sclerosis (ALS) or other neuromuscular disorders. We present a novel P300-based BCI stimulus presentation - the checkerboard paradigm (CBP). CBP performance is compared to that of the standard row/column paradigm (RCP) introduced by Farwell and Donchin (1988). METHODS: Using an 8x9 matrix of alphanumeric characters and keyboard commands, 18 participants used the CBP and RCP in counter-balanced fashion. With approximately 9-12 min of calibration data, we used a stepwise linear discriminant analysis for online classification of subsequent data. RESULTS: Mean online accuracy was significantly higher for the CBP, 92%, than for the RCP, 77%. Correcting for extra selections due to errors, mean bit rate was also significantly higher for the CBP, 23 bits/min, than for the RCP, 17 bits/min. Moreover, the two paradigms produced significantly different waveforms. Initial tests with three advanced ALS participants produced similar results. Furthermore, these individuals preferred the CBP to the RCP. CONCLUSIONS: These results suggest that the CBP is markedly superior to the RCP in performance and user acceptability. SIGNIFICANCE: The CBP has the potential to provide a substantially more effective BCI than the RCP. This is especially important for people with severe neuromuscular disabilities.

Decoding flexion of individual fingers using electrocorticographic signals in humans.

Brain signals can provide the basis for a non-muscular communication and control system, a brain-computer interface (BCI), for people with motor disabilities. A common approach to creating BCI devices is to decode kinematic parameters of movements using signals recorded by intracortical microelectrodes. Recent studies have shown that kinematic parameters of hand movements can also be accurately decoded from signals recorded by electrodes placed on the surface of the brain (electrocorticography (ECoG)). In the present study, we extend these results by demonstrating that it is also possible to decode the time course of the flexion of individual fingers using ECoG signals in humans, and by showing that these flexion time courses are highly specific to the moving finger. These results provide additional support for the hypothesis that ECoG could be the basis for powerful clinically practical BCI systems, and also indicate that ECoG is useful for studying cortical dynamics related to motor function.

Toward a high-throughput auditory P300-based brain-computer interface.

OBJECTIVE: Brain-computer interface (BCI) technology can provide severely disabled people with non-muscular communication. For those most severely disabled, limitations in eye mobility or visual acuity may necessitate auditory BCI systems. The present study investigates the efficacy of the use of six environmental sounds to operate a 6x6 P300 Speller. METHODS: A two-group design was used to ascertain whether participants benefited from visual cues early in training. Group A (N=5) received only auditory stimuli during all 11 sessions, whereas Group AV (N=5) received simultaneous auditory and visual stimuli in initial sessions after which the visual stimuli were systematically removed. Stepwise linear discriminant analysis determined the matrix item that elicited the largest P300 response and thereby identified the desired choice. RESULTS: Online results and offline analyses showed that the two groups achieved equivalent accuracy. In the last session, eight of 10 participants achieved 50% or more, and four of these achieved 75% or more, online accuracy (2.8% accuracy expected by chance). Mean bit rates averaged about 2 bits/min, and maximum bit rates reached 5.6 bits/min. CONCLUSIONS: This study indicates that an auditory P300 BCI is feasible, that reasonable classification accuracy and rate of communication are achievable, and that the paradigm should be further evaluated with a group of severely disabled participants who have limited visual mobility. SIGNIFICANCE: With further development, this auditory P300 BCI could be of substantial value to severely disabled people who cannot use a visual BCI.

A P300-based brain-computer interface for people with amyotrophic lateral sclerosis.

OBJECTIVE: The current study evaluates the efficacy of a P300-based brain-computer interface (BCI) communication device for individuals with advanced ALS. METHODS: Participants attended to one cell of a N x N matrix while the N rows and N columns flashed randomly. Each cell of the matrix contained one character. Every flash of an attended character served as a rare event in an oddball sequence and elicited a P300 response. Classification coefficients derived using a stepwise linear discriminant function were applied to the data after each set of flashes. The character receiving the highest discriminant score was presented as feedback. RESULTS: In Phase I, six participants used a 6 x 6 matrix on 12 separate days with a mean rate of 1.2 selections/min and mean online and offline accuracies of 62% and 82%, respectively. In Phase II, four participants used either a 6 x 6 or a 7 x 7 matrix to produce novel and spontaneous statements with a mean online rate of 2.1 selections/min and online accuracy of 79%. The amplitude and latency of the P300 remained stable over 40 weeks. CONCLUSIONS: Participants could communicate with the P300-based BCI and performance was stable over many months. SIGNIFICANCE: BCIs could provide an alternative communication and control technology in the daily lives of people severely disabled by ALS.

Two-dimensional movement control using electrocorticographic signals in humans.

We show here that a brain-computer interface (BCI) using electrocorticographic activity (ECoG) and imagined or overt motor tasks enables humans to control a computer cursor in two dimensions. Over a brief training period of 12-36 min, each of five human subjects acquired substantial control of particular ECoG features recorded from several locations over the same hemisphere, and achieved average success rates of 53-73% in a two-dimensional four-target center-out task in which chance accuracy was 25%. Our results support the expectation that ECoG-based BCIs can combine high performance with technical and clinical practicality, and also indicate promising directions for further research.

Brain-computer interfaces (BCIs): detection instead of classification.

Many studies over the past two decades have shown that people can use brain signals to convey their intent to a computer through brain-computer interfaces (BCIs). These devices operate by recording signals from the brain and translating these signals into device commands. They can be used by people who are severely paralyzed to communicate without any use of muscle activity. One of the major impediments in translating this novel technology into clinical applications is the current requirement for preliminary analyses to identify the brain signal features best suited for communication. This paper introduces and validates signal detection, which does not require such analysis procedures, as a new concept in BCI signal processing. This detection concept is realized with Gaussian mixture models (GMMs) that are used to model resting brain activity so that any change in relevant brain signals can be detected. It is implemented in a package called SIGFRIED (SIGnal modeling For Real-time Identification and Event Detection). The results indicate that SIGFRIED produces results that are within the range of those achieved using a common analysis strategy that requires preliminary identification of signal features. They indicate that such laborious analysis procedures could be replaced by merely recording brain signals during rest. In summary, this paper demonstrates how SIGFRIED could be used to overcome one of the present impediments to translation of laboratory BCI demonstrations into clinically practical applications.

Toward enhanced P300 speller performance.

This study examines the effects of expanding the classical P300 feature space on the classification performance of data collected from a P300 speller paradigm [Farwell LA, Donchin E. Talking off the top of your head: toward a mental prosthesis utilizing event-related brain potentials. Electroenceph Clin Neurophysiol 1988;70:510-23]. Using stepwise linear discriminant analysis (SWLDA) to construct a classifier, the effects of spatial channel selection, channel referencing, data decimation, and maximum number of model features are compared with the intent of establishing a baseline not only for the SWLDA classifier, but for related P300 speller classification methods in general. By supplementing the classical P300 recording locations with posterior locations, online classification performance of P300 speller responses can be significantly improved using SWLDA and the favorable parameters derived from the offline comparative analysis.

Decoding two-dimensional movement trajectories using electrocorticographic signals in humans.

Signals from the brain could provide a non-muscular communication and control system, a brain-computer interface (BCI), for people who are severely paralyzed. A common BCI research strategy begins by decoding kinematic parameters from brain signals recorded during actual arm movement. It has been assumed that these parameters can be derived accurately only from signals recorded by intracortical microelectrodes, but the long-term stability of such electrodes is uncertain. The present study disproves this widespread assumption by showing in humans that kinematic parameters can also be decoded from signals recorded by subdural electrodes on the cortical surface (ECoG) with an accuracy comparable to that achieved in monkey studies using intracortical microelectrodes. A new ECoG feature labeled the local motor potential (LMP) provided the most information about movement. Furthermore, features displayed cosine tuning that has previously been described only for signals recorded within the brain. These results suggest that ECoG could be a more stable and less invasive alternative to intracortical electrodes for BCI systems, and could also prove useful in studies of motor function.

Spinal cord plasticity in acquisition and maintenance of motor skills.

Throughout normal life, activity-dependent plasticity occurs in the spinal cord as well as in brain. Like other central nervous system (CNS) plasticity, spinal cord plasticity can occur at numerous neuronal and synaptic sites and through a variety of mechanisms. Spinal cord plasticity is prominent early in life and contributes to mastery of standard behaviours like locomotion and rapid withdrawal from pain. Later in life, spinal cord plasticity has a role in acquisition and maintenance of new motor skills, and in compensation for peripheral and central changes accompanying ageing, disease and trauma. Mastery of the simplest behaviours is accompanied by complex spinal and supraspinal plasticity. This complexity is necessary, in order to preserve the complete behavioural repertoire, and is also inevitable, due to the ubiquity of activity-dependent CNS plasticity. Explorations of spinal cord plasticity are necessary for understanding motor skills. Furthermore, the spinal cord's comparative simplicity and accessibility makes it a logical starting point for studying skill acquisition. Induction and guidance of activity-dependent spinal cord plasticity will probably play an important role in realization of effective new rehabilitation methods for spinal cord injuries, cerebral palsy and other motor disorders.

An evaluation of autoregressive spectral estimation model order for brain-computer interface applications.

Autoregressive (AR) spectral estimation is a popular method for modeling the electroencephalogram (EEG), and therefore the frequency domain EEG phenomena that are used for control of a brain-computer interface (BCI). Several studies have been conducted to evaluate the optimal AR model order for EEG, but the criteria used in these studies does not necessarily equate to the optimal AR model order for sensorimotor rhythm (SMR)-based BCI control applications. The present study confirms this by evaluating the EEG spectra of data obtained during control of SMR-BCI using different AR model orders and model evaluation criteria. The results indicate that the AR model order that optimizes SMR-BCI control performance is generally higher than the model orders that are frequently used in SMR-BCI studies.

Patients with ALS can use sensorimotor rhythms to operate a brain-computer interface.

People with severe motor disabilities can maintain an acceptable quality of life if they can communicate. Brain-computer interfaces (BCIs), which do not depend on muscle control, can provide communication. Four people severely disabled by ALS learned to operate a BCI with EEG rhythms recorded over sensorimotor cortex. These results suggest that a sensorimotor rhythm-based BCI could help maintain quality of life for people with ALS.

EMG contamination of EEG: spectral and topographical characteristics.

OBJECTIVE: Electromyogram (EMG) contamination is often a problem in electroencephalogram (EEG) recording, particularly, for those applications such as EEG-based brain-computer interfaces that rely on automated measurements of EEG features. As an essential prelude to developing methods for recognizing and eliminating EMG contamination of EEG, this study defines the spectral and topographical characteristics of frontalis and temporalis muscle EMG over the entire scalp. It describes both average data and the range of individual differences. METHODS: In 25 healthy adults, signals from 64 scalp and 4 facial locations were recorded during relaxation and during defined (15, 30, or 70% of maximum) contractions of frontalis or temporalis muscles. RESULTS: In the average data, EMG had a broad frequency distribution from 0 to >200 Hz. Amplitude was greatest at 20-30 Hz frontally and 40-80 Hz temporally. Temporalis spectra also showed a smaller peak around 20 Hz. These spectral components attenuated and broadened centrally. Even with weak (15%) contraction, EMG was detectable (P<0.001) near the vertex at frequencies >12 Hz in the average data and >8 Hz in some individuals. CONCLUSIONS: Frontalis or temporalis muscle EMG recorded from the scalp has spectral and topographical features that vary substantially across individuals. EMG spectra often have peaks in the beta frequency range that resemble EEG beta peaks. SIGNIFICANCE: While EMG contamination is greatest at the periphery of the scalp near the active muscles, even weak contractions can produce EMG that obscures or mimics EEG alpha, mu, or beta rhythms over the entire scalp. Recognition and elimination of this contamination is likely to require recording from an appropriate set of peripheral scalp locations.

Effects of chronic nerve cuff and intramuscular electrodes on rat triceps surae motor units.

In order to assess the long-term effects of implanted electrodes on motor unit properties, we studied triceps surae (TS) motor units in rats implanted for 3-10 months with a tibial nerve cuff electrode for H-reflex elicitation and intramuscular electrodes for recording TS electromyographic activity. Motor units with sag from implanted rats displayed greater tetanic force than those from unimplanted rats. Motor units without sag had shorter twitch contraction times. This disrupted the relationship between sag and contraction time that was always present in unimplanted rats. These differences were consistent with a small degree of muscle denervation and subsequent reinnervation. Further analyses ascribed this effect to the nerve cuff rather than to the intramuscular electrodes. Comparable changes in motor unit properties may occur in humans with implanted nerve cuffs.

Motor unit properties after operant conditioning of rat H-reflex.

Operant conditioning of the H-reflex produces plasticity at several sites in the spinal cord, including the motoneuron. This study assessed whether this spinal cord plasticity is accompanied by changes in motor unit contractile properties. Thirty-one adult male Sprague-Dawley rats implanted for chronic recording of triceps surae electromyographic activity and H-reflex elicitation were exposed for at least 40 days to HRup or HRdown training, in which reward occurred when the H-reflex was greater than (12 HRup rats) or less than (12 HRdown rats) a criterion value, or continued under the control mode in which the H-reflex was simply measured (7 HRcon rats). At the end of H-reflex data collection, rats were anesthetized and the contractile properties of 797 single triceps surae motor units activated by intraaxonal (or intramyelin) current injection were determined. Motor units were classified as S, FR, Fint, or FF on the basis of sag and fatigue properties. Maximum tetanic force and twitch contraction time were also measured. HRdown rats exhibited a significant increase in the fatigue index of fast-twitch motor units. This resulted in a significant decrease in the percentage of Fint motor units and a significant increase in that of FR motor units. HRup conditioning had no effect on fatigue index. Neither HRup nor HRdown conditioning affected maximum tetanic force or twitch contraction time. These data are consistent with the hypothesis that conditioning mode-specific change in motoneuron firing patterns causes activity-dependent change in muscle properties.