Electromagnetic muscle stretch strongly excites sensorimotor cortex neurons in behaving primates.

Responses of single units in primary motor and sensory cortex of behaving primates to electromagnetic stretch of the muscle flexor carpi ulnaris are comparable in latency and intensity to responses to wrist extension. Thus, muscle stretch appears to be a major factor in cortical response to limb displacement during performance and probably has an important role in motor control at the cortical level.

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.

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.

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.

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.

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.

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.

The complex structure of a simple memory.

Operant conditioning of the vertebrate H-reflex, which appears to be closely related to learning that occurs in real life, is accompanied by plasticity at multiple sites. Change occurs in the firing threshold and conduction velocity of the motoneuron, in several different synaptic terminal populations on the motoneuron, and probably in interneurons as well. Change also occurs contralaterally. The corticospinal tract probably has an essential role in producing this plasticity. While certain of these changes, such as that in the firing threshold, are likely to contribute to the rewarded behavior (primary plasticity), others might preserve previously learned behaviors (compensatory plasticity), or are simply activity-driven products of change elsewhere (reactive plasticity). As these data and those from other simple vertebrate and invertebrate models indicate, a complex pattern of plasticity appears to be the necessary and inevitable outcome of even the simplest learning.

Memory traces in spinal cord.

The complexity and inaccessibility of the vertebrate CNS impede the localization and description of memory traces and the definition of the processes that create them. Recent work has shown that the spinal stretch reflex (SSR), which is produced by a monosynaptic two-neuron pathway, can be operantly conditioned, and that memory traces responsible for this behavioral change reside in the spinal cord. The probable locations are the terminal of the Ia affernt neuron on the motoneuron and/or the motoneuron itself. Because it modifies a simple well-defined and accessible pathway, SSR conditioning may be a valuable experimental model for studying vertebrate memory.

Triceps surae motoneuron morphology in the rat: a quantitative light microscopic study.

The rat is now the model of choice for many studies of motor function. However, little quantitative information on the structure of rat motoneurons is available. In conjunction with efforts to define the physiologic and anatomic substrates of operantly conditioned plasticity in the spinal cord, 13 physiologically identified triceps surae motoneurons in the rat lumbar spinal cord were labeled intracellularly with horseradish peroxidase and completely reconstructed and measured with a computer-based neuron-tracing system. Somata were all located in the ventral horn of lumbar segments 4-5, had an average diameter of 35 microns, and had 6-12 dendrites. Dendrites ramified throughout the ventral horn and also penetrated the white matter. Their spread was greater in the rostrocaudal and dorsoventral directions (1.53 +/- 0.24 mm and 1.35 +/- 0.23 mm, respectively) than in the mediolateral direction (0.85 +/- 0.14 mm). Regardless of soma location, dendritic fields usually extended throughout the ipsilateral coronal cross-section of the ventral horn. As a result, the ventral or lateral extent of the field was correlated strongly with the soma's distance from the ventral or lateral border, respectively, of the ventral horn. Furthermore, although soma locations in the coronal plane varied widely, the centers of the dendritic fields tended to cluster near the center of the ventral horn. Dendrites constituted 96.2-98.4% (mean +/- SD = 97.3 +/- 0.7%) of the total neuronal surface area. Each of the 104 dendrites studied had an average of 13 branch points and 27 segments. First-order segment diameters ranged from 1.4 to 11.7 microns (mean +/- SD = 5.3 +/- 2.1 microns). Total dendritic length, surface area, volume, number of dendritic segments, and maximum segment order were correlated strongly with diameter of the first-order segment. Proceeding distally between branch points, the mean decrease in dendritic diameter (i.e., tapering) +/- the standard deviation was 22 +/- 8% of the proximal diameter. The average ratio +/- the standard deviation of the sum of the average diameters of each daughter segment raised to the 1.5 power to the average diameter of the parent segment raised to the 1.5 power (i.e., Rall's ratio; Rall, 1959) was 0.87 +/- 0.08. In comparison with cat alpha-motoneurons, rat motoneurons had smaller soma diameters, fewer dendrites, smaller total surface areas, and shorter total dendritic lengths. However, the number of terminations per dendrite was similar in the two species, so that rat motoneurons had more terminations per unit dendritic length.(ABSTRACT TRUNCATED AT 400 WORDS)

Synaptic terminal coverage of primate triceps surae motoneurons.

This study examined the synaptic terminal coverage of primate triceps surae (TS) motoneurons at the electron microscopic level. In three male pigtail macaques, motoneurons were labeled by retrograde transport of cholera toxin-horseradish peroxidase that was injected into TS muscles bilaterally and visualized with tetramethylbenzidine stabilized with diaminobenzidine. Somatic, proximal dendritic, and distal dendritic synaptic terminals were classified by standard criteria and measured. Overall and type-specific synaptic terminal coverages and frequencies were determined. Labeled cells were located in caudal L5 to rostral S1 ventral horn and ranged from 40 to 74 microns in diameter (average, 54 microns). The range and unimodal distribution of diameters, the label used, and the presence of C terminals on almost all cells indicated that the 15 cell bodies and associated proximal dendrites analyzed here probably belonged to alpha-motoneurons. Synaptic terminals covered 39% of the cell body membrane, 60% of the proximal dendritic membrane, and 40% of the distal dendritic membrane. At each of these three sites, F terminals (flattened or pleomorphic vesicles, usually symmetric active zones, average contact length 1.6 microns) were most common, averaging 52%, 56%, and 58% of total coverage and 56%, 57%, and 58% of total number of cell bodies, proximal dendrites, and distal dendrites respectively. S terminals (round vesicles, usually asymmetric active zones, average contact length 1.3 microns) averaged 24%, 29%, and 33% of coverage and 33%, 35%, and 36% of number at these three sites, respectively. Thus, S terminals were slightly more prominent relative to F terminals on distal dendrites than on cell bodies. C terminals (spherical vesicles, subsynaptic cisterns associated with rough endoplasmic reticulum, average contact length 3.5 microns) constituted 24% and 11% of total terminal coverage on cell bodies and proximal dendrites, respectively, and averaged 11% and 6% of terminal number at these two locations. M terminals (spherical vesicles, postsynaptic Taxi bodies, some with presynaptic terminals, average contact length 2.7 microns) were absent on cell bodies and averaged 3% and 7% of total coverage and 2% and 5% of terminals on proximal and distal dendrites, respectively. Except for M terminals, which tended to be smaller distally, terminal contact length was not correlated with location. Total and type-specific coverages and frequencies were not correlated with cell body diameter. Primate TS motoneurons are similar to cat TS motoneurons in synaptic terminal morphology, frequency, and distribution. However, primate terminals appear to be smaller, so that the fraction of membrane covered by them is lower.

Brain-computer communication: unlocking the locked in.

With the increasing efficiency of life-support systems and better intensive care, more patients survive severe injuries of the brain and spinal cord. Many of these patients experience locked-in syndrome: The active mind is locked in a paralyzed body. Consequently, communication is extremely restricted or impossible. A muscle-independent communication channel overcomes this problem and is realized through a brain-computer interface, a direct connection between brain and computer. The number of technically elaborated brain-computer interfaces is in contrast with the number of systems used in the daily life of locked-in patients. It is hypothesized that a profound knowledge and consideration of psychological principles are necessary to make brain-computer interfaces feasible for locked-in patients.

Operant conditioning of H-reflex in spinal cord-injured rats.

Operant conditioning of the spinal stretch reflex or its electrical analog, the H-reflex, is a new model for exploring the mechanisms of supraspinal control over spinal cord function. Both rats and primates can gradually increase (HRup conditioning mode) or decrease (HRdown conditioning mode) soleus H-reflex magnitude when exposed to an operant conditioning task. This study used H-reflex operant conditioning to assess and modify spinal cord function after injury. Soleus H-reflexes were elicited and recorded with chronically implanted electrodes from rats that had been subjected to calibrated contusion injuries to the spinal cord at T8. From 18 to 140 days after injury, background EMG, M response amplitude, and initial H-reflex amplitude were not significantly different from those of normal rats. HRdown conditioning was successful in some, but not all, spinal cord-injured rats. The H-reflex decrease achieved by conditioning was inversely correlated with the severity of the injury as assessed histologically or by time to return of bladder function. It was not correlated with the length of time between injury and the beginning of conditioning. The results confirm the importance of descending control from supraspinal structures in mediating operantly conditioned change in H-reflex amplitude. In conjunction with recent human studies, they suggest that H-reflex conditioning could provide a sensitive new means for assessing spinal cord function after injury, and might also provide a method for initiating and guiding functional rehabilitation.

Short-Term and medium-term effects of spinal cord tract transections on soleus H-reflex in freely moving rats.

Spinal cord function is normally influenced by descending activity from supraspinal structures. When injury removes or distorts this influence, function changes and spasticity and other disabling problems eventually appear. Understanding how descending activity affects spinal cord function could lead to new means for inducing, guiding, and assessing recovery after injury. In this study, we investigated the short-term and medium-term effects of spinal cord bilateral dorsal column (DC), unilateral (ipsilateral) lateral column (LC), bilateral dorsal column ascending tract (DA), or bilateral dorsal column corticospinal tract (CST) transection at vertebral level T8-T9 on the soleus H-reflex in freely moving rats. Data were collected continuously for 10-20 days before and for 20-155 days after bilateral DC (13 rats), DA (10 rats), CST (eight rats), or ipsilateral LC (seven rats) transection. Histological examination showed that transections were 98(+/- 3 SD)% complete for DC rats, 80(+/- 20)% complete for LC rats, 91(+/- 13 SD)% complete for DA rats, and 95(+/-13)% complete for CST rats. LC, CST, and DA transections produced an immediate (i.e., first-day) increase in H-reflex amplitude. LC transection also produced a small decrease in background activity in the first few posttransection days. Other than this small decrease, none of the transections produced evidence for the phenomenon of spinal shock. For all transections, all measures returned to or neared pretransection values within 2 weeks. DA and LC transections were associated with modest increase in H-reflex amplitude 1-3 months after transection. These medium-term effects must be taken into account when assessing transection effects on operant conditioning of the H-reflex. At the same time, the results are consistent with other evidence that, while H-reflex rate dependence and H-reflex operant conditioning are sensitive measures of spinal cord injury, the H-reflex itself is not.

Operant conditioning of H-reflex increase in spinal cord--injured rats.

Operant conditioning of the spinal stretch reflex or its electrical analog, the H-reflex, is a new model for exploring the mechanisms of long-term supraspinal control over spinal cord function. Primates and rats can gradually increase (HRup conditioning mode) or decrease (HRdown conditioning mode) the H-reflex when reward is based on H-reflex amplitude. An earlier study indicated that HRdown conditioning of the soleus H-reflex in rats is impaired following contusion injury to thoracic spinal cord. The extent of impairment was correlated with the percent of white matter lost at the injury site. The present study investigated the effects of spinal cord injury on HRup conditioning. Soleus H-reflexes were elicited and recorded with chronically implanted electrodes from 14 rats that had been subjected to calibrated contusion injuries to the spinal cord at T8. At the lesion epicenter, 12-39% of the white matter remained. After control-mode data were collected, each rat was exposed to the HRup conditioning mode for 50 days. Final H-reflex amplitudes after HRup conditioning averaged 112% (+/-22% SD) of control. This value was significantly smaller than that for 13 normal rats exposed to HRup conditioning, in which final amplitude averaged 153% (+/-51%) SD of control. As previously reported for HRdown conditioning after spinal cord injury, success was inversely correlated with the severity of the injury as assessed by white matter preservation and by time to return of bladder function. HRup and HRdown conditioning are similarly sensitive to injury. These results further demonstrate that H-reflex conditioning is a sensitive measure of the long-term effects of injury on supraspinal control over spinal cord functions and could prove a valuable measure of therapeutic efficacy.

Operantly conditioned plasticity in spinal cord.

Recent work has shown that the monosynaptic pathway of the SSR can be operantly conditioned, and that a significant part of the plasticity responsible for the behavioral change resides in the spinal cord. The most likely sites of this activity-driven plasticity are the synapse of the Ia afferent neuron on the motoneuron and/or the motoneuron itself. Because the SSR pathway is the simplest and most accessible stimulus-response pathway in the vertebrate CNS, it may provide a valuable experimental model for elucidating activity-driven CNS changes responsible for learning.

Operant conditioning of H-reflex in freely moving monkeys.

The H-reflex, the electrical analog of the stretch reflex or tendon jerk, is the simplest behavior of the primate CNS. It is subserved by a wholly spinal two-neuron reflex arc. Recent studies show that this reflex can be increased or decreased by operant conditioning, and that such conditioning causes plastic changes in the spinal cord itself. Thus, H-reflex conditioning provides a powerful new model for investigating primate memory traces. The key feature of this model, the conditioning task, originally required animal restraint. This report describes a new tether-based design that allows H-reflex measurement and conditioning without restraint. This design integrates the conditioning task into the life of the freely moving animal.

Adaptive plasticity in the primate spinal stretch reflex: reversal and re-development.

Monkeys can gradually increase or decrease the amplitude of the segmentally mediated spinal stretch reflex (SSR) without change in initial muscle length or background EMG activity. Both increase (under the SSR increases mode) and decrease (under the SSR decreases mode) occur slowly, progressing steadily over weeks. The present study investigated reversal and re-development of SSR amplitude change. Over a period of months, following collection of control data, monkeys were exposed to one mode, then to the other, and then to the first mode again. Development, reversal, and re-development of change all took place over weeks, following very similar courses. These data are consistent with the hypothesis that persistent segmental alteration underlies SSR amplitude change. Such persistent segmental alteration would constitute a technically accessible substrate of memory.