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.

Using a smart wheelchair as a gaming device for floor-projected games: a mixed-reality environment for training powered-wheelchair driving skills.

For children with a severe disability, such as can arise from cerebral palsy, becoming independent in mobility is a critical goal. Currently, however, driver's training for powered wheelchair use is labor intensive, requiring hand-over-hand assistance from a skilled therapist to keep the trainee safe. This paper describes the design of a mixed reality environment for semi-autonomous training of wheelchair driving skills. In this system, the wheelchair is used as the gaming input device, and users train driving skills by maneuvering through floor-projected games created with a multi-projector system and a multi-camera tracking system. A force feedback joystick assists in steering and enhances safety.

Learning to perform a new movement with robotic assistance: comparison of haptic guidance and visual demonstration.

BACKGROUND: Mechanical guidance with a robotic device is a candidate technique for teaching people desired movement patterns during motor rehabilitation, surgery, and sports training, but it is unclear how effective this approach is as compared to visual demonstration alone. Further, little is known about motor learning and retention involved with either robot-mediated mechanical guidance or visual demonstration alone. METHODS: Healthy subjects (n = 20) attempted to reproduce a novel three-dimensional path after practicing it with mechanical guidance from a robot. Subjects viewed their arm as the robot guided it, so this "haptic guidance" training condition provided both somatosensory and visual input. Learning was compared to reproducing the movement following only visual observation of the robot moving along the path, with the hand in the lap (the "visual demonstration" training condition). Retention was assessed periodically by instructing the subjects to reproduce the path without robotic demonstration. RESULTS: Subjects improved in ability to reproduce the path following practice in the haptic guidance or visual demonstration training conditions, as evidenced by a 30-40% decrease in spatial error across 126 movement attempts in each condition. Performance gains were not significantly different between the two techniques, but there was a nearly significant trend for the visual demonstration condition to be better than the haptic guidance condition (p = 0.09). The 95% confidence interval of the mean difference between the techniques was at most 25% of the absolute error in the last cycle. When asked to reproduce the path repeatedly following either training condition, the subjects' performance degraded significantly over the course of a few trials. The tracing errors were not random, but instead were consistent with a systematic evolution toward another path, as if being drawn to an "attractor path". CONCLUSION: These results indicate that both forms of robotic demonstration can improve short-term performance of a novel desired path. The availability of both haptic and visual input during the haptic guidance condition did not significantly improve performance compared to visual input alone in the visual demonstration condition. Further, the motor system is inclined to repeat its previous mistakes following just a few movements without robotic demonstration, but these systematic errors can be reduced with periodic training.

Robotic assessment of locomotor recovery in spinal contused rats.

The purpose of this study was to investigate the ability of a robotic device, "the rat stepper", to assess intrinsic locomotor recovery following spinal cord contusion injury in adult rats. The device consists of a motorized body weight support mechanism that precisely controls the load to the hindlimbs during stepping, and two small robotic arms that measure and manipulate hindlimb movement. Sixteen rats received a contusion injury to the mid thoracic spinal cord with different severity levels (mild, moderate, severe, and sham). The animals were then evaluated weekly using the rat stepper, beginning one week after injury and continuing for a period of twelve weeks, across a range of body weight support levels. The contused animals demonstrated recovery in a standard locomotor assessment score (the BBB score), with most of the recovery occurring by four weeks post injury. We analyzed fourteen robotic measures of stepping and found that the measures that were most sensitive to intrinsic recovery were step velocity and inter limb coordination. These measures were also significantly correlated with the BBB score. The number of steps taken during testing was not sensitive to intrinsic recovery, nor correlated to the BBB score. These results suggest that step quality, rather than quantity, best reflects recovery after contusion injury in adult, untrained rats. Thus, robotic motion capture of only a few steps can provide a sensitive, valid measure of locomotor recovery after contusion.

Adaptive assistance for guided force training in chronic stroke.

This work describes a novel form of robotic therapy for the upper extremity in chronic stroke. Based on previous results, we hypothesized that a training task that encourages subjects to consciously guide endpoint forces generated by the hemiparetic arm will result in significant gains in functional ability of the arm, superior to more conventional methods of therapy. In addition, since stroke survivors present with varying degrees of arm movement ability, we developed an adaptive algorithm that tailors the amount of assistance provided in completing the guided force training task. The algorithm adapts a coefficient for velocity-dependent assistance based on measured movement speed, on a trial-to-trial basis. The training algorithm has been implemented with a simple linear robotic device called the ARM Guide. One participant completed a two month training program with the adaptive algorithm, resulting in significant improvements in the performance of functional tasks.

Accelerating motor adaptation by influencing neural computations.

When people learn to reach or step in a novel dynamic environment, they initially exhibit a large trajectory error, which they gradually reduce with practice. The error evolution is well modeled by a process in which the motor command on the next movement is adjusted in proportion to the previous movement's trajectory error. We hypothesized that we could accelerate motor adaptation by transiently increasing trajectory error. We tested this hypothesis by quantifying adaptation to a viscous force field applied during the swing phase of stepping in two conditions. In the first condition, we applied then removed the field for 75 steps each, for four iterations. Subjects adapted to each field exposure with a mean time constant of 3.4 steps. In the second condition, we repeated this experiment, but increased the strength of the field for only the first step in each field exposure. We predicted the field strength increase needed by solving a finite difference equation that described the error evolution. Adaptation was significantly faster when the field was transiently amplified (mean time constant = 2 trials). These results demonstrate that it is possible to increase the rate of adaptation to a novel dynamic environment based on knowledge of the computational mechanisms that underlie adaptation.

Motor adaptation as an optimal combination of computational strategies.

To efficiently and accurately manipulate objects, the nervous system must adjust motor commands based on experience. Four major adaptive strategies that could help achieve this goal are: internal model formation of the environmental dynamics, minimizing force, trajectory planning, and selectively stiffening the arm. We measured motor adaptation to a robotic force field with and without a large background force requirement. We then developed a computational model of motor adaptation that allowed the relative contribution of the four strategies to be estimated. Motor adaptation was best modeled as a blend of strategies, with internal model formation playing a greater role when forces were smaller and predictable; impedance control had a higher priority when forces were smaller and unpredictable; force minimization was more important when forces were larger; and trajectory planning was involved in both large and small background force conditions. These results are consistent with the viewpoint that the nervous system effectively seeks to minimize a cost-function containing force, stiffness, and position error terms.

Monitoring functional arm movement for home-based therapy after stroke.

The goal of this project is to develop a means for individuals with stroke to practice arm movement therapy at home with remote monitoring. We previously developed a Web-based system for repetitive movement training (Java Therapy). This paper describes a new input device for the system that measures and assists in naturalistic arm movement, as well as software enhancements. The new input device is an instrumented, adult-sized version of Wilmington robotic exoskeleton (WREX), which is a five degrees-of-freedom orthosis that counterbalances the weight of the arm using elastic bands. To test the ability of the new device (Training-WREX or "T-WREX") to measure and assist in functional arm movements, we measured five chronic stroke subjects' movement ability while wearing the orthosis without gravity balance compared to wearing the orthosis with gravity balance. T-WREX's gravity balance function improved a clinical measure of arm movement (Fugl-Meyer Score), range of motion of reaching movements, and accuracy of drawing movements. Coupled with an enhanced version of Java Therapy, T-WREX will thus provide a means to assist functional arm movement training at home, either over the Web in real-time, or stand-alone with periodic communication with a remote site.

Robotic gait training: toward more natural movements and optimal training algorithms.

This paper overviews our recent efforts to develop robotic devices to help people relearn how to walk after spinal cord injury. Our efforts are focused on two goals. The first is to develop robotic devices that allow natural gait movements and good force control. We have developed a five degrees-of-freedom robot (PAM) that accommodates natural pelvic movement during walking. PAM uses pneumatic actuators and a nonlinear control algorithm to achieve good force control. We have also developed a novel leg robot, ARTHuR, which makes use of a linear motor to precisely apply forces to the leg during stepping. Our second goal is to develop optimal training algorithms for robotic gait training. Toward this goal, we have developed a small-scale robotic device that allows us to test locomotor training techniques in rodent models. We have also developed an instrumentation system that allows us to measure how experienced therapists manually assist limb movement. Finally, we are developing computational models of motor rehabilitation. These models suggest that assisting in stepping only as needed with a force-controlled robotic device may be an effective method for improving locomotor recovery.

The rat lumbosacral spinal cord adapts to robotic loading applied during stance.

Load-related afferent information modifies the magnitude and timing of hindlimb muscle activity during stepping in decerebrate animals and spinal cord-injured humans and animals, suggesting that the spinal cord mediates load-related locomotor responses. In this study, we found that stepping on a treadmill by adult rats that received complete, midthoracic spinal cord transections as neonates could be altered by loading the hindlimbs using a pair of small robotic arms. The robotic arms applied a downward force to the lower shanks of the hindlimbs during the stance phase and measured the position of the lower shank during stepping. No external force was applied during the swing phase of the step. When applied bilaterally, this stance force field perturbed the hindlimb trajectories so that the ankle position was shifted downward during stance. In response to this perturbation, both the stance and step cycle durations decreased. During swing, the hindlimb initially accelerated toward the normal, unperturbed swing trajectory and then tracked the normal trajectory. Bilateral loading increased the magnitude of the medial gastrocnemius electromyographic (EMG) burst during stance and increased the amplitude of the semitendinosus and rectus femoris EMG bursts. When the force field was applied unilaterally, stance duration decreased in the loaded hindlimb, while swing duration was decreased in the contralateral hindlimb, thereby preserving interlimb coordination. These results demonstrate the feasibility of using robotic devices to mechanically modulate afferent input to the injured spinal cord during weight-supported locomotion. In addition, these results indicate that the lumbosacral spinal cord responds to load-related input applied to the lower shank during stance by modifying step timing and muscle activation patterns, while preserving normal swing kinematics and interlimb coordination.

Impedance control and internal model formation when reaching in a randomly varying dynamical environment.

We investigated the effects of trial-to-trial, random variation in environmental forces on the motor adaptation of human subjects during reaching. Novel sequences of dynamic environments were applied to subjects' hands by a robot. Subjects reached first in a "mean field" having a constant gain relating force and velocity, then in a "noise field," having a gain that varied randomly between reaches according to a normal distribution with a mean identical to that of the mean field. The unpredictable nature of the noise field did not degrade adaptation as quantified by final kinematic error and rate of adaptation. To achieve this performance, the nervous system used a dual strategy. It increased the impedance of the arm as evidenced by a significant reduction in aftereffect size following removal of the noise field. Simultaneously, it formed an internal model of the mean of the random environment, as evidenced by a minimization of trajectory error on trials for which the noise field gain was close to the mean field gain. We conclude that the human motor system is capable of predicting and compensating for the dynamics of an environment that varies substantially and randomly from trial to trial, while simultaneously increasing the arm's impedance to minimize the consequence of errors in the prediction.

Retraining the injured spinal cord.

The present review presents a series of concepts that may be useful in developing rehabilitative strategies to enhance recovery of posture and locomotion following spinal cord injury. First, the loss of supraspinal input results in a marked change in the functional efficacy of the remaining synapses and neurons of intraspinal and peripheral afferent (dorsal root ganglion) origin. Second, following a complete transection the lumbrosacral spinal cord can recover greater levels of motor performance if it has been exposed to the afferent and intraspinal activation patterns that are associated with standing and stepping. Third, the spinal cord can more readily reacquire the ability to stand and step following spinal cord transection with repetitive exposure to standing and stepping. Fourth, robotic assistive devices can be used to guide the kinematics of the limbs and thus expose the spinal cord to the new normal activity patterns associated with a particular motor task following spinal cord injury. In addition, such robotic assistive devices can provide immediate quantification of the limb kinematics. Fifth, the behavioural and physiological effects of spinal cord transection are reflected in adaptations in most, if not all, neurotransmitter systems in the lumbosacral spinal cord. Evidence is presented that both the GABAergic and glycinergic inhibitory systems are up-regulated following complete spinal cord transection and that step training results in some aspects of these transmitter systems being down-regulated towards control levels. These concepts and observations demonstrate that (a) the spinal cord can interpret complex afferent information and generate the appropriate motor task; and (b) motor ability can be defined to a large degree by training.

Persistence of motor adaptation during constrained, multi-joint, arm movements.

We studied the stability of changes in motor performance associated with adaptation to a novel dynamic environment during goal-directed movements of the dominant arm. Eleven normal, human subjects made targeted reaching movements in the horizontal plane while holding the handle of a two-joint robotic manipulator. This robot was programmed to generate a novel viscous force field that perturbed the limb perpendicular to the desired direction of movement. Following adaptation to this force field, we sought to determine the relative role of kinematic errors and dynamic criteria in promoting recovery from the adapted state. In particular, we compared kinematic and dynamic measures of performance when kinematic errors were allowed to occur after removal of the viscous fields, or prevented by imposing a simulated, mechanical "channel" on movements. Hand forces recorded at the handle revealed that when kinematic errors were prevented from occurring by the application of the channel, recovery from adaptation to the novel field was much slower compared with when kinematic aftereffects were allowed to take place. In particular, when kinematic errors were prevented, subjects persisted in generating large forces that were unnecessary to generate an accurate reach. The magnitude of these forces decreased slowly over time, at a much slower rate than when subjects were allowed to make kinematic errors. This finding provides strong experimental evidence that both kinematic and dynamic criteria influence motor adaptation, and that kinematic-dependent factors play a dominant role in the rapid loss of adaptation after restoring the original dynamics.

Understanding and treating arm movement impairment after chronic brain injury: progress with the ARM guide.

Significant potential exists for enhancing physical rehabilitation following neurologic injury through the use of robotic and mechatronic devices (or "rehabilitators"). We review the development of a rehabilitator (the "ARM Guide") to diagnose and treat arm movement impairment following stroke and other brain injuries. As a diagnostic tool, the ARM Guide provides a basis for evaluation of several key motor impairments, including abnormal tone, incoordination, and weakness. As a therapeutic tool, the device provides a means to implement and evaluate active assist therapy for the arm. Initial results with three stroke subjects demonstrate that such therapy can produce quantifiable benefits in the chronic hemiparetic arm. Directions for future research regarding the efficacy and practicality of rehabilitators are discussed.

Guidance-based quantification of arm impairment following brain injury: a pilot study.

This paper reports the design and preliminary testing of a device for evaluating arm impairment after brain injury. The assisted rehabilitation and measurement (ARM) Guide is capable of mechanically guiding reaching and retrieval movements across the workspace and of measuring constraint forces and range of motion during guidance. We tested the device on four hemiplegic brain-injured individuals and four unimpaired control subjects. During guided movement, the brain-injured subjects generated distinct spatial patterns of constraint force with their impaired arms that were consistent with the standard flexion and extension "synergies" described in the clinical literature. In addition, the impaired arms exhibited well-defined workspace deficits as measured by the ARM Guide. These results suggest that constraint force and range of motion measurements during mechanically guided movement may prove useful for precise monitoring of arm impairment and of the effects of treatment techniques targeted at abnormal synergies and workspace deficits.

Assessment of active and passive restraint during guided reaching after chronic brain injury.

We report the use of a mechatronic device for assessing arm movement impairment after chronic brain injury. The device, called the "Assisted Rehabilitation and Measurement Guide," is designed to guide reaching movements across the workspace, to measure movement and force generation, and to apply controlled forces to the arm along linear reaching paths. We performed a series of experiments using the device in order to identify the contribution of active muscle and passive tissue restraint to decreased active range of motion of guided reaching (i.e., "workspace deficits") in a group of five chronic, spastic hemiparetic, brain-injured subjects. Our findings were that passive tissue restraint was increased in the spastic arms, as compared to the contralateral, nonparetic arms. Active muscle restraint, on the other hand, was typically comparable in the two arms, as quantified by measurements of active arm stiffness at the workspace boundary during reaching. In all subjects, there was evidence of movement-generated weakness, consistent with a small contribution of spasticity to workspace deficits. These results demonstrate the feasibility of mechatronic assessment of the causes of decreased functional movement, and could provide a basis for enhanced treatment planning and monitoring following brain injury.

Mechatronic assessment of arm impairment after chronic brain injury.

Significant potential exists for mechatronic devices to improve assessment and treatment of individuals with a movement disability following stroke, traumatic brain injury, or cerebral palsy. We report the use of a mechatronic device for evaluation of the arm after chronic brain injury. We performed a series of experiments with the device in order to identify the relative contribution of three different motor impairments to decreased active range of motion of reaching in five brain-injured subjects. Our findings were that passive tissue restraint and agonist weakness, rather than antagonist restraint, were the most common contributors to decreased active range of motion. These results demonstrate the feasibility of objective assessment of functional movement using a mechatronic device, and could provide the basis for improved, individualized treatment planning and monitoring following brain injury.

Human control of a simple two-hand grasp.

We investigated how people control fast, accurate movements of a load using a simple two-hand grasp. By providing a clear instruction to several subjects, we isolated a single control strategy. The kinematics produced by this control strategy are nearly indistinguishable from those produced during singlehand movements, but the torques are quite different: one hand accelerates not only itself, but also the load and the other hand, while the other hand brakes the hand-load-hand system. As a result, the hands squeeze the load with a large force during the movement. The dynamics of the hand-load-hand system are of the same form as the dynamics of a single-hand system. Apparently, by taking advantage of this dynamic similarity and of the spring-like properties of muscle, the human motor control system can control the two-hand grasp system simply by modifying the muscle activation patterns used to control single-hand movements. The task dynamics of two-hand grasp do not require that the load be squeezed during the movement, and squeezing the load wastes torque that could be used to move more quickly. However, the human motor control system may choose this squeezing strategy because it reliably brakes the hand-load-hand system despite inherent variability in the braking of individual hands.

Feedforward stabilization in a bimanual unloading task.

When one hand removes a load from the other hand, feedforward motor commands stabilize the position of the unloaded hand. We studied the stabilization of the postural hand using a novel apparatus that allowed unloading at different rates, and unexpected uncoupling of the unloading force from the postural hand. Feedforward stabilization of hand position was observed in all subjects. This stabilization was achieved both by deactivation of postural agonist muscles and by activation of postural antagonist muscles. The neural feedforward command apparently increased with unloading rate. However, the command only partially canceled the interaction torque generated by removing the load, and stabilization became less effective as unloading rate increased.