Vincent S. Huang

Robotic neurorehabilitation: a computational motor learning perspective

Conventional neurorehabilitation appears to have little impact on impairment over and above that of spontaneous biological recovery. Robotic neurorehabilitation has the potential for a greater impact on impairment due to easy deployment, its applicability across of a wide range of motor impairment, its high measurement reliability, and the capacity to deliver high dosage and high intensity training protocols.We first describe current knowledge of the natural history of arm recovery after stroke and of outcome prediction in individual patients. Rehabilitation strategies and outcome measures for impairment versus function are compared. The topics of dosage, intensity, and time of rehabilitation are then discussed.Robots are particularly suitable for both rigorous testing and application of motor learning principles to neurorehabilitation. Computational motor control and learning principles derived from studies in healthy subjects are introduced in the context of robotic neurorehabilitation. Particular attention is paid to the idea of context, task generalization and training schedule. The assumptions that underlie the choice of both movement trajectory programmed into the robot and the degree of active participation required by subjects are examined. We consider rehabilitation as a general learning problem, and examine it from the perspective of theoretical learning frameworks such as supervised and unsupervised learning. We discuss the limitations of current robotic neurorehabilitation paradigms and suggest new research directions from the perspective of computational motor learning.

Improvement After Constraint-Induced Movement Therapy Recovery of Normal Motor Control or Task-Specific Compensation?

Background. Constraint-induced movement therapy (CIMT) has proven effective in increasing functional use of the affected arm in patients with chronic stroke. The mechanism of CIMT is not well understood. Objective. To demonstrate, in a proof-of-concept study, the feasibility of using kinematic measures in conjunction with clinical outcome measures to better understand the mechanism of recovery in chronic stroke patients with mild to moderate motor impairments who undergo CIMT. Methods. A total of 10 patients with chronic stroke were enrolled in a modified CIMT protocol over 2 weeks. Treatment response was assessed with the Action Research Arm Test (ARAT), the Upper-Extremity Fugl-Meyer score (FM-UE), and kinematic analysis of visually guided arm and wrist movements. All assessments were performed twice before the therapeutic intervention and once afterward. Results. There was a clinically meaningful improvement in ARAT from the second pre-CIMT session to the post-CIMT session compared with the change between the 2 pre-CIMT sessions. In contrast, FM-UE and kinematic measures showed no meaningful improvements. Conclusions. Functional improvement in the affected arm after CIMT in patients with chronic stroke appears to be mediated through compensatory strategies rather than a decrease in impairment or return to more normal motor control. We suggest that future large-scale studies of new interventions for neurorehabilitation track performance using kinematic analyses as well as clinical scales.

Persistence of motor memories reflects statistics of the learning event

Learning to control a new tool (i.e., a novel environment) produces an internal model, i.e., a motor memory that allows the brain to implicitly predict the behavior of the tool. Data from a wide array of experiments suggest that formation of motor memory is not a single process, but one that is due to multiple adaptive processes with different time constants. Here we asked whether these time constants are invariant or are they influenced by the statistics of the learning event. To measure the time constants, we controlled the statistics of the learning event in a reaching task and then assayed the decay rates of motor output in a set of trials in which errors were effectively removed. We found that prior experience with a rapid change in the environment increased the decay rate of memories acquired later in response to a gradual change in the same environment. Prior experience in an environment that changed gradually reduced the decay rates of memories acquired later in response to a rapid change in that same environment. Indeed we found that by manipulating the prior statistics of the learning experience, we could readily alter the decay rates of a given motor memory. This suggests that time scales of processes that support motor memory are not constant. Rather decay of motor memory is the brains implicit estimate of how likely it is that the environment will change with time. During motor learning, prior statistics that suggest changes are likely to be permanent result in slowly decaying memories, whereas prior statistics that suggest changes are transient result in rapidly decaying memories.

Overcoming Motor “Forgetting” Through Reinforcement Of Learned Actions

The human motor system rapidly adapts to systematic perturbations but the adapted behavior seems to be forgotten equally rapidly. The reason for this forgetting is unclear, as is how to overcome it to promote long-term learning. Here we show that adapted behavior can be stabilized by a period of binary feedback about success and failure in the absence of vector error feedback. We examined the time course of decay after adaptation to a visuomotor rotation through a visual error-clamp condition—trials in which subjects received false visual feedback showing perfect directional performance, regardless of the movements they actually made. Exposure to this error-clamp following initial visuomotor adaptation led to a rapid reversion to baseline behavior. In contrast, exposure to binary feedback after initial adaptation turned the adapted state into a new baseline, to which subjects reverted after transient exposure to another visuomotor rotation. When both binary feedback and vector error were present, some subjects exhibited rapid decay to the original baseline, while others persisted in the new baseline. We propose that learning can be decomposed into two components—a fast-learning, fast-forgetting adaptation process that is sensitive to vector errors and insensitive to task success, and a second process driven by success that learns more slowly but is less susceptible to forgetting. These two learning systems may be recruited to different degrees across individuals. Understanding this competitive balance and exploiting the long-term retention properties of learning through reinforcement is likely to be essential for successful neuro-rehabilitation.

Robotic therapy for chronic stroke: general recovery of impairment or improved task-specific skill?

There is a great need to develop new approaches for rehabilitation of the upper limb after stroke. Robotic therapy is a promising form of neurorehabilitation that can be delivered in higher doses than conventional therapy. Here we sought to determine whether the reported effects of robotic therapy, which have been based on clinical measures of impairment and function, are accompanied by improved motor control. Patients with chronic hemiparesis were trained for 3 wk, 3 days a week, with titrated assistive robotic therapy in two and three dimensions. Motor control improvements (i.e., skill) in both arms were assessed with a separate untrained visually guided reaching task. We devised a novel PCA-based analysis of arm trajectories that is sensitive to changes in the quality of entire movement trajectories without needing to prespecify particular kinematic features. Robotic therapy led to skill improvements in the contralesional arm. These changes were not accompanied by changes in clinical measures of impairment or function. There are two possible interpretations of these results. One is that robotic therapy only leads to small task-specific improvements in motor control via normal skill-learning mechanisms. The other is that kinematic assays are more sensitive than clinical measures to a small general improvement in motor control.

Persistent Residual Errors in Motor Adaptation Tasks: Reversion to Baseline and Exploratory Escape

When movements are perturbed in adaptation tasks, humans and other animals show incomplete compensation, tolerating small but sustained residual errors that persist despite repeated trials. State-space models explain this residual asymptotic error as interplay between learning from error and reversion to baseline, a form of forgetting. Previous work using zero-error-clamp trials has shown that reversion to baseline is not obligatory and can be overcome by manipulating feedback. We posited that novel error-clamp trials, in which feedback is constrained but has nonzero error and variance, might serve as a contextual cue for recruitment of other learning mechanisms that would then close the residual error. When error clamps were nonzero and had zero variance, human subjects changed their learning policy, using exploration in response to the residual error, despite their willingness to sustain such an error during the training block. In contrast, when the distribution of feedback in clamp trials was naturalistic, with persistent mean error but also with variance, a state-space model accounted for behavior in clamps, even in the absence of task success. Therefore, when the distribution of errors matched those during training, state-space models captured behavior during both adaptation and error-clamp trials because error-based learning dominated; when the distribution of feedback was altered, other forms of learning were triggered that did not follow the state-space model dynamics exhibited during training. The residual error during adaptation appears attributable to an error-dependent learning process that has the property of reversion toward baseline and that can suppress other forms of learning.