Cheol E. Han

Motor Learning Without Doing: Trial-by-Trial Improvement in Motor Performance During Mental Training

Although there is converging experimental and clinical evidences suggesting that mental training with motor imagery can improve motor performance, it is unclear how humans can learn movements through mental training despite the lack of sensory feedback from the body and the environment. In a first experiment, we measured the trial-by-trial decrease in durations of executed movements (physical training group) and mentally simulated movements (motor-imagery training group), by means of training on a multiple-target arm-pointing task requiring high accuracy and speed. Movement durations were significantly lower in posttest compared with pretest after both physical and motor-imagery training. Although both the posttraining performance and the rate of learning were smaller in motor-imagery training group than in physical training group, the change in movement duration and the asymptotic movement duration after a hypothetical large number of trials were identical. The two control groups (eye-movement training and rest groups) did not show change in movement duration. In the second experiment, additional kinematic analyses revealed that arm movements were straighter and faster both immediately and 24 h after physical and motor-imagery training. No such improvements were observed in the eye-movement training group. Our results suggest that the brain uses state estimation, provided by internal forward model predictions, to improve motor performance during mental training. Furthermore, our results suggest that mental practice can, at least in young healthy subjects and if given after a short bout of physical practice, be successfully substituted to physical practice to improve motor performance.

Stroke rehabilitation reaches a threshold.

Motor training with the upper limb affected by stroke partially reverses the loss of cortical representation after lesion and has been proposed to increase spontaneous arm use. Moreover, repeated attempts to use the affected hand in daily activities create a form of practice that can potentially lead to further improvement in motor performance. We thus hypothesized that if motor retraining after stroke increases spontaneous arm use sufficiently, then the patient will enter a virtuous circle in which spontaneous arm use and motor performance reinforce each other. In contrast, if the dose of therapy is not sufficient to bring spontaneous use above threshold, then performance will not increase and the patient will further develop compensatory strategies with the less affected hand. To refine this hypothesis, we developed a computational model of bilateral hand use in arm reaching to study the interactions between adaptive decision making and motor relearning after motor cortex lesion. The model contains a left and a right motor cortex, each controlling the opposite arm, and a single action choice module. The action choice module learns, via reinforcement learning, the value of using each arm for reaching in specific directions. Each motor cortex uses a neural population code to specify the initial direction along which the contralateral hand moves towards a target. The motor cortex learns to minimize directional errors and to maximize neuronal activity for each movement. The derived learning rule accounts for the reversal of the loss of cortical representation after rehabilitation and the increase of this loss after stroke with insufficient rehabilitation. Further, our model exhibits nonlinear and bistable behavior: if natural recovery, motor training, or both, brings performance above a certain threshold, then training can be stopped, as the repeated spontaneous arm use provides a form of motor learning that further bootstraps performance and spontaneous use. Below this threshold, motor training is “in vain”: there is little spontaneous arm use after training, the model exhibits learned nonuse, and compensatory movements with the less affected hand are reinforced. By exploring the nonlinear dynamics of stroke recovery using a biologically plausible neural model that accounts for reversal of the loss of motor cortex representation following rehabilitation or the lack thereof, respectively, we can explain previously hard to reconcile data on spontaneous arm use in stroke recovery. Further, our threshold prediction could be tested with an adaptive train–wait–train paradigm: if spontaneous arm use has increased in the “wait” period, then the threshold has been reached, and rehabilitation can be stopped. If spontaneous arm use is still low or has decreased, then another bout of rehabilitation is to be provided.

Humans Can Adopt Optimal Discounting Strategy under Real-Time Constraints

Critical to our many daily choices between larger delayed rewards, and smaller more immediate rewards, are the shape and the steepness of the function that discounts rewards with time. Although research in artificial intelligence favors exponential discounting in uncertain environments, studies with humans and animals have consistently shown hyperbolic discounting. We investigated how humans perform in a reward decision task with temporal constraints, in which each choice affects the time remaining for later trials, and in which the delays vary at each trial. We demonstrated that most of our subjects adopted exponential discounting in this experiment. Further, we confirmed analytically that exponential discounting, with a decay rate comparable to that used by our subjects, maximized the total reward gain in our task. Our results suggest that the particular shape and steepness of temporal discounting is determined by the task that the subject is facing, and question the notion of hyperbolic reward discounting as a universal principle.

A functional threshold for long-term use of hand and arm function can be determined: predictions from a computational model and supporting data from the Extremity Constraint-Induced Therapy Evaluation (EXCITE) Trial.

Background Although spontaneous use of the more-affected arm and hand after stroke is an important determinant of participation and quality of life, a number of patients exhibit decreases in use following rehabilitative therapy. A previous neurocomputational model predicted that if the dose of therapy is sufficient to bring performance above a certain threshold, training can be stopped. Objective The aim of this study was to test the hypothesis that there exists a threshold for function of the paretic arm and hand after therapy. If function is above this threshold, spontaneous use will increase in the months following therapy. In contrast, if function is below this threshold, spontaneous use will decrease. Methods New computer simulations are presented showing that changes in arm use following therapy depend on a performance threshold. This prediction was tested by reanalyzing the data from the Extremity Constraint-Induced Therapy Evaluation (EXCITE) trial, a phase III randomized controlled trial in which participants received constraint-induced movement therapy for 2 weeks and were tested both 1 week and 1 year after therapy. Results The results demonstrate that arm and hand function measured immediately after therapy predicts, on average, the long-term change of arm use. Above a functional threshold, use improves. Below this threshold, use decreases. Limitations The reanalysis of the EXCITE trial data provides a “group” threshold above which a majority of patients, but not all, improve spontaneously. A goal of future research is to provide the means to assess when patients reach their individual threshold. Conclusion Understanding of the causal and nonlinear relationship between limb function and daily use is important for the future development of cost-effective interventions and prevention of “rehabilitation in vain.”

Quantifying Arm Nonuse in Individuals Poststroke

Background. Arm nonuse, defined as the difference between what the individual can do when constrained to use the paretic arm and what the individual does when given a free choice to use either arm, has not yet been quantified in individuals poststroke. Objectives. (1) To quantify nonuse poststroke and (2) to develop and test a novel, simple, objective, reliable, and valid instrument, the Bilateral Arm Reaching Test (BART), to quantify arm use and nonuse poststroke. Methods. First, we quantify nonuse with the Quality of Movement (QOM) subscale of the Actual Amount of Use Test (AAUT) by subtracting the AAUT QOM score in the spontaneous use condition from the AAUT QOM score in a subsequent constrained use condition. Second, we quantify arm use and nonuse with BART by comparing reaching performance to visual targets projected over a 2D horizontal hemi–work space in a spontaneous-use condition (in which participants are free to use either arm at each trial) with reaching performance in a constrained-use condition. Results. All participants (N = 24) with chronic stroke and with mild to moderate impairment exhibited nonuse with the AAUT QOM. Nonuse with BART had excellent test-retest reliability and good external validity. Conclusions. BART is the first instrument that can be used repeatedly and practically in the clinic to quantify the effects of neurorehabilitation on arm use and nonuse and in the laboratory for advancing theoretical knowledge about the recovery of arm use and the development of nonuse and “learned nonuse” after stroke.

Use It and Improve It or Lose It: Interactions between Arm Function and Use in Humans Post-stroke

“Use it and improve it, or lose it” is one of the axioms of motor therapy after stroke. There is, however, little understanding of the interactions between arm function and use in humans post-stroke. Here, we explored putative non-linear interactions between upper extremity function and use by developing a first-order dynamical model of stroke recovery with longitudinal data from participants receiving constraint induced movement therapy (CIMT) in the EXCITE clinical trial. Using a Bayesian regression framework, we systematically compared this model with competitive models that included, or not, interactions between function and use. Model comparisons showed that the model with the predicted interactions between arm function and use was the best fitting model. Furthermore, by comparing the model parameters before and after CIMT intervention in participants receiving the intervention one year after randomization, we found that therapy increased the parameter that controls the effect of arm function on arm use. Increase in this parameter, which can be thought of as the confidence to use the arm for a given level of function, lead to increase in spontaneous use after therapy compared to before therapy.

Measuring Habitual Arm Use Post-stroke With a Bilateral Time-Constrained Reaching Task

Background: Spontaneous use of the more-affected arm is a meaningful indicator of stroke recovery. The Bilateral Arm Reaching Test (BART) was previously developed to quantify arm use by measuring arm choice to targets projected over a horizontal hemi-workspace. In order to improve clinical validity, we constrained the available movement time, thereby promoting more spontaneous decision making when selecting between the more-affected and less affected arm during the BART. Methods: Twenty-two individuals with mild to moderate hemiparesis were tested with the time-based BART in three time-constraint conditions: no-time constraint, medium, and fast conditions. Arm use was measured across three sessions with a 2-week interval in a spontaneous choice block, in which participants were instructed to use either the more-affected or the less-affected arm to reach targets. We tested the effect of time-constraint condition on the more-affected arm use, external validity of the BART with the Actual Amount of Use Test (AAUT), and test-retest reliability across the three test sessions. Results: The fast condition in the time-based BART showed reduced use of the more-affected arm compared to the no-time constraint condition P < 0.0001) and the medium condition P = 0.0006; Tukey post hoc analysis after mixed-effect linear regression). In addition, the fast condition showed strong correlation with the AAUT r = 0.829, P < 0.001), and excellent test-retest reliability (ICC = 0.960, P < 0.0001). Conclusion: The revised BART with a time-restricted fast condition provides an objective, accurate, and repeatable measure of spontaneous arm use in individuals with chronic stroke hemiparesis.

A functional threshold for long-term use of hand and arm function can be determined: Predictions from a computational model and supporting data from the extremity constraint-induced therapy evaluation (EXCITE) trial

After the critical period, plasticity in visual cortex is reduced and stability becomes dominant. In people with healthy visual systems, large-scale features of neural circuits – such as the white matter projection zones do not change significantly after the critical period. However, there is still uncertainty about neural circuit reorganization in disease conditions. An important question is whether primary visual cortex (V1) reorganizes due to re-activated plasticity if the retina is damaged after the critical period. Some fMRI studies reported large-scale reorganization in human macular degeneration (MD) patients whereas others did not. We investigated regions of human V1 deprived of input by a retinal lesion (lesion projection zone, or LPZ) in subjects with MD and retinitis pigmentosa. BOLD responses in the V1 LPZ can be elicited by task demands even in regions deprived of feed-forward input. In experiments analyzing these responses, we find that the population receptive field (pRF) sizes of these task-dependent LPZ responses are unusually large compared with the pRF sizes in healthy V1. Our hypothesis is that task-dependent BOLD responses in the LPZ of subjects with retinal dysfunction arise because (a) in the healthy brain there are signals from the LGN to V1 that gate the entry of extrastriate signals, and (b) these gating signals are eliminated by the retinal disease. This model explains response differences between controls and subjects with retinal dysfunction by the loss of the feed-forward gating signal caused by the disease; the model does not appeal to a large-scale cortical reorganization. We speculate on the implications of this hypothesis for visual therapy designed to replace the missing V1 LPZ inputs and restore vision.