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ABSTRACT: Optimization models explain many aspects of biological goal-directed movements. However, most such models use a finite-horizon formulation, which requires a prefixed movement duration to define a cost function and solve the optimization problem. To predict movement duration, these models have to be run multiple times with different prefixed durations until an appropriate duration is found by trial and error. The constrained minimum time model directly predicts movement duration; however, it does not consider sensory feedback and is thus applicable only to open-loop movements. To address these problems, we analyzed and simulated an infinite-horizon optimal feedback control model, with linear plants, that contains both control-dependent and control-independent noise and optimizes steady-state accuracy and energetic costs per unit time. The model applies the steady-state estimator and controller continuously to guide an effector to, and keep it at, target position. As such, it integrates movement control and posture maintenance without artificially dividing them with a precise, prefixed time boundary. Movement pace is determined by the model parameters, and the duration is an emergent property with trial-to-trial variability. By considering the mean duration, we derived both the log and power forms of Fitts's law as different approximations of the model. Moreover, the model reproduces typically observed velocity profiles and occasional transient overshoots. For unbiased sensory feedback, the effector reaches the target without bias, in contrast to finite-horizon models that systematically undershoot target when energetic cost is considered. Finally, the model does not involve backward and forward sweeps in time, its stability is easily checked, and the same solution applies to movements of different initial conditions and distances. We argue that biological systems could use steady-state solutions as default control mechanisms and might seek additional optimization of transient costs when justified or demanded by task or context.
Neural Computation 12/2012; · 1.88 Impact Factor
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ABSTRACT: 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.
Journal of Neuroscience 10/2012; 32(42):14617-21. · 7.11 Impact Factor
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Tomoko Kitago,
Johnny Liang,
Vincent S Huang,
Sheila Hayes,
Phyllis Simon,
Laura Tenteromano,
Ronald M Lazar,
Randolph S Marshall, Pietro Mazzoni,
Laura Lennihan,
John W Krakauer
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ABSTRACT: 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.
Neurorehabilitation and neural repair 07/2012; · 4.49 Impact Factor
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ABSTRACT: The public pays large sums of money to watch skilled motor performance. Notably, however, in recent decades motor skill learning (performance improvement beyond baseline levels) has received less experimental attention than motor adaptation (return to baseline performance in the setting of an external perturbation). Motor skill can be assessed at the levels of task success and movement quality, but the link between these levels remains poorly understood. We devised a motor skill task that required visually guided curved movements of the wrist without a perturbation, and we defined skill learning at the task level as a change in the speed-accuracy trade-off function (SAF). Practice in restricted speed ranges led to a global shift of the SAF. We asked how the SAF shift maps onto changes in trajectory kinematics, to establish a link between task-level performance and fine motor control. Although there were small changes in mean trajectory, improved performance largely consisted of reduction in trial-to-trial variability and increase in movement smoothness. We found evidence for improved feedback control, which could explain the reduction in variability but does not preclude other explanations such as an increased signal-to-noise ratio in cortical representations. Interestingly, submovement structure remained learning invariant. The global generalization of the SAF across a wide range of difficulty suggests that skill for this task is represented in a temporally scalable network. We propose that motor skill acquisition can be characterized as a slow reduction in movement variability, which is distinct from faster model-based learning that reduces systematic error in adaptation paradigms.
Journal of Neurophysiology 04/2012; 108(2):578-94. · 3.32 Impact Factor
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Movement Disorders 11/2011; 26(13):2325-6. · 4.51 Impact Factor
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Movement Disorders 09/2011; 27(2):328-9. · 4.51 Impact Factor
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ABSTRACT: Recent studies of upper limb movements have provided insights into the computations, mechanisms, and taxonomy of human sensorimotor learning. Motor tasks differ with respect to how they weight different learning processes. These include adaptation, an internal-model based process that reduces sensory-prediction errors in order to return performance to pre-perturbation levels, use-dependent plasticity, and operant reinforcement. Visuomotor rotation and force-field tasks impose systematic errors and thereby emphasize adaptation. In skill learning tasks, which for the most part do not involve a perturbation, improved performance is manifest as reduced motor variability and probably depends less on adaptation and more on success-based exploration. Explicit awareness and declarative memory contribute, to varying degrees, to motor learning. The modularity of motor learning processes maps, at least to some extent, onto distinct brain structures.
Current opinion in neurobiology 07/2011; 21(4):636-44. · 7.21 Impact Factor
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ABSTRACT: Although motor learning is likely to involve multiple processes, phenomena observed in error-based motor learning paradigms tend to be conceptualized in terms of only a single process: adaptation, which occurs through updating an internal model. Here we argue that fundamental phenomena like movement direction biases, savings (faster relearning), and interference do not relate to adaptation but instead are attributable to two additional learning processes that can be characterized as model-free: use-dependent plasticity and operant reinforcement. Although usually "hidden" behind adaptation, we demonstrate, with modified visuomotor rotation paradigms, that these distinct model-based and model-free processes combine to learn an error-based motor task. (1) Adaptation of an internal model channels movements toward successful error reduction in visual space. (2) Repetition of the newly adapted movement induces directional biases toward the repeated movement. (3) Operant reinforcement through association of the adapted movement with successful error reduction is responsible for savings.
Neuron 05/2011; 70(4):787-801. · 14.74 Impact Factor
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ABSTRACT: The purpose of this study was to examine longitudinal change in gait and motor function in pre-manifest Huntington's disease (HD).We examined ten pre-manifest subjects at baseline, one and five years. Quantitative gait data were collected with an electronic mat (GAITRite®). We analyzed measures related to speed (velocity, step length, cadence), asymmetry (step length difference), dynamic balance (percent time in double support, support base) and variability in stride length and swing time. Motor function was assessed with the motor component of the Unified Huntington's Disease Rating Scale.Gait velocity decreased (p=0.001), whereas step length difference (p=0.006), stride length variability (p=0.0001) and swing time variability increased (p=0.0001) from baseline to year five. Step length difference (p<0.05) and swing time variability (p<0.05) increased marginally in one year from baseline. UHDRS Total motor score increased over five years (p=0.003), though the increase in one year was not significant (p=0.053). Of the individual motor domain scores (eye, hand movements, gait and balance, chorea) only dystonia worsened over five years (p=0.02). Total motor score (r2= 0.49, p<0.001) and swing time variability (r2= 0.22, p<0.009) were correlated with estimated years to diagnosis.Our results present the longest longitudinal follow up of gait in pre-manifest HD thus far. Despite the small sample size, quantitative gait analysis was able to detect changes in gait speed, symmetry and variability. Swing time variability was particularly important because it increased in one year from baseline and was correlated with estimated time to diagnosis. Our results highlight the importance of predictive outcomes such as gait variability using quantitative analysis.
PLoS currents. 01/2011; 3:RRN1268.
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Movement Disorders 03/2010; 25(4):514-6. · 4.51 Impact Factor
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ABSTRACT: When a new sensorimotor mapping is learned through practice, learning commonly transfers to unpracticed regions of task space, that is, generalization ensues. Does generalization reflect fixed properties of movement representations in the nervous system and thereby limit what visuomotor mappings can and cannot be learned? Or does what needs to be learned determine the shape of generalization? We used the broad generalization properties of visuomotor gain adaptation to address these questions. Adaptation to a single gain for reaching movements is known to generalize broadly across movement directions. By training subjects on two different gains in two directions, we set up a potential conflict between generalization patterns: if generalization of gain adaptation indicates fixed properties of movement amplitude encoding, then learning two different gains in different directions should not be possible. Conversely, if generalization is flexible, then it should be possible to learn two gains. We found that subjects were able to learn two gains simultaneously, although more slowly than when they adapted to a single gain. Analysis of the resulting double-gain generalization patterns, however, unexpectedly revealed that generalization around each training direction did not arise de novo, but could be explained by a weighted combination of single-gain generalization patterns, in which the weighting takes into account the relative angular separation between training directions. Our findings therefore demonstrate that the mappings to each training target can be fully learned through reweighting of single-gain generalization patterns and not through a categorical alteration of these functions. These results are consistent with a modular decomposition approach to visuomotor adaptation, in which a complex mapping results from a combination of simpler mappings in a "mixture-of-experts" architecture.
Journal of Neurophysiology 03/2010; 103(6):2938-52. · 3.32 Impact Factor
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ABSTRACT: Human movement can be guided automatically (implicit control) or attentively (explicit control). Explicit control may be engaged when learning a new movement, while implicit control enables simultaneous execution of multiple actions. Explicit and implicit control can often be assigned arbitrarily: we can simultaneously drive a car and tune the radio, seamlessly allocating implicit or explicit control to either action. This flexibility suggests that sensorimotor signals, including those that encode spatially overlapping perception and behavior, can be accurately segregated to explicit and implicit control processes.
We tested human subjects' ability to segregate sensorimotor signals to parallel control processes by requiring dual (explicit and implicit) control of the same reaching movement and testing for interference between these processes. Healthy control subjects were able to engage dual explicit and implicit motor control without degradation of performance compared to explicit or implicit control alone. We then asked whether segregation of explicit and implicit motor control can be selectively disrupted by studying dual-control performance in subjects with no clinically manifest neurologic deficits in the presymptomatic stage of Huntington's disease (HD). These subjects performed successfully under either explicit or implicit control alone, but were impaired in the dual-control condition.
The human nervous system can exert dual control on a single action, and is therefore able to accurately segregate sensorimotor signals to explicit and implicit control. The impairment observed in the presymptomatic stage of HD points to a possible crucial contribution of the striatum to the segregation of sensorimotor signals to multiple control processes.
PLoS ONE 01/2009; 4(10):e7557. · 4.09 Impact Factor
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ABSTRACT: Adaptation of the motor system to sensorimotor perturbations is a type of learning relevant for tool use and coping with an ever-changing body. Memory for motor adaptation can take the form of savings: an increase in the apparent rate constant of readaptation compared with that of initial adaptation. The assessment of savings is simplified if the sensory errors a subject experiences at the beginning of initial adaptation and the beginning of readaptation are the same. This can be accomplished by introducing either 1) a sufficiently small number of counterperturbation trials (counterperturbation paradigm [CP]) or 2) a sufficiently large number of zero-perturbation trials (washout paradigm [WO]) between initial adaptation and readaptation. A two-rate, linear time-invariant state-space model (SSM(LTI,2)) was recently shown to theoretically produce savings for CP. However, we reasoned from superposition that this model would be unable to explain savings for WO. Using the same task (planar reaching) and type of perturbation (visuomotor rotation), we found comparable savings for both CP and WO paradigms. Although SSM(LTI,2) explained some degree of savings for CP it failed completely for WO. We conclude that for visuomotor rotation, savings in general is not simply a consequence of LTI dynamics. Instead savings for visuomotor rotation involves metalearning, which we show can be modeled as changes in system parameters across the phases of an adaptation experiment.
Journal of Neurophysiology 08/2008; 100(5):2537-48. · 3.32 Impact Factor
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ABSTRACT: People generally select a similar speed for a given motor task, such as reaching for a cup. One well established determinant of movement time is the speed-accuracy trade-off: movement time increases with the accuracy requirement. A second possible determinant is the energetic cost of making a movement. Parkinson's disease (PD), a condition characterized by generalized movement slowing (bradykinesia), provides the opportunity to directly explore this second possibility. We compared reaching movements of patients with PD with those of control subjects in a speed-accuracy trade-off task comprising conditions of increasing difficulty. Subjects completed as many trials as necessary to make 20 movements within a required speed range (trials to criterion, N(c)). Difficulty was reflected in endpoint accuracy and N(c). Patients were as accurate as control subjects in all conditions (i.e., PD did not affect the speed-accuracy trade-off). However, N(c) was consistently higher in patients, indicating reluctance to move fast although accuracy was not compromised. Specifically, the dependence of N(c) on movement energy cost (slope S(N)) was steeper in patients than in control subjects. This difference in S(N) suggests that bradykinesia represents an implicit decision not to move fast because of a shift in the cost/benefit ratio of the energy expenditure needed to move at normal speed. S(N) was less steep, but statistically significant, in control subjects, which demonstrates a role for energetic cost in the normal control of movement speed. We propose that, analogous to the established role of dopamine in explicit reward-seeking behavior, the dopaminergic projection to the striatum provides a signal for implicit "motor motivation."
Journal of Neuroscience 08/2007; 27(27):7105-16. · 7.11 Impact Factor
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ABSTRACT: It has been shown that motion aftereffect (MAE) not only is present at the adapted location but also partially transfers to nearby non-adapted locations. However, it is not clear whether MAE transfers across the fixation point. Since cells in area MSTd have receptive fields that cover both sides of the fixation point and since many MSTd cells, but not cells in earlier visual areas, prefer complex motion patterns such as expansion, we tested cross-fixation transfer of MAE induced by expanding random-dots stimuli. We also used rightward translational motion for comparison. Subjects adapted to motion patterns on a fixed side of the fixation point. Dynamic MAE was then measured with a nulling procedure at both the adapted site and the mirror site across the fixation point. Subjects' eye fixation during stimulus presentation was monitored with an infrared eye tracker. At the adapted site, both the expansion and the translation patterns generated strong MAEs, as expected. However, only the expansion pattern, but not translation pattern, generated significant MAE at the mirror site. This remained true even after we adjusted stimulus parameters to equate the strengths of the expansion MAE and translation MAE at the adapted site. We conclude that there is cross-fixation transfer of MAE for expansion motion but not for translational motion.
Vision Research 11/2006; 46(21):3681-9. · 2.41 Impact Factor
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ABSTRACT: Generalization of motor learning refers to our ability to apply what has been learned in one context to other contexts. When generalization is beneficial, it is termed transfer, and when it is detrimental, it is termed interference. Insight into the mechanism of generalization may be acquired from understanding why training transfers in some contexts but not others. However, identifying relevant contextual cues has proven surprisingly difficult, perhaps because the search has mainly been for cues that are explicit. We hypothesized instead that a relevant contextual cue is an implicit memory of action with a particular body part. To test this hypothesis we considered a task in which participants learned to control motion of a cursor under visuomotor rotation in two contexts: by moving their hand through motion of their shoulder and elbow, or through motion of their wrist. Use of these contextual cues led to three observations: First, in naive participants, learning in the wrist context was much faster than in the arm context. Second, generalization was asymmetric so that arm training benefited subsequent wrist training, but not vice versa. Third, in people who had prior wrist training, generalization from the arm to the wrist was blocked. That is, prior wrist training appeared to prevent both the interference and transfer that subsequent arm training should have caused. To explain the data, we posited that the learner collected statistics of contextual history: all upper arm movements also move the hand, but occasionally we move our hands without moving the upper arm. In a Bayesian framework, history of limb segment use strongly affects parameter uncertainty, which is a measure of the covariance of the contextual cues. This simple Bayesian prior dictated a generalization pattern that largely reproduced all three findings. For motor learning, generalization depends on context, which is determined by the statistics of how we have previously used the various parts of our limbs.
PLoS Biology 11/2006; 4(10):e316. · 11.45 Impact Factor
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ABSTRACT: The relationship between implicit and explicit processes during motor learning, and for visuomotor adaptation in particular, is poorly understood. We set up a conflict between implicit and explicit processes by instructing subjects to counter a visuomotor rotation using a cognitive strategy in a pointing task. Specifically, they were told the exact nature of the directional perturbation, a rotation that directed them 45 degrees counterclockwise from the desired target, and they were instructed to counter it by aiming for the neighboring clockwise target, 45 degrees away. Subjects were initially successful in completely negating the rotation with this strategy. Surprisingly, however, they were unable to sustain explicit control and made increasingly large errors to the desired target. The cognitive strategy failed because subjects simultaneously adapted unconsciously to the rotation to the neighboring target. Notably, the rate of implicit adaptation to the neighboring target was not significantly different from rotation adaptation in the absence of an opposing explicit strategy. These results indicate that explicit strategies cannot substitute for implicit adaptation to a visuomotor rotation and are in fact overridden by the motor planning system. This suggests that the motor system requires that planned and executed trajectories remain congruous in visual space, and enforces this correspondence even at the expense of an opposing explicit task goal.
Journal of Neuroscience 05/2006; 26(14):3642-5. · 7.11 Impact Factor
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Science 02/2004; 303(5656):317-8. · 31.20 Impact Factor
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ABSTRACT: In this case study, we describe the symptoms, neurological exam, neuropsychological test results, and brain pathology of a man who died with Huntington's disease (HD). HD is a rare neurodegenerative disease. Like other movement disorders involving the basal ganglia, HD affects motor, cognitive, and psychiatric functioning. The disease follows an autosomal dominant pattern of inheritance, with onset of symptoms most commonly occurring in the late 30s or early 40s, as in this patient. HD is caused by an unstable expansion of the trinucleotide CAG, coding for glutamine, on chromosome 4. Despite knowledge of the gene mutation responsible for HD, no definitive treatment is currently available to slow or halt progression of the disease. However, symptomatic treatment can significantly improve the quality of life for patients with HD.
Science of Aging Knowledge Environment 11/2003; 2003(43):dn3.
