Person: Smith, Maurice
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Smith, Maurice
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Publication The Decay of Motor Memories Is Independent of Context Change Detection(Public Library of Science, 2015) Brennan, Andrew E.; Smith, MauriceWhen the error signals that guide human motor learning are withheld following training, recently-learned motor memories systematically regress toward untrained performance. It has previously been hypothesized that this regression results from an intrinsic volatility in these memories, resulting in an inevitable decay in the absence of ongoing error signals. However, a recently-proposed alternative posits that even recently-acquired motor memories are intrinsically stable, decaying only if a change in context is detected. This new theory, the context-dependent decay hypothesis, makes two key predictions: (1) after error signals are withheld, decay onset should be systematically delayed until the context change is detected; and (2) manipulations that impair detection by masking context changes should result in prolonged delays in decay onset and reduced decay amplitude at any given time. Here we examine the decay of motor adaptation following the learning of novel environmental dynamics in order to carefully evaluate this hypothesis. To account for potential issues in previous work that supported the context-dependent decay hypothesis, we measured decay using a balanced and baseline-referenced experimental design that allowed for direct comparisons between analogous masked and unmasked context changes. Using both an unbiased variant of the previous decay onset analysis and a novel highly-powered group-level version of this analysis, we found no evidence for systematically delayed decay onset nor for the masked context change affecting decay amplitude or its onset time. We further show how previous estimates of decay onset latency can be substantially biased in the presence of noise, and even more so with correlated noise, explaining the discrepancy between the previous results and our findings. Our results suggest that the decay of motor memories is an intrinsic feature of error-based learning that does not depend on context change detection.Publication The Binding of Learning to Action in Motor Adaptation(Public Library of Science, 2011) Gonzalez Castro, L. Nicolas; Monsen, Craig Bryant; Smith, MauriceIn motor tasks, errors between planned and actual movements generally result in adaptive changes which reduce the occurrence of similar errors in the future. It has commonly been assumed that the motor adaptation arising from an error occurring on a particular movement is specifically associated with the motion that was planned. Here we show that this is not the case. Instead, we demonstrate the binding of the adaptation arising from an error on a particular trial to the motion experienced on that same trial. The formation of this association means that future movements planned to resemble the motion experienced on a given trial benefit maximally from the adaptation arising from it. This reflects the idea that actual rather than planned motions are assigned 'credit' for motor errors because, in a computational sense, the maximal adaptive response would be associated with the condition credited with the error. We studied this process by examining the patterns of generalization associated with motor adaptation to novel dynamic environments during reaching arm movements in humans. We found that these patterns consistently matched those predicted by adaptation associated with the actual rather than the planned motion, with maximal generalization observed where actual motions were clustered. We followed up these findings by showing that a novel training procedure designed to leverage this newfound understanding of the binding of learning to action, can improve adaptation rates by greater than 50%. Our results provide a mechanistic framework for understanding the effects of partial assistance and error augmentation during neurologic rehabilitation, and they suggest ways to optimize their use.Publication Reduction in Learning Rates Associated with Anterograde Interference Results from Interactions between Different Timescales in Motor Adaptation(Public Library of Science, 2010) Sing, Gary Chin-Wei; Smith, MauricePrior experiences can influence future actions. These experiences can not only drive adaptive changes in motor output, but they can also modulate the rate at which these adaptive changes occur. Here we studied anterograde interference in motor adaptation – the ability of a previously learned motor task (Task A) to reduce the rate of subsequently learning a different (and usually opposite) motor task (Task B). We examined the formation of the motor system's capacity for anterograde interference in the adaptive control of human reaching-arm movements by determining the amount of interference after varying durations of exposure to Task A (13, 41, 112, 230, and 369 trials). We found that the amount of anterograde interference observed in the learning of Task B increased with the duration of Task A. However, this increase did not continue indefinitely; instead, the interference reached asymptote after 15–40 trials of Task A. Interestingly, we found that a recently proposed multi-rate model of motor adaptation, composed of two distinct but interacting adaptive processes, predicts several key features of the interference patterns we observed. Specifically, this computational model (without any free parameters) predicts the initial growth and leveling off of anterograde interference that we describe, as well as the asymptotic amount of interference that we observe experimentally (R2 = 0.91). Understanding the mechanisms underlying anterograde interference in motor adaptation may enable the development of improved training and rehabilitation paradigms that mitigate unwanted interference.Publication Adaptation and generalization in acceleration-dependent force fields(Springer Science + Business Media, 2005) Hwang, Eun Jung; Smith, Maurice; Shadmehr, RezaAny passive rigid inertial object that we hold in our hand, e.g., a tennis racquet, imposes a field of forces on the arm that depends on limb position, velocity, and acceleration. A fundamental characteristic of this field is that the forces due to acceleration and velocity are linearly separable in the intrinsic coordinates of the limb. In order to learn such dynamics with a collection of basis elements, a control system would generalize correctly and therefore perform optimally if the basis elements that were sensitive to limb velocity were not sensitive to acceleration, and vice versa. However, in the mammalian nervous system proprioceptive sensors like muscle spindles encode a nonlinear combination of all components of limb state, with sensitivity to velocity dominating sensitivity to acceleration. Therefore, limb state in the space of proprioception is not linearly separable despite the fact that this separation is a desirable property of control systems that form models of inertial objects. In building internal models of limb dynamics, does the brain use a representation that is optimal for control of inertial objects, or a representation that is closely tied to how peripheral sensors measure limb state? Here we show that in humans, patterns of generalization of reaching movements in acceleration-dependent fields are strongly inconsistent with basis elements that are optimized for control of inertial objects. Unlike a robot controller that models the dynamics of the natural world and represents velocity and acceleration independently, internal models of dynamics that people learn appear to be rooted in the properties of proprioception, nonlinearly responding to the pattern of muscle activation and representing velocity more strongly than acceleration.Publication Intact Ability to Learn Internal Models of Arm Dynamics in Huntington's Disease But Not Cerebellar Degeneration(American Physiological Society, 2005) Smith, Maurice; Shadmehr, RezaTwo different compensatory mechanisms are engaged when the nervous system senses errors during a reaching movement. First, on-line feedback control mechanisms produce in-flight corrections to reduce errors in the on-going movement. Second, these errors modify the internal model with which the motor plan is transformed into motor commands for the subsequent movements. What are the neural mechanisms of these compensatory systems? In a previous study, we reported that while on-line error correction was disturbed in patients with Huntington's disease (HD), it was largely intact in patients with cerebellar degeneration. Here we altered dynamics of reaching and studied the effect of error in one trial on the motor commands that initiated the subsequent trial. We observed that in patients with cerebellar degeneration, motor commands changed from trial-to-trial by an amount that was comparable to control subjects. However, these changes were random and were uninformed by the error in the preceding trial. In contrast, the change in motor commands of HD patients was strongly related to the error in the preceding trial. This error-dependent change had a sensitivity that was comparable to healthy controls. As a result, HD patients exhibited no significant deficits in adapting to novel arm dynamics, whereas cerebellar subjects were profoundly impaired. These results demonstrate a double dissociation between on-line and trial-to-trial error correction suggesting that these compensatory mechanisms have distinct neural bases that can be differentially affected by disease.Publication Long-Term Retention Explained by a Model of Short-Term Learning in the Adaptive Control of Reaching(American Physiological Society, 2008) Joiner, Wilsaan M.; Smith, MauriceExtensive theoretical, psychophysical, and neurobiological work has focused on the mechanisms by which short-term learning develops into long-term memory. Better understanding of these mechanisms may lead to the ability to improve the efficiency of training procedures. A key phenomenon in the formation of long-term memory is the effect of over learning on retention—discovered by Ebbinghaus in 1885: when the initial training period in a task is prolonged even beyond what is necessary for good immediate recall, long-term retention improves. Although this over learning effect has received considerable attention as a phenomenon in psychology research, the mechanisms governing this process are not well understood, and the ability to predict the benefit conveyed by varying degrees of over learning does not yet exist. Here we studied the relationship between the duration of an initial training period and the amount of retention 24 h later for the adaptation of human reaching arm movements to a novel force environment. We show that in this motor adaptation task, the amount of long-term retention is predicted not by the overall performance level achieved during the training period but rather by the level of a specific component process in a multi-rate model of short-term memory formation. These findings indicate that while multiple learning processes determine the ability to learn a motor adaptation, only one provides a gateway to long-term memory formation. Understanding the dynamics of this key learning process may allow for the rational design of training and rehabilitation paradigms that maximize the long-term benefit of each session.Publication Dissociable Effects of the Implicit and Explicit Memory Systems on Learning Control of Reaching(Springer Verlag, 2006) Hwang, Eun Jung; Smith, Maurice; Shadmehr, RezaAdaptive control of reaching depends on internal models that associate states in which the limb experienced a force perturbation with motor commands that can compensate for it. Limb state can be sensed via both vision and proprioception. However, adaptation of reaching in novel dynamics results in generalization in the intrinsic coordinates of the limb, suggesting that the proprioceptive states in which the limb was perturbed dominate representation of limb state. To test this hypothesis, we considered a task where position of the hand during a reach was correlated with patterns of force perturbation. This correlation could be sensed via vision, proprioception, or both. As predicted, when the correlations could be sensed only via proprioception, learning was significantly better as compared to when the correlations could only be sensed through vision. We found that learning with visual correlations resulted in subjects who could verbally describe the patterns of perturbations but this awareness was never observed in subjects who learned the task with only proprioceptive correlations. We manipulated the relative values of the visual and proprioceptive parameters and found that the probability of becoming aware strongly depended on the correlations that subjects could visually observe. In all conditions, aware subjects demonstrated a small but significant advantage in their ability to adapt their motor commands. Proprioceptive correlations produced an internal model that strongly influenced reaching performance yet did not lead to awareness. Visual correlations strongly increased the probability of becoming aware, yet had a much smaller but still significant effect on reaching performance. Therefore, practice resulted in acquisition of both implicit and explicit internal models.Publication Effects of Human Cerebellar Thalamus Disruption on Adaptive Control of Reaching(Oxford University Press, 2005) Chen, Haiyin; Hua, Sherwin E.; Smith, Maurice; Lenz, Frederick A.; Shadmehr, RezaLesion or degeneration of the cerebellum can profoundly impair adaptive control of reaching in humans. Computational models have proposed that internal models that help control movements form in the cerebellum and influence planned motor output through the cerebello-thalamo-cortical pathway. However, lesion studies of the cerebellar thalamus have not consistently found impairment in reaching or adaptation of reaching. To elucidate the role of the cerebellar thalamus in humans, we studied a group of essential tremor (ET) patients with deep brain stimulation (DBS) electrodes placed in the cerebellar thalamus. The stimulation can be turned on or off remotely and is thought to reduce tremor by blocking the spread of the pathological output from the cerebellum. We studied the effect of thalamic DBS on the ability to adapt arm movements to novel force fields. Although thalamic DBS resulted in a dramatic and significant reduction of tremor in ET, it also impaired motor adaptation: the larger the stimulation voltage, the greater the reduction in rates of adaptation. We next examined ET patients that had undergone unilateral thalamotomy in the cerebellar thalamus and found that adaptation with the contralateral arm was impaired compared with the ipsilateral arm. Therefore, although both lesion and electrical stimulation of the cerebellar thalamus are highly effective in reducing tremor, they significantly impair the ability of the brain to form internal models of action. Adaptive control of reaching appears to depend on the integrity of the cerebello-thalamo-cortical pathway.Publication A Gain-Field Encoding of Limb Position and Velocity in the Internal Model of Arm Dynamics(Public Library of Science (PLoS), 2003) Hwang, Eun Jung; Donchin, Opher; Smith, Maurice; Shadmehr, RezaAdaptability of reaching movements depends on a computation in the brain that transforms sensory cues, such as those that indicate the position and velocity of the arm, into motor commands. Theoretical consideration shows that the encoding properties of neural elements implementing this transformation dictate how errors should generalize from one limb position and velocity to another. To estimate how sensory cues are encoded by these neural elements, we designed experiments that quantified spatial generalization in environments where forces depended on both position and velocity of the limb. The patterns of error generalization suggest that the neural elements that compute the transformation encode limb position and velocity in intrinsic coordinates via a gain-field; i.e., the elements have directionally dependent tuning that is modulated monotonically with limb position. The gain-field encoding makes the counterintuitive prediction of hypergeneralization: there should be growing extrapolation beyond the trained workspace. Furthermore, nonmonotonic force patterns should be more difficult to learn than monotonic ones. We confirmed these predictions experimentally.Publication Motor Disorder in Huntington's Disease Begins as a Dysfunction in Error Feedback Control(Nature Publishing Group, 2000) Smith, Maurice; Brandt, Jason; Shadmehr, RezaA steady progression of motor dysfunction takes place in Huntington's disease1 (HD). The origin of this disturbance with relation to the motor control process is not understood. Here we studied reaching movements in asymptomatic HD gene-carriers (AGCs) and subjects with manifest HD. We found that movement jerkiness, which characterizes the smoothness and efficiency of motion, was a sensitive indicator of presymptomatic HD progression. A large fraction of AGCs displayed elevated jerk even when more than seven years remained until predicted disease onset. Movement termination was disturbed much more than initiation and was highly variable from trial to trial. Analysis of this variability revealed that the sensitivity of end-movement jerk to subtle, self-generated early-movement errors was greater in HD subjects than in controls. Additionally, we found that HD corrective responses to externally-generated force pulses were greatly disturbed, indicating that HD subjects display aberrant responses to both external and self-generated errors. Because feedback corrections are driven by error and are delayed such that they predominantly affect movement termination, these findings suggest that a dysfunction in error correction characterizes the motor control deficit in early HD. This dysfunction may be observed years before clinical disease onset and grows worse as the disease progresses.