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Biomedical subjects

Maurice A Smith

Publications and source records attributed to Maurice A Smith.

6 recordsLinked to original sources

Interacting adaptive processes with different timescales underlie short-term motor learning.

Multiple processes may contribute to motor skill acquisition, but it is thought that many of these processes require sleep or the passage of long periods of time ranging from several hours to many days or weeks. Here we demonstrate that within a timescale of minutes, two distinct fast-acting processes drive motor adaptation. One process responds weakly to error but retains information well, whereas the other responds strongly but has poor retention. This two-state learning system makes the surprising prediction of spontaneous recovery (or adaptation rebound) if error feedback is clamped at zero following an adaptation-extinction training episode. We used a novel paradigm to experimentally confirm this prediction in human motor learning of reaching, and we show that the interaction between the learning processes in this simple two-state system provides a unifying explanation for several different, apparently unrelated, phenomena in motor adaptation including savings, anterograde interference, spontaneous recovery, and rapid unlearning. Our results suggest that motor adaptation depends on at least two distinct neural systems that have different sensitivity to error and retain information at different rates.

Adaptation, Physiological↗

Dissociable effects of the implicit and explicit memory systems on learning control of reaching.

Adaptive 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.

Adaptation, Psychological↗

Effects of human cerebellar thalamus disruption on adaptive control of reaching.

Lesion 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.

Adaptation, Physiological↗

Adaptation and generalization in acceleration-dependent force fields.

Any 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.

Acceleration↗

Intact ability to learn internal models of arm dynamics in Huntington's disease but not cerebellar degeneration.

Two 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.

Adult↗

A gain-field encoding of limb position and velocity in the internal model of arm dynamics.

Adaptability 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.

Adult↗