The motor commands required to control voluntary movements under various environmental conditions may be formed by adaptively combining a fixed set of motor primitives. Since this motor output must contend with state-dependent physical dynamics during movement, these primitives are thought to depend on the position and velocity of motion. Using a recently developed "error-clamp" technique, we measured the fine temporal structure of changes in motor output during adaptation. Interestingly, these measurements reveal that motor primitives echo a key feature of the neural coding of limb motion-correlated tuning to position and velocity. We show that this correlated tuning explains why initial stages of motor learning are often rapid and stereotyped, whereas later stages are slower and stimulus specific. With our new understanding of these primitives, we design dynamic environments that are intrinsically the easiest or most difficult to learn, suggesting a theoretical basis for the rational design of improved procedures for motor training and rehabilitation.
Actions can be planned in either an intrinsic (body-based) reference frame or an extrinsic (world-based) frame, and understanding how the internal representations associated with these frames contribute to the learning of motor actions is a key issue in motor control. We studied the internal representation of this learning in human subjects by analyzing generalization patterns across an array of different movement directions and workspaces after training a visuomotor rotation in a single movement direction in one workspace. This provided a dense sampling of the generalization function across intrinsic and extrinsic reference frames, which allowed us to dissociate intrinsic and extrinsic representations and determine the manner in which they contributed to the motor memory for a trained action. A first experiment showed that the generalization pattern reflected a memory that was intermediate between intrinsic and extrinsic representations. A second experiment showed that this intermediate representation could not arise from separate intrinsic and extrinsic learning. Instead, we find that the representation of learning is based on a gain-field combination of local representations in intrinsic and extrinsic coordinates. This gain-field representation generalizes between actions by effectively computing similarity based on the (Mahalanobis) distance across intrinsic and extrinsic coordinates and is in line with neural recordings showing mixed intrinsic-extrinsic representations in motor and parietal cortices.
Brayanov JB, Smith MA. Bayesian and "anti-Bayesian" biases in sensory integration for action and perception in the size-weight illusion. J Neurophysiol 103: 1518 -1531, 2010. First published January 20, 2010 doi:10.1152/jn.00814.2009. Which is heavier: a pound of lead or a pound of feathers? This classic trick question belies a simple but surprising truth: when lifted, the pound of lead feels heavier-a phenomenon known as the size-weight illusion. To estimate the weight of an object, our CNS combines two imperfect sources of information: a prior expectation, based on the object's appearance, and direct sensory information from lifting it. Bayes' theorem (or Bayes' law) defines the statistically optimal way to combine multiple information sources for maximally accurate estimation. Here we asked whether the mechanisms for combining these information sources produce statistically optimal weight estimates for both perceptions and actions. We first studied the ability of subjects to hold one hand steady when the other removed an object from it, under conditions in which sensory information about the object's weight sometimes conflicted with prior expectations based on its size. Since the ability to steady the supporting hand depends on the generation of a motor command that accounts for lift timing and object weight, hand motion can be used to gauge biases in weight estimation by the motor system. We found that these motor system weight estimates reflected the integration of prior expectations with real-time proprioceptive information in a Bayesian, statistically optimal fashion that discounted unexpected sensory information. This produces a motor sizeweight illusion that consistently biases weight estimates toward prior expectations. In contrast, when subjects compared the weights of two objects, their perceptions defied Bayes' law, exaggerating the value of unexpected sensory information. This produces a perceptual size-weight illusion that biases weight perceptions away from prior expectations. We term this effect "anti-Bayesian" because the bias is opposite that seen in Bayesian integration. Our findings suggest that two fundamentally different strategies for the integration of prior expectations with sensory information coexist in the nervous system for weight estimation.
The way that a motor adaptation is trained, for example, the manner in which it is introduced or the duration of the training period, can influence its internal representation. However, recent studies examining the gradual versus abrupt introduction of a novel environment have produced conflicting results. Here we examined how these effects determine the effector specificity of motor adaptation during visually guided reaching. After adaptation to velocity-dependent dynamics in the right arm, we estimated the amount of adaptation transferred to the left arm, using error-clamp measurement trials to directly measure changes in learned dynamics. We found that a small but significant amount of generalization to the untrained arm occurs under three different training schedules: a short-duration (15 trials) abrupt presentation, a long-duration (160 trials) abrupt presentation, and a long-duration gradual presentation of the novel dynamic environment. Remarkably, we found essentially no difference between the amount of interlimb generalization when comparing these schedules, with 9-12% transfer of the trained adaptation for all three. However, the duration of training had a pronounced effect on the stability of the interlimb transfer: The transfer elicited from short-duration training decayed rapidly, whereas the transfer from both long-duration training schedules was considerably more persistent (<50% vs. >90% retention over the first 20 trials). These results indicate that the amount of interlimb transfer is similar for gradual versus abrupt training and that interlimb transfer of learned dynamics can occur after even a brief training period but longer training is required for an enduring effect.
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