The decay of motor adaptation to novel movement dynamics reveals an asymmetry in the stability of motion state-dependent learning

Motor adaptation paradigms provide a quantitative method to study short-term modification of motor commands. Despite the growing understanding of the role motion states (e.g., velocity) play in this form of motor learning, there is little information on the relative stability of memories based on these movement characteristics, especially in comparison to the initial adaptation. Here, we trained subjects to make reaching movements perturbed by force patterns dependent upon either limb position or velocity. Following training, subjects were exposed to a series of error-clamp trials to measure the temporal characteristics of the feedforward motor output during the decay of learning. The compensatory force patterns were largely based on the perturbation kinematic (e.g., velocity), but also showed a small contribution from the other motion kinematic (e.g., position). However, the velocity contribution in response to the position-based perturbation decayed at a slower rate than the position contribution to velocity-based training, suggesting a difference in stability. Next, we modified a previous model of motor adaptation to reflect this difference and simulated the behavior for different learning goals. We were interested in the stability of learning when the perturbations were based on different combinations of limb position or velocity that subsequently resulted in biased amounts of motion-based learning. We trained additional subjects on these combined motion-state perturbations and confirmed the predictions of the model. Specifically, we show that (1) there is a significant separation between the observed gain-space trajectories for the learning and decay of adaptation and (2) for combined motion-state perturbations, the gain associated to changes in limb position decayed at a faster rate than the velocity-dependent gain, even when the position-dependent gain at the end of training was significantly greater. Collectively, these results suggest that the state-dependent adaptation associated with movement velocity is relatively more stable than that based on position.Author summary: Human motor adaptation of limb movement in response to force perturbations has been shown to be motion-state dependent. That is, the compensatory response to these disturbances is correlated and proportional to the temporal changes in the position, velocity, and acceleration during the motion. Despite a growing understanding of this adaptation process, there is little information on the relative stability of this learning when based on these different temporal features of movement. Here we modified a previous computational model of motor adaptation to predict the decay of the compensatory response associated to different motion states, specifically learning based on temporal variations in limb position and velocity. We confirmed the simulated behavior by examining the decay of the temporal force output after subjects were trained to compensate for movement disturbances based on different combinations and magnitudes of these two motion states. Both simulation and behavioral results show that velocity-based learning decays at a slower rate than position-based, even when learning is significantly biased towards the latter at the end of training. Collectively, these results suggest that motion-state learning based on movement velocity is more stable than that based on limb position.