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

• Published in: PLoS computational biology 2017-05, Vol.13 (5), p.e1005492-e1005492
• Main Authors: Hosseini, Eghbal A, Nguyen, Katrina P, Joiner, Wilsaan M
• Format: Article
• Language: English
• Subjects: Adaptation; Adaptation, Physiological - physiology; Asymmetry; Aversion learning; Behavior; Bioengineering; Biology and Life Sciences; Commands; Computational Biology; Computer simulation; Decay; Decay rate; Dynamic stability; Dynamics; Earth Sciences; Error analysis; Explicit knowledge; Female; Humans; Kinematics; Laboratories; Learning; Learning - physiology; Male; Mathematical models; Medicine and Health Sciences; Memory; Motion stability; Motor neurons; Motor skill learning; Motor task performance; Movement; Movement - physiology; Neural circuitry; Neurosciences; Perturbation methods; Physical Sciences; Physiological aspects; Psychomotor Performance - physiology; Research and Analysis Methods; Separation; Serial learning; Series (mathematics); Social Sciences; State-dependent learning; Task Performance and Analysis; Training; Trajectories; Velocity
• ISSN: 1553-7358; 1553-734X; 1553-7358
• DOI: 10.1371/journal.pcbi.1005492

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.