Limb motion dictates how motor learning arises from arbitrary environmental dynamics

A key idea in motor learning is that internal models of environmental dynamics are internally represented as functions of spatial variables including position, velocity, and acceleration of body motion. We refer to such a representation as motion dependent. The evidence for a motion-dependent representation is, however, primarily based on examination of the adaptation to motion-dependent dynamic environments. To more rigorously test this idea, we examined the adaptive response to perturbations that cannot be well approximated by motion-state: force-impulses--brief, high-amplitude pulses of force. The induced adaptation characterizes the impulse response of the system--a widely used technique for probing system dynamics in engineering systems identification. Here we examined the adaptive responses to two different force-impulse perturbations during human voluntary reaching movements. We found that although neither could be well approximated by motion-state (R(2) < 0.18 in both cases), both perturbations induced single-trial adaptive responses that were (R(2) > 0.87). Moreover, these responses were similar in shape to those induced by low-fidelity motion-based approximations of the force-impulses (r > 0.88). Remarkably, we found that the motion dependence of the adaptive responses to force-impulses persisted, even after prolonged exposure (R(2) > 0.95). During a 300-trial training period, trial-to-trial fluctuations in the position, velocity, and acceleration of motion accurately predicted trial-to-trial fluctuations in the adaptive response, and the adaptation gradually became more specific to the perturbation, but only via reorganization of the structure of the motion-dependent representation. These results indicate that internal models of environmental dynamics represent these dynamics in a motion-dependent manner, regardless of the nature of the dynamics encountered.