Hierarchical Motor Adaptations Negotiate Failures During Force Field Learning

Author summaryHow do we improve actions after a movement failure? Although negotiating movement failures is obviously crucial, previous motor-control studies have predominantly examined human movement adaptations in the absence of failures, and it remains unclear how failures affect subsequent movement adaptations. Here we examined this issue by developing a novel force field adaptation task where the hand movement during an arm reaching is perturbed by novel forces that induce a large target error, that is a failure. Our experimental observation and computational modeling show that, in addition to the popular 'internal model learning' process of motor adaptations, humans also utilize a 'failure-negotiating' process, that enables them to quickly improve movements in the presence of failure, even at the expense of increased arm trajectory deflections, which are subsequently reduced gradually with training after the achievement of the task success. Our results suggest that a hierarchical interaction between these two processes is a key for humans to negotiate movement failures.Humans have the amazing ability to learn the dynamics of the body and environment to develop motor skills. Traditional motor studies using arm reaching paradigms have viewed this ability as the process of 'internal model adaptation'. However, the behaviors have not been fully explored in the case when reaches fail to attain the intended target. Here we examined human reaching under two force fields types; one that induces failures (i.e., target errors), and the other that does not. Our results show the presence of a distinct failure-driven adaptation process that enables quick task success after failures, and before completion of internal model adaptation, but that can result in persistent changes to the undisturbed trajectory. These behaviors can be explained by considering a hierarchical interaction between internal model adaptation and the failure-driven adaptation of reach direction. Our findings suggest that movement failure is negotiated using hierarchical motor adaptations by humans.