Abstract
Traditional views of sensorimotor adaptation, or adaptation of movements to perturbed sensory feedback, emphasize the role of automatic, implicit correction of sensory prediction errors (differences between predicted and actual sensory outcomes). However, latent memories formed during sensorimotor adaptation, manifest as improved learning (i.e., savings), have recently been attributed to strategic corrections of task errors (failures to achieve task goals). To dissociate contributions of task errors and sensory prediction errors to latent sensorimotor memories, we perturbed target locations to remove or enforce task errors during learning and/or test. We show that prior learning to correct task errors alone, even in the absence of perturbation-induced sensory prediction errors, was sufficient for savings, even when tested in the absence of task errors. In contrast, a history of sensory prediction errors was neither sufficient nor obligatory for savings. Limiting movement preparation time further revealed that the latent memories that are driven by learning to correct task errors take at least two forms: a time-consuming but flexible component, and a rapidly expressible, inflexible component. The results provide strong support for the idea that failure to successfully achieve movement goals is the primary driver of motor memories that manifest as savings. In contrast to previous suggestions, such persistent memories are not exclusively mediated by time-consuming strategic processes, but also comprise a rapidly expressible but inflexible component. The distinct characteristics of these putative processes that contribute to persistent motor memories suggest dissociable underlying mechanisms, and imply that identification of the neural basis for adaptation and savings will require methods that allow such dissociations.
Footnotes
Conflict of interest statement: The authors declare no competing financial interests.
Significance Statement. Latent motor memories formed during sensorimotor adaptation manifest as improved re-learning when sensorimotor perturbations are re-encountered (i.e., savings). Conflicting theories suggest that savings is underpinned by different mechanisms: including a memory of successful actions; a memory of errors; or an aiming strategy to correct task errors. To elucidate this issue, we examined the necessary conditions for savings. We show that learning to correct task errors is sufficient for savings, even when tested in the absence of task errors. In contrast, a history of sensory prediction errors is neither sufficient nor obligatory for savings. Finally, we show that latent sensorimotor memories driven by task errors comprise at least two distinct components: a time-consuming, flexible component, and a rapidly expressible, inflexible component.
updated figures for increased clarity.