Timescales of motor memory formation in dual-adaptation

Abstract

The timescales of adaptation to novel dynamics are well explained by a dual-rate model with slow and fast states. This model can predict interference, savings and spontaneous recovery, but cannot account for adaptation to multiple tasks, as each new task drives unlearning of the previously learned task. Nevertheless, in the presence of appropriate contextual cues, humans are able to adapt simultaneously to opposing dynamics. Consequently this model was expanded, suggesting that dual-adaptation occurs through a single fast process and multiple slow processes. However, such a model does not predict spontaneous recovery within dual-adaptation. Here we assess the existence of multiple fast processes by examining the presence of spontaneous recovery in two experimental variations of an adaptation-de-adaptation-error-clamp paradigm within dual-task adaptation in humans. In both experiments, evidence for spontaneous recovery towards the initially learned dynamics (A) was found in the error-clamp phase, invalidating the one-fast-two-slow dual-rate model. However, as adaptation is not only constrained to two timescales, we fit twelve multi-rate models to the experimental data. BIC model comparison again supported the existence of two fast processes, but extended the timescales to include a third rate: the ultraslow process. Even within our single day experiment, we found little evidence for decay of the learned memory over several hundred error-clamp trials. Overall, we show that dual-adaptation can be best explained by a two-fast-triple-rate model over the timescales of adaptation studied here. Longer term learning may require even slower timescales, explaining why we never forget how to ride a bicycle. Author SummaryRetaining motor skills is crucial to perform basic daily life tasks. However we still have limited understanding of the computational structure of these motor memories, an understanding that is critical for designing rehabilitation. Here we demonstrate that learning any task involves adaptation of independent fast, slow and ultraslow processes to build a motor memory. The selection of the appropriate motor memory is gated through a contextual cue. Together this work extends our understanding of the architecture of motor memories, by merging disparate computational theories to propose a new model.