No abstract

Although motor learning is likely to involve multiple processes, phenomena observed in error-based motor learning paradigms tend to be conceptualized in terms of only a single process – adaptation, which occurs through updating an internal model. Here we argue that fundamental phenomena like movement direction biases, savings (faster relearning) and interference do not relate to adaptation but instead are attributable to two additional learning processes that can be characterized as model-free: use-dependent plasticity and operant reinforcement. Although usually “hidden” behind adaptation, we demonstrate, with modified visuomotor rotation paradigms, that these distinct model-based and model-free processes combine to learn an error-based motor task: (1) Adaptation of an internal model channels movements toward successful error reduction in visual space. (2) Repetition of the newly adapted movement induces directional biases towards the repeated movement. (3) Operant reinforcement through association of the adapted movement with successful error reduction is responsible for savings.

Following a change in the environment or motor apparatus, human subjects are able to rapidly compensate their movements to recover accurate performance. This ability to adapt is thought to be achieved through multiple, qualitatively distinct learning processes acting in parallel. It is unclear, however, what the relative contributions of these multiple processes are during learning. In particular, long-term memories in such paradigms have been extensively studied through the phenomenon of savings-faster adaptation to a given perturbation the second time it is experienced-but it is unclear which components of learning contribute to this effect. Here we show that distinct components of learning in an adaptation task can be dissociated based on the amount of preparation time they require. During adaptation, we occasionally forced subjects to generate movements at very low preparation times. Early in learning, subjects expressed only a limited amount of their prior learning in these trials, though performance improved gradually with further practice. Following washout, subjects exhibited a strong and persistent aftereffect in trials in which preparation time was limited. When subjects were exposed to the same perturbation twice in successive days, they adapted faster the second time. This savings effect was, however, not seen in movements generated at low preparation times. These results demonstrate that preparation time plays a critical role in the expression of some components of learning but not others. Savings is restricted to those components that require prolonged preparation to be expressed and might therefore reflect a declarative rather than procedural form of memory.

Initiating a movement in response to a visual stimulus takes significantly longer than might be expected on the basis of neural transmission delays, but it is unclear why. In a visually guided reaching task, we forced human participants to move at lower-than-normal reaction times to test whether normal reaction times are strictly necessary for accurate movement. We found that participants were, in fact, capable of moving accurately ϳ80 ms earlier than their reaction times would suggest. Reaction times thus include a seemingly unnecessary delay that accounts for approximately one-third of their duration. Close examination of participants' behavior in conventional reaction-time conditions revealed that they generated occasional, spontaneous errors in trials in which their reaction time was unusually short. The pattern of these errors could be well accounted for by a simple model in which the timing of movement initiation is independent of the timing of movement preparation. This independence provides an explanation for why reaction times are usually so sluggish: delaying the mean time of movement initiation relative to preparation reduces the risk that a movement will be initiated before it has been appropriately prepared. Our results suggest that preparation and initiation of movement are mechanistically independent and may have a distinct neural basis. The results also demonstrate that, even in strongly stimulus-driven tasks, presentation of a stimulus does not directly trigger a movement. Rather, the stimulus appears to trigger an internal decision whether to make a movement, reflecting a volitional rather than reactive mode of control.

The human motor system rapidly adapts to systematic perturbations but the adapted behavior seems to be forgotten equally rapidly. The reason for this forgetting is unclear, as is how to overcome it to promote long-term learning. Here we show that adapted behavior can be stabilized by a period of binary feedback about success and failure in the absence of vector error feedback. We examined the time course of decay after adaptation to a visuomotor rotation through a “visual error clamp” condition—trials in which subjects received false visual feedback showing perfect directional performance, regardless of the movements they actually made. Exposure to this error-clamp following initial visuomotor adaptation led to a rapid reversion to baseline behavior. In contrast, exposure to binary feedback after initial adaptation turned the adapted state into a new baseline, to which subjects reverted after transient exposure to another visuomotor rotation. When both binary feedback and vector error were present, some subjects exhibited rapid decay to the original baseline, while others persisted in the new baseline. We propose that learning can be decomposed into two components – a fast-learning, fast-forgetting adaptation process that is sensitive to vector errors and insensitive to task success, and a second process driven by success that learns more slowly but is less susceptible to forgetting. These two learning systems may be recruited to different degrees across individuals. Understanding this competitive balance and exploiting the long-term retention properties of learning through reinforcement is likely to be essential for successful neuro-rehabilitation.