Interacting Adaptive Processes with Different Timescales Underlie Short-Term Motor Learning

TLDR

Multiple processes may contribute to motor skill acquisition, but many require sleep or long periods of time ranging from hours to weeks. This two‑state learning system predicts spontaneous recovery when error feedback is clamped at zero after an adaptation‑extinction episode. A novel reaching paradigm confirmed this prediction, showing that the interaction between the two fast‑acting processes explains savings, anterograde interference, spontaneous recovery, and rapid unlearning. Within minutes, two fast‑acting processes drive motor adaptation—one weakly error‑responsive but well‑retained, the other strongly error‑responsive but poorly retained—and their interaction indicates at least two distinct neural systems with differing error sensitivity and retention rates.

Abstract

Multiple processes may contribute to motor skill acquisition, but it is thought that many of these processes require sleep or the passage of long periods of time ranging from several hours to many days or weeks. Here we demonstrate that within a timescale of minutes, two distinct fast-acting processes drive motor adaptation. One process responds weakly to error but retains information well, whereas the other responds strongly but has poor retention. This two-state learning system makes the surprising prediction of spontaneous recovery (or adaptation rebound) if error feedback is clamped at zero following an adaptation-extinction training episode. We used a novel paradigm to experimentally confirm this prediction in human motor learning of reaching, and we show that the interaction between the learning processes in this simple two-state system provides a unifying explanation for several different, apparently unrelated, phenomena in motor adaptation including savings, anterograde interference, spontaneous recovery, and rapid unlearning. Our results suggest that motor adaptation depends on at least two distinct neural systems that have different sensitivity to error and retain information at different rates.