A double dissociation between savings and long-term memory in motor learning

• Published in: PLoS biology Vol. 21; no. 4; p. e3001799
• Main Authors: Hadjiosif, Alkis M, Morehead, J Ryan, Smith, Maurice A
• Format: Journal Article
• Language: English
• Published: United States Public Library of Science 27.04.2023; Public Library of Science (PLoS)
• Subjects: Biology and Life Sciences; Coexistence; Consolidation; Experiments; Learning curves; Long term memory; Memory; Memory Consolidation; Memory, Long-Term; Mental Recall; Motor skill learning; Observational learning; Paradigms; Physical Sciences; School environment; Social Sciences
• ISSN: 1545-7885; 1544-9173; 1545-7885
• DOI: 10.1371/journal.pbio.3001799

Memories are easier to relearn than learn from scratch. This advantage, known as savings, has been widely assumed to result from the reemergence of stable long-term memories. In fact, the presence of savings has often been used as a marker for whether a memory has been consolidated. However, recent findings have demonstrated that motor learning rates can be systematically controlled, providing a mechanistic alternative to the reemergence of a stable long-term memory. Moreover, recent work has reported conflicting results about whether implicit contributions to savings in motor learning are present, absent, or inverted, suggesting a limited understanding of the underlying mechanisms. To elucidate these mechanisms, we investigate the relationship between savings and long-term memory by experimentally dissecting the underlying memories based on short-term (60-s) temporal persistence. Components of motor memory that are temporally-persistent at 60 s might go on to contribute to stable, consolidated long-term memory, whereas temporally-volatile components that have already decayed away by 60 s cannot. Surprisingly, we find that temporally-volatile implicit learning leads to savings, whereas temporally-persistent learning does not, but that temporally-persistent learning leads to long-term memory at 24 h, whereas temporally-volatile learning does not. This double dissociation between the mechanisms for savings and long-term memory formation challenges widespread assumptions about the connection between savings and memory consolidation. Moreover, we find that temporally-persistent implicit learning not only fails to contribute to savings, but also that it produces an opposite, anti-savings effect, and that the interplay between this temporally-persistent anti-savings and temporally-volatile savings provides an explanation for several seemingly conflicting recent reports about whether implicit contributions to savings are present, absent, or inverted. Finally, the learning curves we observed for the acquisition of temporally-volatile and temporally-persistent implicit memories demonstrate the coexistence of implicit memories with distinct time courses, challenging the assertion that models of context-based learning and estimation should supplant models of adaptive processes with different learning rates. Together, these findings provide new insight into the mechanisms for savings and long-term memory formation.