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

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...

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Autores principales: Hadjiosif, Alkis M., Morehead, J. Ryan, Smith, Maurice A.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Public Library of Science 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10138789/
https://www.ncbi.nlm.nih.gov/pubmed/37104303
http://dx.doi.org/10.1371/journal.pbio.3001799
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author Hadjiosif, Alkis M.
Morehead, J. Ryan
Smith, Maurice A.
author_facet Hadjiosif, Alkis M.
Morehead, J. Ryan
Smith, Maurice A.
author_sort Hadjiosif, Alkis M.
collection PubMed
description 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.
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spelling pubmed-101387892023-04-28 A double dissociation between savings and long-term memory in motor learning Hadjiosif, Alkis M. Morehead, J. Ryan Smith, Maurice A. PLoS Biol Research Article 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. Public Library of Science 2023-04-27 /pmc/articles/PMC10138789/ /pubmed/37104303 http://dx.doi.org/10.1371/journal.pbio.3001799 Text en © 2023 Hadjiosif et al https://creativecommons.org/licenses/by/4.0/This is an open access article distributed under the terms of the Creative Commons Attribution License (https://creativecommons.org/licenses/by/4.0/) , which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
spellingShingle Research Article
Hadjiosif, Alkis M.
Morehead, J. Ryan
Smith, Maurice A.
A double dissociation between savings and long-term memory in motor learning
title A double dissociation between savings and long-term memory in motor learning
title_full A double dissociation between savings and long-term memory in motor learning
title_fullStr A double dissociation between savings and long-term memory in motor learning
title_full_unstemmed A double dissociation between savings and long-term memory in motor learning
title_short A double dissociation between savings and long-term memory in motor learning
title_sort double dissociation between savings and long-term memory in motor learning
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10138789/
https://www.ncbi.nlm.nih.gov/pubmed/37104303
http://dx.doi.org/10.1371/journal.pbio.3001799
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