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Memory for Semantically Related and Unrelated Declarative Information: The Benefit of Sleep, the Cost of Wake

Numerous studies have examined sleep's influence on a range of hippocampus-dependent declarative memory tasks, from text learning to spatial navigation. In this study, we examined the impact of sleep, wake, and time-of-day influences on the processing of declarative information with strong sema...

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Autores principales: Payne, Jessica D., Tucker, Matthew A., Ellenbogen, Jeffrey M., Wamsley, Erin J., Walker, Matthew P., Schacter, Daniel L., Stickgold, Robert
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Public Library of Science 2012
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC3310860/
https://www.ncbi.nlm.nih.gov/pubmed/22457736
http://dx.doi.org/10.1371/journal.pone.0033079
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author Payne, Jessica D.
Tucker, Matthew A.
Ellenbogen, Jeffrey M.
Wamsley, Erin J.
Walker, Matthew P.
Schacter, Daniel L.
Stickgold, Robert
author_facet Payne, Jessica D.
Tucker, Matthew A.
Ellenbogen, Jeffrey M.
Wamsley, Erin J.
Walker, Matthew P.
Schacter, Daniel L.
Stickgold, Robert
author_sort Payne, Jessica D.
collection PubMed
description Numerous studies have examined sleep's influence on a range of hippocampus-dependent declarative memory tasks, from text learning to spatial navigation. In this study, we examined the impact of sleep, wake, and time-of-day influences on the processing of declarative information with strong semantic links (semantically related word pairs) and information requiring the formation of novel associations (unrelated word pairs). Participants encoded a set of related or unrelated word pairs at either 9am or 9pm, and were then tested after an interval of 30 min, 12 hr, or 24 hr. The time of day at which subjects were trained had no effect on training performance or initial memory of either word pair type. At 12 hr retest, memory overall was superior following a night of sleep compared to a day of wakefulness. However, this performance difference was a result of a pronounced deterioration in memory for unrelated word pairs across wake; there was no sleep-wake difference for related word pairs. At 24 hr retest, with all subjects having received both a full night of sleep and a full day of wakefulness, we found that memory was superior when sleep occurred shortly after learning rather than following a full day of wakefulness. Lastly, we present evidence that the rate of deterioration across wakefulness was significantly diminished when a night of sleep preceded the wake period compared to when no sleep preceded wake, suggesting that sleep served to stabilize the memories against the deleterious effects of subsequent wakefulness. Overall, our results demonstrate that 1) the impact of 12 hr of waking interference on memory retention is strongly determined by word-pair type, 2) sleep is most beneficial to memory 24 hr later if it occurs shortly after learning, and 3) sleep does in fact stabilize declarative memories, diminishing the negative impact of subsequent wakefulness.
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spelling pubmed-33108602012-03-28 Memory for Semantically Related and Unrelated Declarative Information: The Benefit of Sleep, the Cost of Wake Payne, Jessica D. Tucker, Matthew A. Ellenbogen, Jeffrey M. Wamsley, Erin J. Walker, Matthew P. Schacter, Daniel L. Stickgold, Robert PLoS One Research Article Numerous studies have examined sleep's influence on a range of hippocampus-dependent declarative memory tasks, from text learning to spatial navigation. In this study, we examined the impact of sleep, wake, and time-of-day influences on the processing of declarative information with strong semantic links (semantically related word pairs) and information requiring the formation of novel associations (unrelated word pairs). Participants encoded a set of related or unrelated word pairs at either 9am or 9pm, and were then tested after an interval of 30 min, 12 hr, or 24 hr. The time of day at which subjects were trained had no effect on training performance or initial memory of either word pair type. At 12 hr retest, memory overall was superior following a night of sleep compared to a day of wakefulness. However, this performance difference was a result of a pronounced deterioration in memory for unrelated word pairs across wake; there was no sleep-wake difference for related word pairs. At 24 hr retest, with all subjects having received both a full night of sleep and a full day of wakefulness, we found that memory was superior when sleep occurred shortly after learning rather than following a full day of wakefulness. Lastly, we present evidence that the rate of deterioration across wakefulness was significantly diminished when a night of sleep preceded the wake period compared to when no sleep preceded wake, suggesting that sleep served to stabilize the memories against the deleterious effects of subsequent wakefulness. Overall, our results demonstrate that 1) the impact of 12 hr of waking interference on memory retention is strongly determined by word-pair type, 2) sleep is most beneficial to memory 24 hr later if it occurs shortly after learning, and 3) sleep does in fact stabilize declarative memories, diminishing the negative impact of subsequent wakefulness. Public Library of Science 2012-03-22 /pmc/articles/PMC3310860/ /pubmed/22457736 http://dx.doi.org/10.1371/journal.pone.0033079 Text en Payne et al. http://creativecommons.org/licenses/by/4.0/ This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are properly credited.
spellingShingle Research Article
Payne, Jessica D.
Tucker, Matthew A.
Ellenbogen, Jeffrey M.
Wamsley, Erin J.
Walker, Matthew P.
Schacter, Daniel L.
Stickgold, Robert
Memory for Semantically Related and Unrelated Declarative Information: The Benefit of Sleep, the Cost of Wake
title Memory for Semantically Related and Unrelated Declarative Information: The Benefit of Sleep, the Cost of Wake
title_full Memory for Semantically Related and Unrelated Declarative Information: The Benefit of Sleep, the Cost of Wake
title_fullStr Memory for Semantically Related and Unrelated Declarative Information: The Benefit of Sleep, the Cost of Wake
title_full_unstemmed Memory for Semantically Related and Unrelated Declarative Information: The Benefit of Sleep, the Cost of Wake
title_short Memory for Semantically Related and Unrelated Declarative Information: The Benefit of Sleep, the Cost of Wake
title_sort memory for semantically related and unrelated declarative information: the benefit of sleep, the cost of wake
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC3310860/
https://www.ncbi.nlm.nih.gov/pubmed/22457736
http://dx.doi.org/10.1371/journal.pone.0033079
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