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Two distinct ways to form long-term object recognition memory during sleep and wakefulness
Memory consolidation is promoted by sleep. However, there is also evidence for consolidation into long-term memory during wakefulness via processes that preferentially affect nonhippocampal representations. We compared, in rats, the effects of 2-h postencoding periods of sleep and wakefulness on the...
Autores principales: | , , , , , |
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Formato: | Online Artículo Texto |
Lenguaje: | English |
Publicado: |
National Academy of Sciences
2022
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Materias: | |
Acceso en línea: | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9407643/ https://www.ncbi.nlm.nih.gov/pubmed/35969775 http://dx.doi.org/10.1073/pnas.2203165119 |
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author | Sawangjit, Anuck Harkotte, Maximilian Oyanedel, Carlos N Niethard, Niels Born, Jan Inostroza, Marion |
author_facet | Sawangjit, Anuck Harkotte, Maximilian Oyanedel, Carlos N Niethard, Niels Born, Jan Inostroza, Marion |
author_sort | Sawangjit, Anuck |
collection | PubMed |
description | Memory consolidation is promoted by sleep. However, there is also evidence for consolidation into long-term memory during wakefulness via processes that preferentially affect nonhippocampal representations. We compared, in rats, the effects of 2-h postencoding periods of sleep and wakefulness on the formation of long-term memory for objects and their associated environmental contexts. We employed a novel-object recognition (NOR) task, using object exploration and exploratory rearing as behavioral indicators of these memories. Remote recall testing (after 1 wk) confirmed significant long-term NOR memory under both conditions, with NOR memory after sleep predicted by the occurrence of EEG spindle–slow oscillation coupling. Rats in the sleep group decreased their exploratory rearing at recall testing, revealing successful recall of the environmental context. By contrast, rats that stayed awake after encoding showed equally high levels of rearing upon remote testing as during encoding, indicating that context memory was lost. Disruption of hippocampal function during the postencoding interval (by muscimol administration) suppressed long-term NOR memory together with context memory formation when animals slept, but enhanced NOR memory when they were awake during this interval. Testing remote recall in a context different from that during encoding impaired NOR memory in the sleep condition, while exploratory rearing was increased. By contrast, NOR memory in the wake rats was preserved and actually superior to that after sleep. Our findings indicate two distinct modes of long-term memory formation: Sleep consolidation is hippocampus dependent and implicates event-context binding, whereas wake consolidation is impaired by hippocampal activation and strengthens context-independent representations. |
format | Online Article Text |
id | pubmed-9407643 |
institution | National Center for Biotechnology Information |
language | English |
publishDate | 2022 |
publisher | National Academy of Sciences |
record_format | MEDLINE/PubMed |
spelling | pubmed-94076432023-02-15 Two distinct ways to form long-term object recognition memory during sleep and wakefulness Sawangjit, Anuck Harkotte, Maximilian Oyanedel, Carlos N Niethard, Niels Born, Jan Inostroza, Marion Proc Natl Acad Sci U S A Social Sciences Memory consolidation is promoted by sleep. However, there is also evidence for consolidation into long-term memory during wakefulness via processes that preferentially affect nonhippocampal representations. We compared, in rats, the effects of 2-h postencoding periods of sleep and wakefulness on the formation of long-term memory for objects and their associated environmental contexts. We employed a novel-object recognition (NOR) task, using object exploration and exploratory rearing as behavioral indicators of these memories. Remote recall testing (after 1 wk) confirmed significant long-term NOR memory under both conditions, with NOR memory after sleep predicted by the occurrence of EEG spindle–slow oscillation coupling. Rats in the sleep group decreased their exploratory rearing at recall testing, revealing successful recall of the environmental context. By contrast, rats that stayed awake after encoding showed equally high levels of rearing upon remote testing as during encoding, indicating that context memory was lost. Disruption of hippocampal function during the postencoding interval (by muscimol administration) suppressed long-term NOR memory together with context memory formation when animals slept, but enhanced NOR memory when they were awake during this interval. Testing remote recall in a context different from that during encoding impaired NOR memory in the sleep condition, while exploratory rearing was increased. By contrast, NOR memory in the wake rats was preserved and actually superior to that after sleep. Our findings indicate two distinct modes of long-term memory formation: Sleep consolidation is hippocampus dependent and implicates event-context binding, whereas wake consolidation is impaired by hippocampal activation and strengthens context-independent representations. National Academy of Sciences 2022-08-15 2022-08-23 /pmc/articles/PMC9407643/ /pubmed/35969775 http://dx.doi.org/10.1073/pnas.2203165119 Text en Copyright © 2022 the Author(s). Published by PNAS. https://creativecommons.org/licenses/by-nc-nd/4.0/This article is distributed under Creative Commons Attribution-NonCommercial-NoDerivatives License 4.0 (CC BY-NC-ND) (https://creativecommons.org/licenses/by-nc-nd/4.0/) . |
spellingShingle | Social Sciences Sawangjit, Anuck Harkotte, Maximilian Oyanedel, Carlos N Niethard, Niels Born, Jan Inostroza, Marion Two distinct ways to form long-term object recognition memory during sleep and wakefulness |
title | Two distinct ways to form long-term object recognition memory during sleep and wakefulness |
title_full | Two distinct ways to form long-term object recognition memory during sleep and wakefulness |
title_fullStr | Two distinct ways to form long-term object recognition memory during sleep and wakefulness |
title_full_unstemmed | Two distinct ways to form long-term object recognition memory during sleep and wakefulness |
title_short | Two distinct ways to form long-term object recognition memory during sleep and wakefulness |
title_sort | two distinct ways to form long-term object recognition memory during sleep and wakefulness |
topic | Social Sciences |
url | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9407643/ https://www.ncbi.nlm.nih.gov/pubmed/35969775 http://dx.doi.org/10.1073/pnas.2203165119 |
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