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Occipital sleep spindles predict sequence learning in a visuo-motor task

STUDY OBJECTIVES: The brain appears to use internal models to successfully interact with its environment via active predictions of future events. Both internal models and the predictions derived from them are based on previous experience. However, it remains unclear how previously encoded informatio...

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Autores principales: Lutz, Nicolas D, Admard, Marie, Genzoni, Elsa, Born, Jan, Rauss, Karsten
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Oxford University Press 2021
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8361350/
https://www.ncbi.nlm.nih.gov/pubmed/33743012
http://dx.doi.org/10.1093/sleep/zsab056
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author Lutz, Nicolas D
Admard, Marie
Genzoni, Elsa
Born, Jan
Rauss, Karsten
author_facet Lutz, Nicolas D
Admard, Marie
Genzoni, Elsa
Born, Jan
Rauss, Karsten
author_sort Lutz, Nicolas D
collection PubMed
description STUDY OBJECTIVES: The brain appears to use internal models to successfully interact with its environment via active predictions of future events. Both internal models and the predictions derived from them are based on previous experience. However, it remains unclear how previously encoded information is maintained to support this function, especially in the visual domain. In the present study, we hypothesized that sleep consolidates newly encoded spatio-temporal regularities to improve predictions afterwards. METHODS: We tested this hypothesis using a novel sequence-learning paradigm that aimed to dissociate perceptual from motor learning. We recorded behavioral performance and high-density electroencephalography (EEG) in male human participants during initial training and during testing two days later, following an experimental night of sleep (n = 16, including high-density EEG recordings) or wakefulness (n = 17). RESULTS: Our results show sleep-dependent behavioral improvements correlated with sleep-spindle activity specifically over occipital cortices. Moreover, event-related potential (ERP) responses indicate a shift of attention away from predictable to unpredictable sequences after sleep, consistent with enhanced automaticity in the processing of predictable sequences. CONCLUSIONS: These findings suggest a sleep-dependent improvement in the prediction of visual sequences, likely related to visual cortex reactivation during sleep spindles. Considering that controls in our experiments did not fully exclude oculomotor contributions, future studies will need to address the extent to which these effects depend on purely perceptual versus oculomotor sequence learning.
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spelling pubmed-83613502021-08-13 Occipital sleep spindles predict sequence learning in a visuo-motor task Lutz, Nicolas D Admard, Marie Genzoni, Elsa Born, Jan Rauss, Karsten Sleep Cognitive, Affective and Behavioral Neuroscience of Sleep STUDY OBJECTIVES: The brain appears to use internal models to successfully interact with its environment via active predictions of future events. Both internal models and the predictions derived from them are based on previous experience. However, it remains unclear how previously encoded information is maintained to support this function, especially in the visual domain. In the present study, we hypothesized that sleep consolidates newly encoded spatio-temporal regularities to improve predictions afterwards. METHODS: We tested this hypothesis using a novel sequence-learning paradigm that aimed to dissociate perceptual from motor learning. We recorded behavioral performance and high-density electroencephalography (EEG) in male human participants during initial training and during testing two days later, following an experimental night of sleep (n = 16, including high-density EEG recordings) or wakefulness (n = 17). RESULTS: Our results show sleep-dependent behavioral improvements correlated with sleep-spindle activity specifically over occipital cortices. Moreover, event-related potential (ERP) responses indicate a shift of attention away from predictable to unpredictable sequences after sleep, consistent with enhanced automaticity in the processing of predictable sequences. CONCLUSIONS: These findings suggest a sleep-dependent improvement in the prediction of visual sequences, likely related to visual cortex reactivation during sleep spindles. Considering that controls in our experiments did not fully exclude oculomotor contributions, future studies will need to address the extent to which these effects depend on purely perceptual versus oculomotor sequence learning. Oxford University Press 2021-03-20 /pmc/articles/PMC8361350/ /pubmed/33743012 http://dx.doi.org/10.1093/sleep/zsab056 Text en © Sleep Research Society 2021. Published by Oxford University Press on behalf of the Sleep Research Society. https://creativecommons.org/licenses/by-nc/4.0/This is an Open Access article distributed under the terms of the Creative Commons Attribution-NonCommercial License (http://creativecommons.org/licenses/by-nc/4.0/ (https://creativecommons.org/licenses/by-nc/4.0/) ), which permits non-commercial re-use, distribution, and reproduction in any medium, provided the original work is properly cited. For commercial re-use, please contact journals.permissions@oup.com
spellingShingle Cognitive, Affective and Behavioral Neuroscience of Sleep
Lutz, Nicolas D
Admard, Marie
Genzoni, Elsa
Born, Jan
Rauss, Karsten
Occipital sleep spindles predict sequence learning in a visuo-motor task
title Occipital sleep spindles predict sequence learning in a visuo-motor task
title_full Occipital sleep spindles predict sequence learning in a visuo-motor task
title_fullStr Occipital sleep spindles predict sequence learning in a visuo-motor task
title_full_unstemmed Occipital sleep spindles predict sequence learning in a visuo-motor task
title_short Occipital sleep spindles predict sequence learning in a visuo-motor task
title_sort occipital sleep spindles predict sequence learning in a visuo-motor task
topic Cognitive, Affective and Behavioral Neuroscience of Sleep
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8361350/
https://www.ncbi.nlm.nih.gov/pubmed/33743012
http://dx.doi.org/10.1093/sleep/zsab056
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