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Right-lateralized sleep spindles are associated with neutral over emotional bias in picture recognition: An overnight study

Sleep is especially important for emotional memories, although the mechanisms for prioritizing emotional content are insufficiently known. As during waking, emotional processing during sleep may be hemispherically asymmetric; right-lateralized rapid-eye movement (REM) sleep theta (~4–7 Hz) is report...

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Autores principales: Halonen, Risto, Luokkala, Sanni, Kuula, Liisa, Antila, Minea, Pesonen, Anu-Katriina
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Springer US 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10260275/
https://www.ncbi.nlm.nih.gov/pubmed/37308745
http://dx.doi.org/10.3758/s13415-023-01113-4
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author Halonen, Risto
Luokkala, Sanni
Kuula, Liisa
Antila, Minea
Pesonen, Anu-Katriina
author_facet Halonen, Risto
Luokkala, Sanni
Kuula, Liisa
Antila, Minea
Pesonen, Anu-Katriina
author_sort Halonen, Risto
collection PubMed
description Sleep is especially important for emotional memories, although the mechanisms for prioritizing emotional content are insufficiently known. As during waking, emotional processing during sleep may be hemispherically asymmetric; right-lateralized rapid-eye movement (REM) sleep theta (~4–7 Hz) is reportedly associated with emotional memory retention. No research exists on lateralized non-REM sleep oscillations. However, sleep spindles, especially when coupled with slow oscillations (SOs), facilitate off-line memory consolidation. Our primary goal was to examine how the lateralization (right-to-left contrast) of REM theta, sleep spindles, and SO-spindle coupling is associated with overnight recognition memory in a task consisting of neutral and emotionally aversive pictures. Thirty-two healthy adults encoded 150 target pictures before overnight sleep. The recognition of target pictures among foils (discriminability, d’) was tested immediately, 12 hours, and 24 hours after encoding. Recognition discriminability between targets and foils was similar for neutral and emotional pictures in immediate and 12-h retrievals. After 24 hours, emotional pictures were less accurately discriminated (p < 0.001). Emotional difference at 24-h retrieval was associated with right-to-left contrast in frontal fast spindle density (p < 0.001). The lateralization of SO-spindle coupling was associated with higher neutral versus emotional difference across all retrievals (p = 0.004). Our findings contribute to a largely unstudied area in sleep-related memory research. Hemispheric asymmetry in non-REM sleep oscillations may contribute to how neutral versus emotional information is processed. This is presumably underlain by both mechanistic offline memory consolidation and a trait-like cognitive/affective bias that influences memory encoding and retrieval. Methodological choices and participants’ affective traits are likely involved. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.3758/s13415-023-01113-4.
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spelling pubmed-102602752023-06-14 Right-lateralized sleep spindles are associated with neutral over emotional bias in picture recognition: An overnight study Halonen, Risto Luokkala, Sanni Kuula, Liisa Antila, Minea Pesonen, Anu-Katriina Cogn Affect Behav Neurosci Research Article Sleep is especially important for emotional memories, although the mechanisms for prioritizing emotional content are insufficiently known. As during waking, emotional processing during sleep may be hemispherically asymmetric; right-lateralized rapid-eye movement (REM) sleep theta (~4–7 Hz) is reportedly associated with emotional memory retention. No research exists on lateralized non-REM sleep oscillations. However, sleep spindles, especially when coupled with slow oscillations (SOs), facilitate off-line memory consolidation. Our primary goal was to examine how the lateralization (right-to-left contrast) of REM theta, sleep spindles, and SO-spindle coupling is associated with overnight recognition memory in a task consisting of neutral and emotionally aversive pictures. Thirty-two healthy adults encoded 150 target pictures before overnight sleep. The recognition of target pictures among foils (discriminability, d’) was tested immediately, 12 hours, and 24 hours after encoding. Recognition discriminability between targets and foils was similar for neutral and emotional pictures in immediate and 12-h retrievals. After 24 hours, emotional pictures were less accurately discriminated (p < 0.001). Emotional difference at 24-h retrieval was associated with right-to-left contrast in frontal fast spindle density (p < 0.001). The lateralization of SO-spindle coupling was associated with higher neutral versus emotional difference across all retrievals (p = 0.004). Our findings contribute to a largely unstudied area in sleep-related memory research. Hemispheric asymmetry in non-REM sleep oscillations may contribute to how neutral versus emotional information is processed. This is presumably underlain by both mechanistic offline memory consolidation and a trait-like cognitive/affective bias that influences memory encoding and retrieval. Methodological choices and participants’ affective traits are likely involved. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.3758/s13415-023-01113-4. Springer US 2023-06-12 2023 /pmc/articles/PMC10260275/ /pubmed/37308745 http://dx.doi.org/10.3758/s13415-023-01113-4 Text en © The Author(s) 2023 https://creativecommons.org/licenses/by/4.0/Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) .
spellingShingle Research Article
Halonen, Risto
Luokkala, Sanni
Kuula, Liisa
Antila, Minea
Pesonen, Anu-Katriina
Right-lateralized sleep spindles are associated with neutral over emotional bias in picture recognition: An overnight study
title Right-lateralized sleep spindles are associated with neutral over emotional bias in picture recognition: An overnight study
title_full Right-lateralized sleep spindles are associated with neutral over emotional bias in picture recognition: An overnight study
title_fullStr Right-lateralized sleep spindles are associated with neutral over emotional bias in picture recognition: An overnight study
title_full_unstemmed Right-lateralized sleep spindles are associated with neutral over emotional bias in picture recognition: An overnight study
title_short Right-lateralized sleep spindles are associated with neutral over emotional bias in picture recognition: An overnight study
title_sort right-lateralized sleep spindles are associated with neutral over emotional bias in picture recognition: an overnight study
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10260275/
https://www.ncbi.nlm.nih.gov/pubmed/37308745
http://dx.doi.org/10.3758/s13415-023-01113-4
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