Sleep-related hippocampo-cortical interplay during emotional memory recollection.
Emotional events are usually better remembered than neutral ones. This effect is mediated in part by a modulation of the hippocampus by the amygdala. Sleep plays a role in the consolidation of declarative memory. We examined the impact of sleep and lack of sleep on the consolidation of emotional (ne...
| Main Authors: | , , , , , , , , , , , , , , , |
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| Format: | Article |
| Language: | English |
| Published: |
Public Library of Science (PLoS)
2007-10-01
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| Series: | PLoS Biology |
| Online Access: | https://doi.org/10.1371/journal.pbio.0050282 |
| _version_ | 1819198419927826432 |
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| author | Virginie Sterpenich Geneviève Albouy Mélanie Boly Gilles Vandewalle Annabelle Darsaud Evelyne Balteau Thien Thanh Dang-Vu Martin Desseilles Arnaud D'Argembeau Steffen Gais Géraldine Rauchs Manuel Schabus Christian Degueldre André Luxen Fabienne Collette Pierre Maquet |
| author_facet | Virginie Sterpenich Geneviève Albouy Mélanie Boly Gilles Vandewalle Annabelle Darsaud Evelyne Balteau Thien Thanh Dang-Vu Martin Desseilles Arnaud D'Argembeau Steffen Gais Géraldine Rauchs Manuel Schabus Christian Degueldre André Luxen Fabienne Collette Pierre Maquet |
| author_sort | Virginie Sterpenich |
| collection | DOAJ |
| description | Emotional events are usually better remembered than neutral ones. This effect is mediated in part by a modulation of the hippocampus by the amygdala. Sleep plays a role in the consolidation of declarative memory. We examined the impact of sleep and lack of sleep on the consolidation of emotional (negative and positive) memories at the macroscopic systems level. Using functional MRI (fMRI), we compared the neural correlates of successful recollection by humans of emotional and neutral stimuli, 72 h after encoding, with or without total sleep deprivation during the first post-encoding night. In contrast to recollection of neutral and positive stimuli, which was deteriorated by sleep deprivation, similar recollection levels were achieved for negative stimuli in both groups. Successful recollection of emotional stimuli elicited larger responses in the hippocampus and various cortical areas, including the medial prefrontal cortex, in the sleep group than in the sleep deprived group. This effect was consistent across subjects for negative items but depended linearly on individual memory performance for positive items. In addition, the hippocampus and medial prefrontal cortex were functionally more connected during recollection of either negative or positive than neutral items, and more so in sleeping than in sleep-deprived subjects. In the sleep-deprived group, recollection of negative items elicited larger responses in the amygdala and an occipital area than in the sleep group. In contrast, no such difference in brain responses between groups was associated with recollection of positive stimuli. The results suggest that the emotional significance of memories influences their sleep-dependent systems-level consolidation. The recruitment of hippocampo-neocortical networks during recollection is enhanced after sleep and is hindered by sleep deprivation. After sleep deprivation, recollection of negative, potentially dangerous, memories recruits an alternate amygdalo-cortical network, which would keep track of emotional information despite sleep deprivation. |
| first_indexed | 2024-12-23T03:00:09Z |
| format | Article |
| id | doaj.art-978fe15275f841c8ae615e00dfcdcd45 |
| institution | Directory Open Access Journal |
| issn | 1544-9173 1545-7885 |
| language | English |
| last_indexed | 2024-12-23T03:00:09Z |
| publishDate | 2007-10-01 |
| publisher | Public Library of Science (PLoS) |
| record_format | Article |
| series | PLoS Biology |
| spelling | doaj.art-978fe15275f841c8ae615e00dfcdcd452022-12-21T18:02:27ZengPublic Library of Science (PLoS)PLoS Biology1544-91731545-78852007-10-01511e28210.1371/journal.pbio.0050282Sleep-related hippocampo-cortical interplay during emotional memory recollection.Virginie SterpenichGeneviève AlbouyMélanie BolyGilles VandewalleAnnabelle DarsaudEvelyne BalteauThien Thanh Dang-VuMartin DesseillesArnaud D'ArgembeauSteffen GaisGéraldine RauchsManuel SchabusChristian DegueldreAndré LuxenFabienne CollettePierre MaquetEmotional events are usually better remembered than neutral ones. This effect is mediated in part by a modulation of the hippocampus by the amygdala. Sleep plays a role in the consolidation of declarative memory. We examined the impact of sleep and lack of sleep on the consolidation of emotional (negative and positive) memories at the macroscopic systems level. Using functional MRI (fMRI), we compared the neural correlates of successful recollection by humans of emotional and neutral stimuli, 72 h after encoding, with or without total sleep deprivation during the first post-encoding night. In contrast to recollection of neutral and positive stimuli, which was deteriorated by sleep deprivation, similar recollection levels were achieved for negative stimuli in both groups. Successful recollection of emotional stimuli elicited larger responses in the hippocampus and various cortical areas, including the medial prefrontal cortex, in the sleep group than in the sleep deprived group. This effect was consistent across subjects for negative items but depended linearly on individual memory performance for positive items. In addition, the hippocampus and medial prefrontal cortex were functionally more connected during recollection of either negative or positive than neutral items, and more so in sleeping than in sleep-deprived subjects. In the sleep-deprived group, recollection of negative items elicited larger responses in the amygdala and an occipital area than in the sleep group. In contrast, no such difference in brain responses between groups was associated with recollection of positive stimuli. The results suggest that the emotional significance of memories influences their sleep-dependent systems-level consolidation. The recruitment of hippocampo-neocortical networks during recollection is enhanced after sleep and is hindered by sleep deprivation. After sleep deprivation, recollection of negative, potentially dangerous, memories recruits an alternate amygdalo-cortical network, which would keep track of emotional information despite sleep deprivation.https://doi.org/10.1371/journal.pbio.0050282 |
| spellingShingle | Virginie Sterpenich Geneviève Albouy Mélanie Boly Gilles Vandewalle Annabelle Darsaud Evelyne Balteau Thien Thanh Dang-Vu Martin Desseilles Arnaud D'Argembeau Steffen Gais Géraldine Rauchs Manuel Schabus Christian Degueldre André Luxen Fabienne Collette Pierre Maquet Sleep-related hippocampo-cortical interplay during emotional memory recollection. PLoS Biology |
| title | Sleep-related hippocampo-cortical interplay during emotional memory recollection. |
| title_full | Sleep-related hippocampo-cortical interplay during emotional memory recollection. |
| title_fullStr | Sleep-related hippocampo-cortical interplay during emotional memory recollection. |
| title_full_unstemmed | Sleep-related hippocampo-cortical interplay during emotional memory recollection. |
| title_short | Sleep-related hippocampo-cortical interplay during emotional memory recollection. |
| title_sort | sleep related hippocampo cortical interplay during emotional memory recollection |
| url | https://doi.org/10.1371/journal.pbio.0050282 |
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