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The impact of overnight consolidation upon memory for emotional and neutral encoding contexts
Open accessAbstract
Sleep plays a role in the consolidation of declarative memories. Although this influence has attracted much attention at the level of behavioural performance, few reports have searched for neural correlates. Here, we studied the impact of sleep upon memory for the context in which stimuli were learned at both behavioural and neural levels. Participants retrieved the association between a presented foreground object and its encoding context following a 12-h retention interval including either wake only or wake plus a night of sleep. Since sleep has been shown to selectively enhance some forms of emotional memory, we examined both neutral and emotionally valenced contexts. Behaviourally, less forgetting was observed across retention intervals containing sleep than retention intervals containing only wakefulness, and this benefit was accompanied by stronger responses in hippocampus and superior parietal cortex. This sleep-related reduction in forgetting did not differ between neutral and negative contexts, but there was a clear interaction between sleep and context valence at the functional level, with left amygdala, right parahippocampus, and other components of the episodic memory system all responding more strongly during correct memory for emotional contexts post-sleep. Connectivity between right parahippocampus and bilateral amygdala/periamygdala was also enhanced during correct post-sleep attribution of emotional contexts. Because there was no interaction between sleep and valence in terms of context memory performance these functional results may be associated with memory for details about the emotional encoding context rather than for the link between that context and the foreground object. Overall, our data show that while context memory decays less across sleep than across an equivalent period of wake, the sleep-related protection of such associations is not influenced by context emotionality in the same way as direct recollection of emotional information.
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Compared with item memory, context memory is particularly sensitive to beneficial effects of sleep.
“In addition, some human studies revealed that, compared with item memory, context memory, a core function of the hippocampus, is particularly sensitive to the beneficial effects of sleep (602,732,1128,1230).”
From About Sleep's Role in Memory (2013) · cites this paper as [732]
The Discussion (page not available in our copy) reports that source memory, a form of context memory, decayed less after sleep than after wakefulness. It does not show that context memory benefits more from sleep than item memory; its item-memory comparison concerns parietal activity, not the relative effect of sleep. (LLM, conf=0.87)
Experimental — accuracy not yet measuredOther studies failed to reveal preferential consolidation of emotional over neutral memories during sleep.
“Some studies indeed demonstrated that sleep preferentially consolidates emotional over neutral memories (574,602,861,896,898,1276); however, others failed to reveal such effects (60,168,732,1147,1148).”
From About Sleep's Role in Memory (2013) · cites this paper as [732]
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Metadata
- Authors
- Lewis, P. A., Cairney, S., Manning, L., & Critchley, H. D.
- Affiliations
- University of Manchester (GB)
- University of Liverpool (GB)
- Brighton and Sussex Medical School (GB)
- Corresponding author
- Lewis, P.A.
- Venue
- Neuropsychologia
- Publisher
- Elsevier BV
- Published
- 2011-07
- Volume
- 49
- Issue
- 9
- Pages
- 2619-2629
- ISSN
- 0028-3932 (ISSN-L)
- PMC
- PMC7614373
- OpenAlex
- W2114681689
- Cited by
- 79
- References
- 72
- Citations by year
- 2025: 3 · 2024: 3 · 2023: 2 · 2022: 2 · 2021: 9 · 2020: 4 · 2019: 6 · 2018: 8 · 2017: 8 · 2016: 4 · 2015: 4 · 2014: 12 · 2013: 10 · 2012: 3
- FWCI
- 4.06
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Locations
- Neuropsychologia (publishedVersion)
- PubMed (publishedVersion)
- Research Explorer (The University of Manchester) (publishedVersion)
- PubMed Central (acceptedVersion)
- ORCA Online Research @Cardiff (Cardiff University) (submittedVersion)
- Funders
- University of Liverpool
- Wellcome Trust VIP Award
- Topics
- Life Sciences › Neuroscience › Cognitive Neuroscience › Sleep and Wakefulness Research
- Life Sciences › Neuroscience › Cognitive Neuroscience › Memory and Neural Mechanisms
- Life Sciences › Neuroscience › Cognitive Neuroscience › Memory Processes and Influences
- Keywords
- sleep-dependent memory consolidation, emotional memory, contextual memory, encoding context, hippocampus, amygdala, parahippocampal cortex, superior parietal cortex, episodic memory, neural correlates of memory, emotional valence, forgetting
- MeSH terms
- Adult, Anthracenes, Association Learning, Brain Mapping, Emotions, Female, Hippocampus, Humans, Magnetic Resonance Imaging, Male, Parietal Lobe, Reference Values, Retention, Psychology, Sleep, Wakefulness, Young Adult
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