Abstract
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.
Highlights
Memory consolidation is the protracted process by which fresh, initially labile, memories are reorganized into enduring stable memories [1]
Mean subjective sleep duration was longer for the total sleep deprivation (TSD) than for the resting sleep (RS) group for the second post-encoding night (F(1,37) 1⁄4 17.45, p, 0.0001), reflecting the expected sleep rebound after deprivation
Functional MRI Results For the sake of completeness, several main effects are reported in the supplemental material: (1) main effect of successful recognition (R þ K responses) separately for the three valences in both groups (Table S3, Figure S1A), (2) the effects of emotion on successful recognition in both groups, and (3) the main effect of memory type in both groups (R versus K responses, Table S5, Figure S2)
Summary
Memory consolidation is the protracted process by which fresh, initially labile, memories are reorganized into enduring stable memories [1]. Memory consolidation results in a progressive rearrangement of memories that can eventually be stored in circuits different from those in which they were initially encoded [2]. A growing body of data suggests that sleep is involved in the consolidation of declarative memories [5]. Sleep protects declarative memories from subsequent interference [7]. Training to a declarative memory task is followed by changes in fine-grained sleep structure during the postencoding night, such as an increase in sleep spindle density [8]. Sleep deprivation hinders the plastic changes that normally occur during sleep and alters the brain responses subsequently recorded at retest [9]
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