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      To Sleep, to Strive, or Both: How Best to Optimize Memory

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          Abstract

          While numerous studies have shown that a night of sleep profits memory relative to wake, we still have little understanding about what factors mediate this effect of sleep. A clear understanding of the dynamics of this effect of sleep beyond the initial night of sleep is also lacking. Here, we examined the effect of extrinsic rewards on sleep-dependent declarative memory processing across 12 and 24 hr training-retest intervals. Subjects were either paid based on their performance at retest ($1 for each correct answer), or received a flat fee for participation. After a 12 hr interval we observed pronounced benefits of both sleep and reward on memory. Over an extended 24 hr interval we found 1) that an initial night of sleep partially protects memories from subsequent deterioration during wake, and 2) that sleep blocks further deterioration, and may even have a restorative effect on memory, when it follows a full day of wake. Interestingly, the benefit imparted to rewarded (relative to unrewarded) stimuli was equal for sleep and wake subjects, suggesting that the sleeping brain may not differentially process rewarded information, relative to wake. However, looking at the overall impact of sleep relative to reward in this protocol, it was apparent that sleep both imparted a stronger mnemonic boost than reward, and provided a benefit to memory regardless of whether it occurred in the first or the second 12 hrs following task training.

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          Most cited references20

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          Reward-motivated learning: mesolimbic activation precedes memory formation.

          We examined anticipatory mechanisms of reward-motivated memory formation using event-related FMRI. In a monetary incentive encoding task, cues signaled high- or low-value reward for memorizing an upcoming scene. When tested 24 hr postscan, subjects were significantly more likely to remember scenes that followed cues for high-value rather than low-value reward. A monetary incentive delay task independently localized regions responsive to reward anticipation. In the encoding task, high-reward cues preceding remembered but not forgotten scenes activated the ventral tegmental area, nucleus accumbens, and hippocampus. Across subjects, greater activation in these regions predicted superior memory performance. Within subject, increased correlation between the hippocampus and ventral tegmental area was associated with enhanced long-term memory for the subsequent scene. These findings demonstrate that brain activation preceding stimulus encoding can predict declarative memory formation. The findings are consistent with the hypothesis that reward motivation promotes memory formation via dopamine release in the hippocampus prior to learning.
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            Reward-related FMRI activation of dopaminergic midbrain is associated with enhanced hippocampus-dependent long-term memory formation.

            Long-term potentiation in the hippocampus can be enhanced and prolonged by dopaminergic inputs from midbrain structures such as the substantia nigra. This improved synaptic plasticity is hypothesized to be associated with better memory consolidation in the hippocampus. We used a condition that reliably elicits a dopaminergic response, reward anticipation, to study the relationship between activity of dopaminergic midbrain areas and hippocampal long-term memory in healthy adults. Pictures of object drawings that predicted monetary reward were associated with stronger fMRI activity in reward-related brain areas, including the substantia nigra, compared with non-reward-predicting pictures. Three weeks later, recollection and source memory were better for reward-predicting than for non-reward-predicting pictures. FMRI activity in the hippocampus and the midbrain was higher for reward-predicting pictures that were later recognized compared with later forgotten pictures. These data are consistent with the hypothesis that activation of dopaminergic midbrain regions enhances hippocampus-dependent memory formation, possibly by enhancing consolidation.
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              Sleep spindles and their significance for declarative memory consolidation.

              Functional significance of stage 2 sleep spindle activity for declarative memory consolidation. Randomized, within-subject, multicenter. Weekly sleep laboratory visits, actigraphy, and sleep diary (4 weeks). Twenty-four healthy subjects (12 men) aged between 20 and 30 years. Declarative memory task or nonlearning control task before sleep. This study measured spindle activity during stage 2 sleep following a (declarative) word-pair association task as compared to a control task. Participants performed a cued recall in the evening after learning (160 word pairs) as well as in the subsequent morning after 8 hours of undisturbed sleep with full polysomnography. Overnight change in the number of recalled words, but not absolute memory performance, correlated significantly with increased spindle activity during the experimental night (r24 = .63, P < .01). Time spent in each sleep stage could not account for this relationship. A growing body of evidence supports the active role of sleep for information reprocessing. Whereas past research focused mainly on the distinct rapid eye movement and slow-wave sleep, these results indicate that increased sleep stage 2 spindle activity is related to an increase in recall performance and, thus, may reflect memory consolidation.
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                Author and article information

                Contributors
                Role: Editor
                Journal
                PLoS One
                plos
                plosone
                PLoS ONE
                Public Library of Science (San Francisco, USA )
                1932-6203
                2011
                20 July 2011
                : 6
                : 7
                : e21737
                Affiliations
                [1 ]Department of Psychiatry, Harvard Medical School, Boston, Massachusetts, United States of America
                [2 ]Department of Psychology, Harvard University, Cambridge, Massachusetts, United States of America
                [3 ]Center for Sleep and Cognition, Boston, Massachusetts, United States of America
                University of Alberta, Canada
                Author notes

                Conceived and designed the experiments: MAT RS. Performed the experiments: MAT SXT AU. Analyzed the data: MAT RS SXT. Contributed reagents/materials/analysis tools: AM. Wrote the paper: MAT SXT RS.

                Article
                PONE-D-11-01501
                10.1371/journal.pone.0021737
                3140493
                21799746
                f09e884d-a65d-4db4-9231-aefe8cef914b
                Tucker et al. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
                History
                : 18 January 2011
                : 10 June 2011
                Page count
                Pages: 6
                Categories
                Research Article
                Biology
                Anatomy and Physiology
                Physiological Processes
                Sleep
                Neuroscience
                Learning and Memory

                Uncategorized
                Uncategorized

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