The last decade has seen a dramatic increase in our understanding of sleep-dependent memory consolidation, moving it from a generally discredited (or at best ignored) concept to a largely accepted tenet among both memory and sleep researchers, even found in undergraduate psychology textbooks. This work has established a firm connection between sleep and memory function. But given the complexity of both sleep and memory, each of which comprise multiple stages and subtypes, even the most basic characterizations of this phenomenon remain unclear. Which types of memory are consolidated during sleep? Which components of consolidation occur during sleep? Which sleep stages mediate this consolidation? And what physiological processes underlie sleep-dependent consolidation? To date, most studies have sought to assign consolidation of particular classes of memory to discrete sleep stages, for example consolidation of procedural memories to REM sleep or declarative memories to slow wave sleep (SWS). But exceptions to this simple dichotomy come close to outnumbering supporting studies. Several new studies, presented here, lead us to now propose a unified sleep-dependent memory consolidation hypothesis, to describe how sleep stages contribute to memory consolidation. We propose that sleep plays a more nuanced role in memory processing than previously considered, with sleep stages being selectively involved not with specific memory types, but with specific components of the memory consolidation process. Specifically, we propose that SWS stabilizes recently acquired declarative and procedural memories, while REM and Stage 2 nonREM sleep subsequently enhance them, selectively reinforcing their most valuable components and integrating them into preexisting networks of stored information. As we will show below, this new hypothesis is consistent with the growing literature of sleep-dependent consolidation across a range of memory functions, and is strongly supported by our Preliminary Results. These new results, in concert with the unified memory consolidation hypothesis, move the study of sleep and memory beyond a discussion of classical memory consolidation (i.e., stabilization), into the realm of more powerful and valuable forms of sleep-dependent memory enhancement that (i) enlarge the neural networks in which memories are stored,(ii) extract patterns and rules from large bodies of encoded information and (iii) integrate them with other, older memories into rich semantic networks, thereby selectively enhancing those aspects of memories of greatest value to the organism. In the research program proposed below, we will test our unified sleep-dependent memory consolidation hypothesis through integrated studies designed to identify (1) the types of memories consolidated during sleep, (2) the sleep stage correlates of both their stabilization and their various forms of enhancement (e.g. integration, rule extraction) and (3) the physiological substrates of these processes.

Public Health Relevance

Western society has become increasingly sleep deprived, and nowhere is this more true than in the United States, where there is a popular belief that the only consequence of sleep deprivation is sleepiness which can be overcome with effort or drugs, and that a good night's sleep on the weekend can completely reverse any deleterious effects of mid-week deprivation. But it is now clear that sleep plays a critical role in the stabilization and enhancement of recently formed memories, and that sleep loss can cause the irrevocable loss of these potential benefits. We now put forward a unified sleep-dependent memory consolidation hypothesis, proposing that deep, slow wave sleep stabilizes recently acquired memories, while REM sleep and lighter, Stage-2 nonREM sleep subsequently enhance these memories, selectively reinforcing their most valuable components and integrating them into preexisting networks of stored information.

Agency
National Institute of Health (NIH)
Institute
National Institute of Mental Health (NIMH)
Type
Research Project (R01)
Project #
5R01MH048832-16
Application #
7805453
Study Section
Cognition and Perception Study Section (CP)
Program Officer
Vicentic, Aleksandra
Project Start
1993-09-01
Project End
2014-02-28
Budget Start
2010-03-01
Budget End
2011-02-28
Support Year
16
Fiscal Year
2010
Total Cost
$526,014
Indirect Cost
Name
Beth Israel Deaconess Medical Center
Department
Type
DUNS #
071723621
City
Boston
State
MA
Country
United States
Zip Code
02215
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Cox, Roy; Schapiro, Anna C; Manoach, Dara S et al. (2017) Individual Differences in Frequency and Topography of Slow and Fast Sleep Spindles. Front Hum Neurosci 11:433
Purcell, S M; Manoach, D S; Demanuele, C et al. (2017) Characterizing sleep spindles in 11,630 individuals from the National Sleep Research Resource. Nat Commun 8:15930
Demanuele, Charmaine; Bartsch, Ullrich; Baran, Bengi et al. (2017) Coordination of Slow Waves With Sleep Spindles Predicts Sleep-Dependent Memory Consolidation in Schizophrenia. Sleep 40:
Tucker, Matthew A; Nguyen, Nam; Stickgold, Robert (2016) Experience Playing a Musical Instrument and Overnight Sleep Enhance Performance on a Sequential Typing Task. PLoS One 11:e0159608
Manoach, Dara S; Pan, Jen Q; Purcell, Shaun M et al. (2016) Reduced Sleep Spindles in Schizophrenia: A Treatable Endophenotype That Links Risk Genes to Impaired Cognition? Biol Psychiatry 80:599-608
Walker, Matthew P; Stickgold, Robert (2016) Understanding the boundary conditions of memory reconsolidation. Proc Natl Acad Sci U S A 113:E3991-2
Gregory, Michael D; Robertson, Edwin M; Manoach, Dara S et al. (2016) Thinking About a Task Is Associated with Increased Connectivity in Regions Activated by Task Performance. Brain Connect 6:164-8
Barsky, Murray M; Tucker, Matthew A; Stickgold, Robert (2015) REM sleep enhancement of probabilistic classification learning is sensitive to subsequent interference. Neurobiol Learn Mem 122:63-8
Manoach, Dara S; Stickgold, Robert (2015) Sleep, memory and schizophrenia. Sleep Med 16:553-4

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