Peer review of Walker's 'A refined model of sleep …'
Various
Source: Behavioral and Brain Sciences, 28, Issue 01, February 2005, pp 65-86
Paper - Abstract

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Reviews

  1. Redefining memory consolidation (Mercedes Atienza and Jose L. Cantero). Abstract: Based on brain state-dependent behavioral changes, consolidation of sensorimotor memories has been posited to evolve in two different functional stages. Only the second of these stages requires sleep1 and leads to performance benefits. Recent results, however, suggest that sleep2 is not always crucial for the expression of delayed behavioral gains but might be critical for enhancing automaticity in the absence of attention, another expression of memory consolidation.
  2. Molecular mechanisms of synaptic consolidation during sleep3: BDNF function and dendritic protein synthesis (Clive R. Bramham). Abstract: Insights into the role of sleep4 in the molecular mechanisms of memory consolidation may come from studies of activity-dependent synaptic plasticity, such as long-term potentiation (LTP). This commentary posits a specific contribution of sleep5 to LTP stabilization, in which mRNA transported to dendrites during wakefulness is translated during sleep6. Brain-derived neurotrophic factor may drive the translation of newly transported and resident mRNA.
  3. Sleep7 is optimizing (Thomas L. Clarke). Abstract: It is suggested that Walker's consolidation-based enhancement of memory during REM sleep8 corresponds to the simulated annealing technique used for function optimization, and that robotic and AI design could benefit from inclusion of a deliberate REM-like memory optimization phase.
  4. Where is the classic interference theory for sleep9 and memory? (Anton Coenen). Abstract: Walker's target article proposes a refinement of the well known two-stage model of memory formation to explain the positive effects of sleep10 on consolidation. After a first stage in which a labile memory representation is formed, a further stabilisation of the memory trace takes place in the second stage, which is dependent on (REM) sleep11. Walker has refined the latter stage into a stage in which a consolidation-based enhancement occurs. It is not completely clear what consolidation-based enhancement implies and how it can be dissociated from a stage for memory-stabilisation. A more serious consideration, however, is whether a second stage in memory consolidation that is solely dependent on sleep12, is really necessary. The classical, passive, interference theory is able to explain adequately the findings related to the effects of sleep13 and memory, and can lead perhaps better to an understanding of the highly variable data in this field.
  5. Motor memory: Consolidation–based enhancement effect revisited (Julien Doyon, Julie Carrier, Alain Simard, Abdallah Hadj Tahar, Amélie Morin, Habib Benali and Leslie G. Ungerleider). Abstract: Following Karni's seminal work, Walker and other researchers have recently provided gradually convincing evidence that sleep14 is critical for the consolidation-based enhancement (CBE) of motor sequence learning. Studies in our laboratory using a motor adaptation paradigm, however, show that CBE can also occur after the simple passage of time, suggesting that sleep15 effects on memory consolidation are task-related, and possibly dependent on anatomically dissociable circuits.
  6. Do words go to sleep16? Exploring consolidation of spoken forms through direct and indirect measures (Nicolas Dumay and M. Gareth Gaskell). Abstract: We address the notion of integration of new memory representations and the potential dependence of this phenomenon on sleep17, in light of recent findings on the lexicalization of spoken words. A distinction is introduced between measures tapping directly into the strength of the newly acquired knowledge and indirect measures assessing the influence of this knowledge on spoken word identification.
  7. What is consolidated during sleep-dependent18 motor skill learning? Luca A. Finelli and Terrence J. Sejnowski. Abstract: Learning procedural skills involves improvement in speed and accuracy. Walker proposes two stages of memory consolidation: enhancement, which requires sleep19, and stabilization, which does not require sleep20. Speed improvement for a motor learning task but not accuracy occurs after sleep-dependent21 enhancement. We discuss this finding in the context of computational models and underlying sleep22 mechanisms.
  8. Sleep23 and memory: Definitions, terminology, models, and predictions? (Jonathan K. Foster and Andrew C. Wilson. Abstract: In this target article, Walker seeks to clarify the current state of knowledge regarding sleep24 and memory. Walker's review represents an impressively heuristic attempt to synthesize the relevant literature. In this commentary, we question the focus on procedural memory and the use of the term “consolidation,” and we consider the extent to which empirically testable predictions can be derived from Walker's model.
  9. Old wine (most of it) in new bottles: Where are dreams and what is the memory? (Ramon Greenberg. Abstract: I discuss how the work in Walker's article adds to the considerable body of research on dreaming, sleep25, and memory that appeared in the early days of modern sleep26 research. I also consider the issue of REM-independent and REM-dependent kinds of learning. This requires including emotional issues in our discussion, and therefore emphasizes the importance of studying and understanding dreams.
  10. Consolidating consolidation? Sleep27 stages, memory systems, and procedures (John A. Groeger and Derk-Jan Dijk. Abstract: We argue that by neglecting the fact that procedural memory may also have episodic qualities, and by considering only a systems approach to memory, Walker's account of consolidation of learning during subsequent sleep28 ignores alternative accounts of how sleep29 stages may be interdependent. We also question the proposition that sleep-based30 consolidation largely bypasses hippocampal structures.
  11. Resistance to interference and the emergence of delayed gains in newly acquired procedural memories: Synaptic and system consolidation? (Maria Korman, Tamar Flash and Avi Karni. Abstract: The progressive multistage stabilization of memory (consolidation) relies on post-acquisition neural reorganization. We hypothesize that two processes subserve procedural memory consolidation and are reflected in delayed post-acquisition performance gains: (1) synaptic consolidation, which is classical Hebbian, and (2) in some tasks, concurrently or consequently, “system consolidation,” which might in some skills be sleep-dependent31. Behavioral interference may affect either type of consolidation.
  12. Neurosignals – Incorporating CNS electrophysiology into cognitive process (James F. Pagel). Abstract: This commentary reviews electrophysiological research suggesting that oscillatory electrical potentials recorded by the EEG could have function at cellular and DNA levels. Evidence supporting the potential functional significance of sleep-state-specific32 frequencies includes psychoactive neurochemical alteration of CNS electrophysiology, and sleep-state-specific33 alteration of dreaming. As Walker proposes, physiologic electrical fields are likely to have a functional role in the consolidation of memory.
  13. Beyond acetylcholine: Next steps for sleep34 and memory research (Jessica D. Payne, Willoughby B. Britton, Richard R. Bootzin and Lynn Nadel. Abstract: We consider Walker's thorough review in the context of thinking about future research on the relation between sleep35 and memory. We first address methodological issues including type of memory and sleep-stage36 dependency. We suggest a broader investigation of potential signaling molecules that may be critical to sleep-related37 consolidation. A brief review of the importance of the stress hormone cortisol illustrates this point.
  14. Filling one gap by creating another: Memory stabilization is not all-or-nothing, either (Philippe Peigneux, Arnaud Destrebecqz, Christophe Hotermans and Axel Cleeremans. Abstract: Walker proposes that procedural memory formation involves two specific stages of consolidation: wake-dependent stabilization, followed by sleep-dependent38 enhancement. If sleep-based39 enhancement of procedural memory formation is now well supported by evidence obtained at different levels of cognitive and neurophysiological organization, wake-dependent mechanisms for stabilization have not been demonstrated as convincingly, and still require more systematic characterization.
  15. New perspectives on sleep40 disturbances and memory in human pathological and psychopharmacological states (Margaret A. Piggott and Elaine K. Perry. Abstract: Matthew Walker's article has prompted us to consider neuropsychiatric disorders and pharmacological effects associated with sleep41 alterations, and aspects of memory affected. Not all disorders involving insomnia show memory impairment, and hypersomnias can be associated with memory deficits. The use of cholinergic medication in dementia indicates that consideration of the link between sleep42 and memory is more than academic.
  16. Procedural replay: The anatomy and physics of the sleep43 spindle (Helene Sophrin Porte). Abstract: This commentary implicates the neostriatum in the production of the EEG sleep44 spindle and in the processing of motor procedural learning in sleep45. Whether the sleep46 spindle may implement not only the consolidation-based enhancement of procedural learning, but also its initial consolidation, is considered; as is the fit between (1) corticostriatal anatomy and physiology, and (2) the physical properties of the sleep47 spindle.
  17. REM sleep48, dreaming, and procedural memory (Michael Schredl). Abstract: In this commentary the “incredibly robust” evidence for the relationship between sleep49 and procedural memory is questioned; inconsistencies in the existing data are pointed out. In addition, some suggestions about extending research are made, for example, studying REM sleep50 augmentation or memory consolidation in patients with sleep51 disorders. Last, the possibility of a relationship between dreaming and memory processes is discussed.
  18. Memory consolidation during sleep52: A form of brain restitution (Bhavin R. Sheth). Abstract: Does sleep53 restore brain function or does it consolidate memory? I argue that memory consolidation during sleep54 is an offshoot of restitution. Continual learning causes local synapse-specific neural fatigue, which then masks expression of that learning, especially on time-limited tests of procedural skills. Sleep55 serves to restore the fatigued synapses, revealing the consolidation-based enhancement observed as a “latent” overnight improvement in learning.
  19. The incredible, shrinking sleep-learning56 connection (Jerome M. Siegel). Abstract:
    Initial claims that REM sleep57 is important in the consolidation of all memories have been revised and reduced to the claim that sleep58 has a role only in the consolidation of procedural learning. Now, Walker hypothesizes that sleep59 has no role in the “stabilization phase of consolidation” but only in the “enhanced learning” phase of procedural learning. Evidence for this vague, truncated hypothesis remains as inconsistent as that for prior claims.
  20. Consolidation enhancement: Which stages of sleep60 for which tasks? (Carlyle T. Smith). Abstract: The Walker model raises a number of questions, particularly about the nature of the sleep61 states involved in consolidation enhancement. While REM sleep62, Stage 2 sleep63, and Stage 3/4 sleep64 have been implicated in procedural learning, we still do not understand which types of learning are involved with specific sleep65 states. Several possible ideas for future research are suggested.
  21. The challenge of identifying cellular mechanisms of memory formation during sleep66 (Ronald Szymusiak). Abstract: Cellular mechanisms hypothesized to underlie sleep-dependent67 memory consolidation are expressed throughout the brain during sleep68. Use of sleep69 deprivation to evaluate the functional importance of these mechanisms is confounded by degradation in waking performance resulting from impaired vigilance. There is a need for methods that will permit disruption of specific mechanisms during sleep70 only in the neuronal circuits most critically involved in learning. This should be accomplished without global sleep71 disruption and with preservation of the restorative aspects of sleep72.
  22. Sleep73 and synaptic homeostasis (Giulio Tononi and Chiara Cirelli). Abstract: We propose that sleep74 is linked to synaptic homeostasis. Specifically, we propose that: (1) Wakefulness is associated with synaptic potentiation in cortical circuits; (2) synaptic potentiation is tied to the homeostatic regulation of slow wave activity; (3) slow wave activity is associated with synaptic downscaling; and (4) synaptic downscaling is tied to several beneficial effects of sleep75, including performance enhancement.
  23. Sleep76 is for rest, waking consciousness is for learning and memory – of any kind (Robert P. Vertes). Abstract: Although considerable attention has been paid to the possible involvement of sleep77 in memory processing, there is no substantial evidence for it. Walker describes a phenomenon of consolidation-based enhancement (CBE), whereby performance on select procedural tasks improves with overnight sleep78; that is, without additional practice on the tasks. CBE, however, appears restricted to a few tasks, and even with these tasks CBE is not confined to sleep79 but also occurs during wakefulness. Sleep80 serves no unique role in this process. At best, CBE is a slow, time-dependent process of consolidation that begins with task acquisition in waking and can under some circumstances extend to sleep81.

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