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• W2919952431 abstract "Is it really possible to learn new information during deep sleep? A new study suggests that implicit vocabulary binding can occur while we are snoozing. It also seems that the success of learning depends heavily upon the timing of such ‘sleepy stimulation’. Is it really possible to learn new information during deep sleep? A new study suggests that implicit vocabulary binding can occur while we are snoozing. It also seems that the success of learning depends heavily upon the timing of such ‘sleepy stimulation’. Sleep is a stage of high neuronal activity in which the brain can constantly monitor its surroundings and execute cognitive processing regardless of reduced consciousness. Anyone who has experienced sleep deprivation can relate to the detrimental effect of sleep loss on memory. However, despite reports of classical conditioning during sleep [1Arzi A. Shedlesky L. Ben-Shaul M. Nasser K. Oksenberg A. Hairston I.S. Sobel N. Humans can learn new information during sleep.Nat. Neurosci. 2012; 15: 1460-1465Crossref PubMed Scopus (149) Google Scholar, 2Andrillon T. Pressnitzer D. Léger D. Kouider S. Formation and suppression of acoustic memories during human sleep.Nat. Commun. 2017; 8: 179Crossref PubMed Scopus (45) Google Scholar], the possibility that the brain might be able to actively learn semantic information while in a state of slumber has been largely overlooked, since learning may require forms of top down processing which are absent during sleep. Excitingly, ideas on this topic are about to change. A new study by Züst et al. [3Züst M.A. Ruch S. Wiest R. Henke K. Implicit vocabulary learning during sleep is bound to slow-wave peaks.Curr. Biol. 2019; 29: 541-553Abstract Full Text Full Text PDF PubMed Scopus (34) Google Scholar] reported in a recent issue of Current Biology shows that semantic memories can, in fact, be freshly encoded during deep sleep. Sleep facilitates the integration of newly encoded material into more stable memories, so they can be retrieved after long periods of time or combined with other information to form semantic memories. Encoded information can be linked to external sensory cues which can then be used to trigger the reactivation of this learned material in subsequent sleep through a process called targeted memory reactivation (TMR) [4Belal S. Cousins J. El-Deredy W. Parkes L. Schneider J. Tsujimura H. Zoumpoulaki A. Perapoch M. Santamaria L. Lewis P. Identification of memory reactivation during sleep by EEG classification.Neuroimage. 2018; 176: 203-214Crossref PubMed Scopus (26) Google Scholar]. Substantial evidence supports a role for oscillatory brain activity in memory consolidation [5Schreiner T. Rasch B. The beneficial role of memory reactivation for language learning during sleep: a review.Brain Lang. 2017; 167: 94-105Crossref PubMed Scopus (39) Google Scholar]. Sleep EEG alternates between non-rapid eye movement (NREM), which is characterised by slow oscillations and sleep spindles, and rapid eye movement (REM), which is characterised by mixed frequency activity with sporadic theta bursts. Slow oscillations are high amplitude neocortical oscillations (0.5–3 Hz) which predominant during deep slow wave sleep and modulate faster oscillations. Sleep spindles are oscillatory bursts (12–15 Hz) with a thalamocortical origin that occur throughout stage 2 of NREM [6Staresina B.P. Ole Bergmann T. Bonnefond M. van der Meij R. Jensen O. Deuker L. Elger C.E. Axmacher N. Fell J. Hierarchical nesting of slow oscillations, spindles and ripples in the human hippocampus during sleep.Nat. Neurosci. 2015; 18: 1679-1686Crossref PubMed Scopus (382) Google Scholar]. The interplay between slow oscillations and spindles is thought to be the central machinery of memory consolidation, whereas cortical theta activity (4–8 Hz) is thought to mark reactivation of verbal material in NREM [5Schreiner T. Rasch B. The beneficial role of memory reactivation for language learning during sleep: a review.Brain Lang. 2017; 167: 94-105Crossref PubMed Scopus (39) Google Scholar] and enhanced memory processing in REM [7Boyce R. Williams S. Adamantidis A. REM sleep and memory.Curr. Opin. Neurobiol. 2017; 44: 167-177Crossref PubMed Scopus (64) Google Scholar]. Arguably, the potential to create new associations is reduced during slow wave sleep [8Peigneux P. Laureys S. Delbeuck X. Maquet P. Sleeping brain, learning brain. The role of sleep for memory systems.Neuroreport. 2001; 12: A111-A124Crossref PubMed Scopus (250) Google Scholar] because this sleep stage involves reduced levels of acetylcholine and synaptic potentiation, elements that are required for learning [9Gais S. Born J. Low acetylcholine during slow-wave sleep is critical for declarative memory consolidation.Proc. Natl. Acad. Sci. USA. 2004; 101: 2140-2144Crossref PubMed Scopus (325) Google Scholar, 10Timofeev I. Chauvette S. Sleep slow oscillation and plasticity.Curr. Opin. Neurobiol. 2017; 44: 116-126Crossref PubMed Scopus (66) Google Scholar]. Nevertheless, animal studies have shown that it is possible to create new spatial memories by stimulating the reward system in concert with the spiking of place cells (e.g., hippocampal neurons which respond to a particular spatial location) during sleep [11De Lavilléon G. Lacroix M. Rondi-Reig L. Benchenane K. Explicit memory creation during sleep: a causal role of place cell on navigation.Nat. Neurosci. 2013; 18: 1-39Google Scholar]. In humans, non-declarative learning can be achieved in sleep [1Arzi A. Shedlesky L. Ben-Shaul M. Nasser K. Oksenberg A. Hairston I.S. Sobel N. Humans can learn new information during sleep.Nat. Neurosci. 2012; 15: 1460-1465Crossref PubMed Scopus (149) Google Scholar, 2Andrillon T. Pressnitzer D. Léger D. Kouider S. Formation and suppression of acoustic memories during human sleep.Nat. Commun. 2017; 8: 179Crossref PubMed Scopus (45) Google Scholar], though success depends on the sleep stage in which stimuli are presented. Thus, auditory perceptual learning is inhibited when stimuli are presented in slow wave sleep but facilitated when they are presented in both shallower NREM and REM [2Andrillon T. Pressnitzer D. Léger D. Kouider S. Formation and suppression of acoustic memories during human sleep.Nat. Commun. 2017; 8: 179Crossref PubMed Scopus (45) Google Scholar]. Conversely, olfactory conditioning survived till the next morning when learned in NREM but not REM [1Arzi A. Shedlesky L. Ben-Shaul M. Nasser K. Oksenberg A. Hairston I.S. Sobel N. Humans can learn new information during sleep.Nat. Neurosci. 2012; 15: 1460-1465Crossref PubMed Scopus (149) Google Scholar], and implicit verbal information presented during sleep is positively related to slow wave activity [12Ruch S. Koenig T. Mathis J. Roth C. Henke K. Word encoding during sleep is suggested by correlations between word-evoked up-states and post-sleep semantic priming.Front. Psychol. 2014; 5: 1-14Crossref PubMed Scopus (11) Google Scholar]. In their new study, Züst et al. build on this non-declarative literature by showing that implicit semantic learning of verbal information is also possible during slow wave sleep, and more specifically, such learning only occurs when stimuli are presented at the peaks of the slow oscillations. To examine this, Züst and colleagues repeatedly presented a series of word–pseudoword pairs during deep NREM sleep. Upon awakening, participants were asked to identify whether each presented pseudoword represented an object that fits into a shoe box (e.g., for a stapler the response would be “yes”, while for a car the response would be “no”). Surprisingly, the participants were able to perform this task above chance, with discernible markers of hippocampal recall [3Züst M.A. Ruch S. Wiest R. Henke K. Implicit vocabulary learning during sleep is bound to slow-wave peaks.Curr. Biol. 2019; 29: 541-553Abstract Full Text Full Text PDF PubMed Scopus (34) Google Scholar]. Züst et al. show that implicit binding was established only when the second word of the pair was played on the peak of the subsequent slow oscillation on at least two occasions. Furthermore, binding only took place if these occasions occurred during intervals of decreased theta power. The authors conclude that the optimal timing for stimulus binding is at the peak of the slow oscillation with low theta activity. In their remarkable study, Züst et al. suggest that implicit binding in sleep is facilitated by periods of neural excitability during the peaks of slow oscillations (Figure 1A). Considering up-states as intervals of activated neural dynamics similar to wakefulness is not a new idea. Evidence from both in vitro and in vivo experiments indicates that wakefulness and deep-sleep up-states involve similar dynamics in terms of mechanisms for neural activation and network modulation in both cortical and thalamic areas [13Destexhe A. Hughes S.W. Rudolph M. Crunelli V. Are corticothalamic “up” states fragments of wakefulness?.Trends Neurosci. 2007; 30: 334-342Abstract Full Text Full Text PDF PubMed Scopus (251) Google Scholar]. Moreover, as the authors point out, up-states may represent periods of synaptic potentiation that could promote learning processes irrespective of the increased inhibition inherent in deep sleep [10Timofeev I. Chauvette S. Sleep slow oscillation and plasticity.Curr. Opin. Neurobiol. 2017; 44: 116-126Crossref PubMed Scopus (66) Google Scholar]. Now, the data from Züst et al. provide novel support for the idea that external inputs can be processed during these up-states, even though these periods are excluded from conscious awareness. However, more direct evidence is required to clarify this point. Thus, the work of Züst et al. will serve as a base for further hypothesis-driven examination of these interesting mini wake states in slow wave sleep. For instance, future studies could apply different stimuli during the peaks and troughs of slow oscillations in order to determine whether those applied at the peaks are really encoded better. Similarly, phase-targeted stimuli could be employed at the hippocampal level in animal experiments using the method from previous work [11De Lavilléon G. Lacroix M. Rondi-Reig L. Benchenane K. Explicit memory creation during sleep: a causal role of place cell on navigation.Nat. Neurosci. 2013; 18: 1-39Google Scholar]. Thus, place cells could be tagged using concurrent reward system stimulation, but this could be done at either the peak or the trough of cortical slow oscillations. Animals should subsequently prefer places associated with the cells which were rewarded in the peak phase. Züst et al. observe that a decrease in prefrontal theta power facilitates implicit verbal binding. They interpret this as a break in consolidation, as indexed by increased theta, which allows an opening for encoding to take place. In wake, encoding and recall are facilitated by the modulatory action of both sub-cortical and hippocampal theta [14Hanslmayr S. Staresina B.P. Bowman H. Oscillations and episodic memory: addressing the synchronization/desynchronization conundrum.Trends Neurosci. 2016; 39: 16-25Abstract Full Text Full Text PDF PubMed Scopus (201) Google Scholar], and changes in theta power are thought to coordinate language memory in all states of consciousness [5Schreiner T. Rasch B. The beneficial role of memory reactivation for language learning during sleep: a review.Brain Lang. 2017; 167: 94-105Crossref PubMed Scopus (39) Google Scholar]. However, the role of theta in memory consolidation during sleep is still very unclear. In interpreting the reduced theta as a break in consolidation, Züst et al. are building on a series of clever studies of vocabulary learning which have collectively to the suggestion that theta activity represents memory replay [5Schreiner T. Rasch B. The beneficial role of memory reactivation for language learning during sleep: a review.Brain Lang. 2017; 167: 94-105Crossref PubMed Scopus (39) Google Scholar]. Thus, in NREM sleep, TMR that elicits an increase in theta about 500 ms post cue at frontal electrodes leads to memory consolidation, while TMR that elicits no theta has no behavioural benefit [5Schreiner T. Rasch B. The beneficial role of memory reactivation for language learning during sleep: a review.Brain Lang. 2017; 167: 94-105Crossref PubMed Scopus (39) Google Scholar]. Furthermore, applying TMR stimuli too close together in time appears to prevent the theta response, and also removes the behavioural benefit of TMR [15Schreiner T. Lehmann M. Rasch B. Auditory feedback blocks memory benefits of cueing during sleep.Nat. Commun. 2015; 6: 8729Crossref PubMed Scopus (78) Google Scholar]. Finally, phase synchrony of cortical theta is conserved from TMR cued replay to retrieval [16Schreiner T. Doeller C.F. Jensen O. Rasch B. Staudigl T. Theta phase-coordinated memory reactivation reoccurs in a slow-oscillatory rhythm during NREM sleep.Cell Rep. 2018; : 296-301Abstract Full Text Full Text PDF PubMed Scopus (42) Google Scholar], suggesting that the phase pattern somehow actually represents learned information. Importantly, however, increased theta power is not commonly associated with memory consolidation in normal sleep which hasn’t been manipulated by TMR [17Rasch B. Born J. About sleep’s role in memory.Physiol. Rev. 2013; 93: 681-766Crossref PubMed Scopus (1437) Google Scholar], suggesting that these effects may relate to the presentation of auditory cues rather than to the memory task. After all, auditory stimuli during NREM sleep routinely elicit a theta response in frontal electrodes at about 500 ms post cue even when the stimulation has no meaning [18Papalambros N.A. Santostasi G. Malkani R.G. Braun R. Weintraub S. Paller K.A. Zee P.C. Acoustic enhancement of sleep slow oscillations and concomitant memory improvement in older adults.Front. Hum. Neurosci. 2017; 11: 1-14Crossref PubMed Scopus (133) Google Scholar, 19Ong J.L. Lo J.C. Chee N.I.Y.N. Santostasi G. Paller K.A. Zee P.C. Chee M.W.L.L. Effects of phase-locked acoustic stimulation during a nap on EEG spectra and declarative memory consolidation.Sleep Med. 2016; 20: 88-97Abstract Full Text Full Text PDF PubMed Scopus (94) Google Scholar, 20Cox R. Korjoukov I. de Boer M. Talamini L.M. Sound asleep: processing and retention of slow oscillation phase-targeted stimuli.PLoS One. 2014; 9: e101567Crossref PubMed Scopus (43) Google Scholar], and could thus not cue a memory replay. In the vocabulary studies, theta is consistently shown to increase for words that are better remembered after sleep [5Schreiner T. Rasch B. The beneficial role of memory reactivation for language learning during sleep: a review.Brain Lang. 2017; 167: 94-105Crossref PubMed Scopus (39) Google Scholar]. While entirely consistent with the idea that theta somehow marks replay which strengthens memories, this is also consistent with superior sensory processing for these successfully cued stimuli, as compared to stimuli for which memory is not enhanced by TMR, since cues cannot elicit replay if they are not processed. Following this line of thought, it may be worth considering an alternative interpretation of Züst et al.’s findings with respect to theta. Instead of representing a dip in consolidation, the reduced theta power which predicted successful encoding could represent a lull in the sensory reprocessing of prior stimuli, making the brain more receptive to incoming stimuli. Words presented during such a lull would be more likely to be detected and processed (Figure 1B). While tantalising, note that both this sensory processing interpretation and the consolidation-related interpretation suggested by Züst et al. are speculative. More work will be needed before we truly understand the role of theta oscillations during stimulus processing in sleep. The tight link between sleep and memory is undeniable, and the resurgent notion of learning while asleep is fascinating. Züst et al. make us question where the limits of the neural ability to acquire new information under deep states of unconsciousness actually lie, and why the brain has evolved to allow these specific phases of unconscious learning. We have just started to learn how to learn asleep, and many snoozes are still ahead to consolidate what we know and fully comprehend this brain function." @default.
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