Local coupling between sleep spindles and slow oscillations supports the stabilization of motor memories

Solano, Agustín; Riquelme, Luis A.; Pérez-Chada, Daniel; Della‐Maggiore, Valeria

doi:10.1101/2020.08.24.264697

Cited by 5 publications

(2 citation statements)

References 102 publications

(150 reference statements)

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“…Sleep-related memory effects are proposed to be biased toward stimuli following temporal or sequence-based regularities compared to relational information (for review, see Lerner and Gluck 2019). This is posited to occur via the hippocampal complex encoding temporal occurrences of sensory input (Durrant et al 2011), which are replayed during SWS, potentially via SO-spindle coupling (e.g., Navarrete et al 2020; Solano et al 2020). Here, we provide evidence supporting this account.…”

Section: Discussionmentioning

confidence: 99%

Slow oscillation-spindle coupling predicts sequence-based language learning

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Helfrich

Corcoran

et al. 2020

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word count: 174 Introduction word count: 1,756 Discussion word count: 2,677ABSTRACT Language is one of the most defining human capabilities, involving the coordination of brain networks that generalise the meaning of linguistic units of varying complexity. On a neural level, neocortical slow waves and thalamic spindles during sleep facilitate the reactivation of newly encoded memory traces, manifesting in distinct oscillatory activity during retrieval. However, it is currently unknown if the effect of sleep on memory extends to the generalisation of the mechanisms that subserve sentence comprehension. We address this question by analysing electroencephalogram data recorded from 36 participants during an artificial language learning task and an 8hr nocturnal sleep period. We found that a period of sleep was associated with increased alpha/beta synchronisation and improved behavioural performance. Cross-frequency coupling analyses also revealed that spindle-slow wave coupling predicted the consolidation of varying word order permutations, which was associated with distinct patterns of task-related oscillatory activity during sentence processing. Taken together, this study presents converging behavioural and neurophysiological evidence for a role of sleep in the consolidation of higher order language learning and associated oscillatory neuronal activity.Keywords: Sleep and memory; language learning; modified miniature language; sentence processing; neuronal oscillations SIGNIFICANCE STATEMENTThe endogenous temporal coordination of neural oscillations supports information processing during both wake and sleep states. Here we demonstrate that spindle-slow wave coupling during non-rapid eye movement sleep predicts the consolidation of complex grammatical rules and modulates task-related oscillatory dynamics previously implicated in sentence processing. We show that increases in alpha/beta synchronisation predict enhanced sensitivity to grammatical violations after a period of sleep and strong spindle-slow wave coupling modulates subsequent task-related theta activity to influence behaviour. Our findings reveal a complex interaction between both wake-and sleep-related oscillatory dynamics during the early stages of language learning beyond the single word level.

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Section: Discussionmentioning

confidence: 99%

Slow oscillation-spindle coupling predicts sequence-based language learning

Cross

Helfrich

Corcoran

et al. 2020

Preprint

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“…Overall, this is in line with the existing literature that the prioritization of emotional memory during sleep is more of an exception than the norm ( Prehn-Kristensen et al, 2009 , 2013 ; Baran et al, 2012 ; Morgenthaler et al, 2014 ; Göder et al, 2015 ; Bolinger et al, 2018 ; Kurz et al, 2019 ; Davidson et al, 2021 ). Additionally, previous studies indicate that the proportion of rapid eye movement sleep and slow-wave sleep ( Cairney et al, 2015 ) and the local coupling between sleep spindles and slow oscillations ( Solano et al, 2021 ) both play crucial roles in memory consolidation. Future research with polysomnography-monitored sleep data is needed to investigate how different aspects of sleep architecture may facilitate age-related shifts in positive memory bias.…”

Section: Discussionmentioning

confidence: 99%

Age-related positivity effect in emotional memory consolidation from middle age to late adulthood

Niu,

Utayde,

Sanders

et al. 2024

Front. Behav. Neurosci.

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BackgroundWhile younger adults are more likely to attend to, process, and remember negative relative to positive information, healthy older adults show the opposite pattern. The current study evaluates when, exactly, this positivity shift begins, and how it influences memory performance for positive, negative, and neutral information.MethodsA total of 274 healthy early middle-aged (35–47), late middle-aged (48–59), and older adults (>59) viewed scenes consisting of a negative, positive, or a neutral object placed on a plausible neutral background, and rated each scene for its valence and arousal. After 12 h spanning a night of sleep (n = 137) or a day of wakefulness (n = 137), participants completed an unexpected memory test during which they were shown objects and backgrounds separately and indicated whether the scene component was the “same,” “similar,” or “new” to what they viewed during the study session.Results and conclusionsWe found that both late middle-aged and older adults rated positive and neutral scenes more positively compared to early middle-aged adults. However, only older adults showed better memory for positive objects relative to negative objects, and a greater positive memory trade-off magnitude (i.e., remembering positive objects at the cost of their associated neutral backgrounds) than negative memory trade-off magnitude (i.e., remembering negative objects at the cost of their associated neutral backgrounds). Our findings suggest that while the positivity bias may not emerge in memory until older adulthood, a shift toward positivity in terms of processing may begin in middle age.

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Sequence-specific delayed gains in motor fluency evolve after movement observation training in the absence of early sleep

Maaravi-Hesseg,

Cohen,

Karni

2024

Sci Rep

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Following physical practice, delayed, consolidation-phase, gains in the performance of the trained finger-to-thumb opposition sequence (FOS) can be expressed, in young adults, only after a sleep interval is afforded. These delayed gains are order-of-movements specific. However, in several perceptual learning tasks, time post-learning, rather than an interval of sleep, may suffice for the expression of delayed performance gains. Here we tested whether the affordance of a sleep interval is necessary for the expression of delayed performance gains after FOS training by repeated observation. Participants were trained by observing videos displaying a left hand repeatedly performing a 5-element FOS. To assess post-session observation-related learning and delayed gains participants were tested in performing the observed (trained) and an unobserved (new, the 5-elements mirror-reversed) FOS sequences. Repeated observation of a FOS conferred no advantage to its performance, compared to the unobserved FOS, immediately after practice. However, a clear advantage for the observed FOS emerged by 12 h post-training, irrespective of whether this interval included sleep or not; the largest gains appeared by 24 h post-training. These results indicate that time-dependent, offline consolidation processes take place after observation training even in the absence of sleep; akin to perceptual learning rather than physical FOS practice.

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Local coupling between sleep spindles and slow oscillations supports the stabilization of motor memories

Cited by 5 publications

References 102 publications

Slow oscillation-spindle coupling predicts sequence-based language learning

Slow oscillation-spindle coupling predicts sequence-based language learning

Age-related positivity effect in emotional memory consolidation from middle age to late adulthood

Sequence-specific delayed gains in motor fluency evolve after movement observation training in the absence of early sleep

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