Phase‐amplitude coupling of sleep slow oscillatory and spindle activity correlates with overnight memory consolidation

Mikutta, Christian; Feige, Bernd; Maier, Jonathan G.; Hertenstein, Elisabeth; Holz, Johannes; Riemann, Dieter; Nissen, Christoph

doi:10.1111/jsr.12835

Cited by 73 publications

(99 citation statements)

References 19 publications

(36 reference statements)

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“…Recent work highlights an inherently coupled, hierarchical organization of brain oscillatory activity during sleep (cross-frequency coupling). For instance, recent studies corroborate the notion that the phase-amplitude coupling of sleep slow waves and sleep spindles serve critical functions of sleep, such as memory consolidation [53] and changes in neural plasticity [54,55]. Our own unpublished data suggest an attenuation of phase-amplitude coupling in patients with in-somnia compared to controls, which might relate to the perception of nonrestorative sleep.…”

Section: Insomniasupporting

confidence: 81%

Targeting Arousal and Sleep through Noninvasive Brain Stimulation to Improve Mental Health

et al. 2020

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Arousal and sleep represent fundamental physiological domains, and alterations in the form of insomnia (difficulty falling or staying asleep) or hypersomnia (increased propensity for falling asleep or increased sleep duration) are prevalent clinical problems. Current first-line treatments include psychotherapy and pharmacotherapy. Despite significant success, a number of patients do not benefit sufficiently. Progress is limited by an incomplete understanding of the neurobiology of insomnia and hypersomnia. This work summarizes current concepts of the regulation of arousal and sleep and its modulation through noninvasive brain stimulation (NIBS), including transcranial magnetic, current, and auditory stimulation. Particularly, we suggest: (1) characterization of patients with sleep problems -across diagnostic entities of mental disorders -based on specific alterations of sleep, including alterations of sleep slow waves, sleep spindles, cross-frequency coupling of brain oscillations, local sleep-wake regulation, and REM sleep and (2) targeting these with specific NIBS techniques. While evidence is accumulating that the modulation of specific alterations of sleep through NIBS is feasible, it remains to be tested whether this translates to clinically relevant effects and new treatment developments.

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Section: Insomniasupporting

confidence: 81%

Targeting Arousal and Sleep through Noninvasive Brain Stimulation to Improve Mental Health

et al. 2020

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“…Then we filtered the same trials between 12 -16 Hz and extracted the instantaneous amplitude from the Hilbert transform. For every participant at channel C4 (selection based on Helfrich et al, 2018 andMikutta et al, 2019) and epoch, we detected the maximal sleep spindle amplitude and corresponding SO phase angle. The mean circular direction (phase) and resultant vector length (coupling strength) across all NREM events were determined using the CircStat toolbox in MATLAB (Berens, 2009).…”

Section: Sleep Parameters and Sleep Eeg Analysesmentioning

confidence: 99%

“…"Behavioural Results" can be explained by correlates of sleep-related memory consolidation. Based on recent research (e.g., Helfrich et al, 2018;Holz et al, 2012;Mikutta et al, 2019), we focussed on two cardinal markers of sleep-related memory consolidation: (1) the coupling strength between maximal spindle amplitude and the phase of the slow oscillation, and (2) spindle onset relative to the phase of the SO. While Phase did not significantly predict changes in behavioural performance across sleep (Phase x Type x Grammatically: χ2(1) = .13, p = .71), there was a significant Coupling x Type x Grammatically interaction on behavioural difference scores (χ2(1) = 4.97, p = .02); see Figure 5A and 5B for the preferred spindle onset to SO phase and phase of SO of maximal spindle amplitude, respectively).…”

Section: Associations Between Nrem Neurophysiology and Memory Retentionmentioning

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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“…Contrary to our SWS time finding, the amount of slow oscillation-spindle coupling was negatively correlated with memory in the stress group. This suggests that coupling impairs memory following stress, rather than promote it as is typically found for non-stressed participants and neutral memories (Mikutta et al, 2019;Niknazar et al, 2015). These effects were stronger for emotional items compared to neutral ones, suggesting that stress and SWS coupling may interact to impede the consolidation of emotional memories to a greater extent than neutral memories.…”

Section: Discussionmentioning

confidence: 76%

“…In humans, this coordination has been demonstrated in epilepsy patients with intracranial hippocampal recordings (Staresina et al, 2015). Although hippocampal ripples cannot be detected non-invasively, slow oscillation-spindle coupling as detected via scalp EEG has been associated with memory consolidation in healthy humans (Denis et al, 2020;Mikutta et al, 2019;Niknazar et al, 2015;Zhang et al, 2020).…”

Section: Introductionmentioning

confidence: 98%

Slow oscillation-spindle coupling is negatively associated with emotional memory formation following stress

Denis

Kim

Kark

et al. 2020

Preprint

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Sleep and stress have both been shown to enhance emotional memory consolidation. They also interact, with the largest benefit of sleep on emotional memory being seen when stress occurs either shortly before or after memory encoding. Slow wave sleep (SWS) is believed to be critical for episodic memory consolidation, facilitated by the coupling of slow oscillations and sleep spindles. However, prior work in humans has only demonstrated slow oscillation-spindle coupling to be associated with consolidation of neutral information in non-stressed participants.Whether coupling interacts with stress to facilitate emotional memory consolidation is unknown.To address this exploratory question, we reanalyzed an existing dataset of N=64 individuals.Participants underwent a psychosocial stressor (n=32) or comparable control (n=32) prior to the encoding of 150 line drawings of neutral, positive, and negative images. All participants then slept overnight with polysomnographic recordings. The next day, they were given a surprise memory test. In the stress group, percentage of time spent in SWS was positively correlated with memory for images of all valences (all r>.35, p<.043). Results were primarily driven by those who showed a high cortisol response to the stressor (all r>.65, p<.007), compared to low cortisol responders (all r<.31, all p>.25). However, the amount of slow oscillation-spindle coupling during SWS was negatively associated with neutral (r=-.45, p=.01) and emotional (r=-.66, p<.001) memory in the stress group. The negative association with emotional memory was significantly stronger than for neutral memory (Meng z=2.04, p=.04). Between stress and control groups, there were no differences in any of the sleep measures assessed. These results highlight the importance of considering sleep microarchitecture events in addition to overall sleep stage time and suggests that stress may alter the relationship between SWS and memory consolidation.

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Phase‐amplitude coupling of sleep slow oscillatory and spindle activity correlates with overnight memory consolidation

Cited by 73 publications

References 19 publications

Targeting Arousal and Sleep through Noninvasive Brain Stimulation to Improve Mental Health

Targeting Arousal and Sleep through Noninvasive Brain Stimulation to Improve Mental Health

Slow oscillation-spindle coupling predicts sequence-based language learning

Slow oscillation-spindle coupling is negatively associated with emotional memory formation following stress

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