Triangular Relationship between Sleep Spindle Activity, General Cognitive Ability and the Efficiency of Declarative Learning

Lustenberger, Caroline; Maric, Angelina; Dürr, Roland; Achermann, Peter; Huber, Reto

doi:10.1371/journal.pone.0049561

Cited by 64 publications

(58 citation statements)

References 36 publications

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“…Furthermore, the degree of encoding restoration positively correlated with the duration of Stage 2 NREM sleep as well as the number of corresponding fast (13.5 – 15 Hz) sleep spindles over the left prefrontal cortex. Similar learning-related spindle associations have recently been reported across a full night of sleep [89]. Adding to the suggestion that NREM sleep aids in the restoration of encoding, prefrontal electrical stimulation targeting the enhancement of NREM slow wave activity also increases subsequent post-awakening episodic memory encoding ability [90].…”

Section: Sleep and Memory Processing In The Human Brainsupporting

confidence: 53%

Sleep, Plasticity and Memory from Molecules to Whole-Brain Networks

et al. 2013

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Despite the ubiquity of sleep across phylogeny, its function remains elusive. In this review, we consider one compelling candidate: brain plasticity associated with memory processing. Focusing largely on hippocampus-dependent memory in rodents and humans, we describe molecular, cellular, network, whole-brain and behavioral evidence establishing a role for sleep both in preparation for initial memory encoding, and in the subsequent offline consolidation ofmemory. Sleep and sleep deprivation bidirectionally alter molecular signaling pathways that regulate synaptic strength and control plasticity-related gene transcription and protein translation. At the cellular level, sleep deprivation impairs cellular excitability necessary for inducing synaptic potentiation and accelerates the decay of long-lasting forms of synaptic plasticity. In contrast, NREM and REM sleep enhance previously induced synaptic potentiation, although synaptic de-potentiation during sleep has also been observed. Beyond single cell dynamics, large-scale cell ensembles express coordinated replay of prior learning-related firing patterns during subsequent sleep. This occurs in the hippocampus, in the cortex, and between the hippocampus and cortex, commonly in association with specific NREM sleep oscillations. At the whole-brain level, somewhat analogous learning-associated hippocampal (re)activation during NREM sleep has been reported in humans. Moreover, the same cortical NREM oscillations associated with replay in rodents also promote human hippocampal memory consolidation, and this process can be manipulated using exogenous reactivation cues during sleep. Mirroring molecular findings in rodents, specific NREM sleep oscillations before encoding refresh human hippocampal learning capacity, while deprivation of sleep conversely impairs subsequent hippocampal activity and associated encoding. Together, these cross-descriptive level findings demonstrate that the unique neurobiology of sleep exert powerful effects on molecular, cellular and network mechanism of plasticity that govern both initial learning and subsequent long-term memory consolidation.

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Section: Sleep and Memory Processing In The Human Brainsupporting

confidence: 53%

Sleep, Plasticity and Memory from Molecules to Whole-Brain Networks

et al. 2013

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“…In the absence of a causal link, it also remains a matter of debate whether spindles per se are important for learning, or whether spindling propensity merely reflects the efficiency and the connectivity of the TC system. A recent report, for example, states that the subjective spindle profile only provides an indirect measure of the cognitive and encoding performance during the learning phase, but is not decisive for sleep-dependent consolidation [98]. This interpretation is consistent 1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25 26 27 28 29 30 31 32 33 34 35 36 37 38 39 40 41 42 43 44 45 46 47 48 49 50 51 52 53 54 55 56 57 58 59 60 61 62 63 64 65 15 with two related observations.…”

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confidence: 99%

Manipulating sleep spindles – expanding views on sleep, memory, and disease

Astori

Wimmer²,

Lüthi³

2013

Trends in Neurosciences

128

113

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Abstract:Sleep spindles are distinctive electroencephalographic (EEG) oscillations emerging during non-rapid-eye-movement sleep (NREMS) that have been implicated in multiple brain functions, including sleep quality, sensory gating, learning and memory. Despite considerable knowledge about the mechanisms underlying these neuronal rhythms, their function remains poorly understood and current views are largely based on correlational evidence. Here, we review recent studies in humans and rodents that have begun to broaden our understanding of the role of spindles in the normal and disordered brain. We show that newly identified molecular substrates of spindle oscillations, in combination with evolving technological progress, offer novel targets and tools to selectively manipulate spindles and dissect their role in sleep-dependent processes. Powered by Editorial Manager® and ProduXion Manager® from Aries Systems CorporationAstori et al. Highlights Newly recognized ion channel subtypes generating spindle rhythms are described. The contribution of spindles to arousal threshold and sleep quality is discussed. The proposed role of spindles in memory consolidation is examined. A function of thalamic spindles in neural development is suggested. 1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25 26 27 28 29 30 31 32 33 34 35 36 37 38 39 40 41 42 43 44 45 46 47 48 49 50 51 52 53 54 55 56 57 58 59 60 61 62 63 64 1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25 26 27 28 29 30 31 32 33 34 35 36 37 38 39 40 41 42 43 44 45 46 47 48 49 50 51 52 53 54 55 56 57 58 59 60 61 62 63 64 65 4 Previous excellent reviews have thoroughly described cellular and network bases of spindle generation [3,6,7]. Here, we first review recent work on genetic models that has expanded the mechanistic understanding of this EEG rhythm through the modification of novel molecular substrates. We then discuss the current views about the functional aspects of spindles in brain physiology and pathology, as obtained from studies in naturally sleeping animals and humans. We highlight studies indicating that spindles are accessible for selective interventions, and that, with emerging technologies, will open avenues to decipher spindle function. Novel molecular aspects of spindle generationSleep spindles emerge from a limited set of cellular participants: the resonating core of these waxing-and-waning oscillations resides in the nRt-TC loop, which sustains repetitive burst discharges of its cellular components under the control of cortical inputs (Figure 1 Another important factor in the generation and maintenance of reticular intrinsic oscillations is the aforementioned SK2 or Kcnn2 channel. The vigorous Ca 2+ influx in nRt dendrites originating from Ca V 3.3 channels gates SK2 channels, thereby creating a burstafterhyperpolarization (bAHP) [12,19]. As T channels recover partially from inactivation duri...

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“…Together, these findings suggest that spindles strengthen synapses to consolidate memory during sleep. There is also mounting evidence of a more general role for spindles in cognition based on their correlations with learning ability and IQ (61-63), relationships that may be mediated by memory enhancement.…”

Section: Sleep Spindles Mediate Memory Consolidationmentioning

confidence: 99%

Reduced Sleep Spindles in Schizophrenia: A Treatable Endophenotype That Links Risk Genes to Impaired Cognition?

Manoach

Pan

Purcell

et al. 2016

Biological Psychiatry

184

155

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Although schizophrenia is defined by waking phenomena, abnormal sleep is a common feature. In particular, there is accumulating evidence of a sleep spindle deficit. Sleep spindles, a defining thalamocortical oscillation of non-rapid eye movement Stage 2 sleep, correlate with IQ and are thought to promote long-term potentiation and enhance memory consolidation. Here we review evidence that reduced spindle activity in schizophrenia is an endophenotype that impairs sleep-dependent memory consolidation, contributes to symptoms and is a novel treatment biomarker. Studies showing that spindles can be pharmacologically enhanced in schizophrenia and that increasing spindles improves memory in healthy individuals suggest that treating spindle deficits in schizophrenia may improve cognition. Spindle activity is highly heritable and recent large-scale genome-wide association studies have identified schizophrenia risk genes that may contribute to spindle deficits and illuminate their mechanisms. For example, the schizophrenia risk gene CACNA1I encodes a calcium channel that is abundantly expressed in the thalamic spindle generator and plays a critical role in spindle activity in a mouse knockout. Future genetic studies of animals and humans can delineate the role of this and other genes in spindles. Such cross-disciplinary research, by forging empirical links in causal chains from risk genes to proteins and cellular functions, through to endophenotypes, cognitive impairments, symptoms and diagnosis, has the potential to advance the mechanistic understanding, treatment and prevention of schizophrenia. This review highlights the importance of deficient sleep-dependent memory consolidation among the cognitive deficits of schizophrenia and implicates reduced sleep spindles as a potentially treatable mechanism.

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Triangular Relationship between Sleep Spindle Activity, General Cognitive Ability and the Efficiency of Declarative Learning

Cited by 64 publications

References 36 publications

Sleep, Plasticity and Memory from Molecules to Whole-Brain Networks

Sleep, Plasticity and Memory from Molecules to Whole-Brain Networks

Manipulating sleep spindles – expanding views on sleep, memory, and disease

Reduced Sleep Spindles in Schizophrenia: A Treatable Endophenotype That Links Risk Genes to Impaired Cognition?

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