How Memory Replay in Sleep Boosts Creative Problem-Solving

Lewis, Penelope A.; Knoblich, Günther; Poe, Gina R.

doi:10.1016/j.tics.2018.03.009

Cited by 143 publications

(126 citation statements)

References 76 publications

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“…Because our recordings began after animals had received considerable experience with the maze environment during the pre-training phase, we may have captured a set of operational demands unlike initial learning. To reconcile our finding of generalization with previous reports of orthogonalization, we propose that both mechanisms act on the organization of memory but at different timescales: orthogonalization dominates an early, fast encoding process which emphasizes the uniqueness of current experiences, while generalization acts as a slower refinement of existing memory representations by finding statistical regularities; both of these processes likely involve regions outside the hippocampus (Ghosh & Gilboa, 2013; Koster et al, 2018; Lewis, Knoblich, & Poe, 2018). This distinction suggests that it is more appropriate for our work to be framed in terms of long-term mechanisms of memory stability, rather than those which are relevant to shaping the initial learning and encoding process.…”

Section: Discussionsupporting

confidence: 70%

Hippocampal spatial memory representations in mice are heterogeneously stable

Levy

Kinsky

Mau

et al. 2019

Preprint

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The population of hippocampal neurons actively coding space continually changes across days as mice repeatedly perform tasks. Many hippocampal place cells become inactive while other previously silent neurons become active, challenging the belief that stable behaviors and memory representations are supported by stable patterns of neural activity. Active cell replacement may disambiguate unique episodes that contain overlapping memory cues, and could contribute to reorganization of memory representations. How active cell replacement affects the evolution of representations of different behaviors within a single task is unknown. We trained mice to perform a Delayed Non-Match to Place (DNMP) task over multiple weeks, and performed calcium imaging in area CA1 of the dorsal hippocampus using head-mounted miniature microscopes. Cells active on the central stem of the maze “split” their calcium activity according to the animal’s upcoming turn direction (left or right), the current task phase (study or test), or both task dimensions, even while spatial cues remained unchanged. We found that different splitter neuron populations were replaced at unequal rates, resulting in an increasing number of cells modulated by turn direction and a decreasing number of cells with combined modulation by both turn direction and task phase. Despite continual reorganization, the ensemble code stably segregated these task dimensions. These results show that hippocampal memories can heterogeneously reorganize even while behavior is unchanging.Significance statementSingle photon calcium imaging using head-mounted miniature microscopes in freely moving animals, has enabled researchers to measure the long term stability of hippocampal pyramidal cells during repeated behaviors. Previous studies have demonstrated instability of neural circuit components including dendritic spines and axonal boutons. It is now known that single units in the neuronal population exhibiting behaviorally relevant activity eventually become inactive and that previously silent neurons can quickly acquire task-relevant activity. The function of such population dynamics is unknown. We show here that population dynamics differ for cells coding distinct task dimensions, suggesting such dynamics are part of a mechanism for latent memory reorganization. These results add to a growing body of work showing that maintenance of episodic memory is an ongoing and dynamic process.

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Section: Discussionsupporting

confidence: 70%

Hippocampal spatial memory representations in mice are heterogeneously stable

Levy

Kinsky

Mau

et al. 2019

Preprint

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“…It is unclear how exactly those objectNEs jump up into activity. A common explanation is that objectNEs, primed by previous activity or current sensory or subcortical stimulation, activate spontaneously, triggered by the ponto-geniculo-occipital (PGO) waves that characterize REM sleep 29 . In the words of Hobson & McCarley, the neocortex is making "the best of a bad job in producing even partially coherent dream imagery from the relatively noisy signals sent up from the brain stem" 30 .…”

Section: Prefrontal Analysismentioning

confidence: 99%

Neuroscience of imagination and implications for human evolution

Vyshedskiy¹

2019

Preprint

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“…Statistical learning requires adequate consolidation and generalisation over time, a process known to be supported by sleep (Albouy, King, Maquet, & Doyon, 2013;Durrant et al, 2016;Durrant, Taylor, Cairney, & Lewis, 2011;Lewis, Knoblich, & Poe, 2018;Lutz, Wolf, Hubner, Born, & Rauss, 2018). Behaviourally, sleep strengthens predictive sequence coding (Lutz et al, 2018), including the acquisition and prediction of auditory statistical regularities (Durrant, Cairney, & Lewis, 2013;Durrant et al, 2016).…”

Section: Introductionmentioning

confidence: 99%

Slow oscillation-spindle coupling predicts sequence-based language learning

Cross

Helfrich

Corcoran

et al. 2020

Preprint

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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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How Memory Replay in Sleep Boosts Creative Problem-Solving

Cited by 143 publications

References 76 publications

Hippocampal spatial memory representations in mice are heterogeneously stable

Hippocampal spatial memory representations in mice are heterogeneously stable

Neuroscience of imagination and implications for human evolution

Slow oscillation-spindle coupling predicts sequence-based language learning

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