Neuronal Oscillations Indicate Sleep-dependent Changes in the Cortical Memory Trace

Köster, Moritz; Finger, Holger; Kater, Maren-Jo; Schenk, Christoph; Gruber, Thomas

doi:10.1162/jocn_a_01071

Cited by 9 publications

(8 citation statements)

References 53 publications

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“…In a second step, to further scrutinize the differences between incidental and intentional encoding, we focused on frontal and posterior electrode clusters. This was due to the close correspondence of grand mean topographies of theta and alpha activation across age groups (see Fig 3 ) and to the frontal and posterior alpha and theta networks identified in previous assessments with students [ 19 , 27 , 47 ]. Specifically, we entered the average signals over the electrodes of all frontal and posterior clusters and entered these into a Cluster (frontal, posterior), Condition (incidental, intentional) and Age Group (adults, older and younger children) ANOVA.…”

Section: Methodssupporting

confidence: 59%

Neuronal oscillations reveal the processes underlying intentional compared to incidental learning in children and young adults

2017

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This EEG study investigated the neuronal processes during intentional compared to incidental learning in young adults and two groups of children aged 10 and 7 years. Theta (3–8 Hz) and alpha (10–16 Hz) neuronal oscillations were analyzed to compare encoding processes during an intentional and an incidental encoding task. In all three age groups, both encoding conditions were associated with an increase in event-related theta activity. Encoding-related alpha suppression increased with age. Memory performance was higher in the intentional compared to the incidental task in all age groups. Furthermore, intentional learning was associated with an improved encoding of perceptual features, which were relevant for the retrieval phase. Theta activity increased from incidental to intentional encoding. Specifically, frontal theta increased in all age groups, while parietal theta increased only in adults and older children. In younger children, parietal theta was similarly high in both encoding phases. While alpha suppression may reflect semantic processes during encoding, increased theta activity during intentional encoding may indicate perceptual binding processes, in accordance with the demands of the encoding task. Higher encoding-related alpha suppression in the older age groups, together with age differences in parietal theta activity during incidental learning in young children, is in line with recent theoretical accounts, emphasizing the role of perceptual processes in mnemonic processing in young children, whereas semantic encoding processes continue to mature throughout middle childhood.

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Section: Methodssupporting

confidence: 59%

Neuronal oscillations reveal the processes underlying intentional compared to incidental learning in children and young adults

2017

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“…For beta, we selected an anterior-central and anterior-left electrode cluster (FC1/FC2/Fz/F4/FC6/F8), which has been reported as a significant ROI for beta activity during higher-order language tasks (i.e., Bastiaansen & Hagoort, 2015;de Diego-Balaguer et al, 2011;Kepinska, Pereda, et al, 2017). Finally, a central-left electrode cluster (T7/CP5/C3/CP1/Cz/CP2) was chosen for the theta band based on studies reporting sleeprelated memory effects (Koster, Finger, Kater, Schenk, & Gruber, 2016), as well as memoryrelated computations during language processing (Kielar et al, 2014;Meyer et al, 2015).…”

Section: Discussionmentioning

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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“…The present paper is a companion paper of a sleep study 32 . Thus, the memory for half of the stimuli was tests before, the other half after a three hour interval (i.e., after a sleep or wake interval of the sleep study).…”

Section: Methodsmentioning

confidence: 99%

“…At least 18 trials remained for each condition of each participant and thus all remaining participants were included in the final analyses. Furthermore, we applied a correction of saccade-related transient potentials 36 , used in several previous publications 25 , 32 , 36 to remove miniature eye-movement artifacts 37 . Due to artifact correction procedures approximately 10% of the original trials were removed.…”

Section: Methodsmentioning

confidence: 99%

“…To account for the variability in frequency bands across individuals 21 , we identified the peak theta, alpha and gamma frequencies, individually for each subject, based on the mean spectral activity across all encoding conditions 11 , 25 , 32 . This resulted in (Mean ± SD ): 3.8 Hz ± 0.8 Hz theta frequencies, 9.8 Hz ± 2.2 Hz alpha frequencies and 57.3 Hz ± 10.2 Hz gamma frequencies.…”

Section: Methodsmentioning

confidence: 99%

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Theta-gamma coupling binds visual perceptual features in an associative memory task

Köster

Finger

Graetz

et al. 2018

Sci Rep

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It is an integral function of the human brain to sample novel information from the environment and to integrate them into existing representations. Recent evidence suggests a specific role for the theta rhythm (4–8 Hz) in mnemonic processes and the coupling between the theta and the gamma rhythm (40–120 Hz) in ordering and binding perceptual features during encoding. Furthermore, decreases in the alpha rhythm (8–12 Hz) are assumed to gate perceptual information processes in semantic networks. In the present study, we used an associative memory task (object-color combinations) with pictures versus words as stimuli (high versus low visual information) to separate associative memory from visual perceptual processes during memory formation. We found increased theta power for later remembered versus later forgotten items (independent of the color judgement) and an increase in phase-amplitude coupling between frontal theta and fronto-temporal gamma oscillations, specific for the formation of picture-color associations. Furthermore, parietal alpha suppression and gamma power were higher for pictures compared to words. These findings support the idea of a theta-gamma code in binding visual perceptual features during encoding. Furthermore, alpha suppression likely reflects perceptual gating processes in semantic networks and is insensitive to mnemonic and associative binding processes. Gamma oscillations may promote visual perceptual information in visual cortical networks, which is integrated into existing representations by prefrontal control processes, working at a theta pace.

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Neuronal Oscillations Indicate Sleep-dependent Changes in the Cortical Memory Trace

Cited by 9 publications

References 53 publications

Neuronal oscillations reveal the processes underlying intentional compared to incidental learning in children and young adults

Neuronal oscillations reveal the processes underlying intentional compared to incidental learning in children and young adults

Slow oscillation-spindle coupling predicts sequence-based language learning

Theta-gamma coupling binds visual perceptual features in an associative memory task

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