Targeted memory reactivation during sleep elicits neural signals related to learning content (original) (raw)
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Identification of memory reactivation during sleep by EEG classification
NeuroImage, 2018
Memory reactivation during sleep is critical for consolidation, but also extremely difficult to measure as it is subtle, distributed and temporally unpredictable. This article reports a novel method for detecting such reactivation in standard sleep recordings. During learning, participants produced a complex sequence of finger presses, with each finger cued by a distinct audio-visual stimulus. Auditory cues were then re-played during subsequent sleep to trigger neural reactivation through a method known as targeted memory reactivation (TMR). Next, we used electroencephalography data from the learning session to train a machine learning classifier, and then applied this classifier to sleep data to determine how successfully each tone had elicited memory reactivation. Neural reactivation was classified above chance in all participants when TMR was applied in SWS, and in 5 of the 14 participants to whom TMR was applied in N2. Classification success reduced across numerous repetitions o...
Cortical reactivations during sleep spindles following declarative learning
NeuroImage, 2019
Increasing evidence suggests that sleep spindles are involved in memory consolidation, but few studies have investigated the effects of learning on brain responses associated with spindles in humans. Here we used simultaneous electroencephalography (EEG) and functional magnetic resonance imaging (fMRI) during sleep to assess haemodynamic brain responses related to spindles after learning. Twenty young healthy participants were scanned with EEG/fMRI during (i) a declarative memory face sequence learning task, (ii) subsequent sleep, and (iii) recall after sleep (learning night). As a control condition an identical EEG/fMRI scanning protocol was performed after participants over-learned the face sequence task to complete mastery (control night). Results demonstrated increased responses in the fusiform gyrus both during encoding before sleep and during successful recall after sleep, in the learning night compared to the control night. During sleep, a larger response in the fusiform gyrus was observed in the presence of fast spindles during the learning as compared to the control night. Our findings support a cortical reactivation during fast spindles of brain regions previously involved in declarative learning and subsequently activated during memory recall, thereby promoting the cortical consolidation of memory traces.
Decoding material-specific memory reprocessing during sleep in humans
Neuronal learning activity is reactivated during sleep but the dynamics of this reactivation in humans are still poorly understood. Here we use multivariate pattern classification to decode electrical brain activity during sleep and determine what type of images participants had viewed in a preceding learning session. We find significant patterns of learning-related processing during rapid eye movement (REM) and non-REM (NREM) sleep, which are generalizable across subjects. This processing occurs in a cyclic fashion during time windows congruous to critical periods of synaptic plasticity. Its spatial distribution over the scalp and relevant frequencies differ between NREM and REM sleep. Moreover, only the strength of reprocessing in slow-wave sleep influenced later memory performance, speaking for at least two distinct underlying mechanisms between these states. We thus show that memory reprocessing occurs in both NREM and REM sleep in humans and that it pertains to different aspects of the consolidation process.
Encoding difficulty promotes postlearning changes in sleep spindle activity during napping
The Journal of …, 2006
Here, we investigated experience-dependent changes in daytime sleep EEG activity after declarative learning of unrelated word pairs. At weekly intervals, 13 young male volunteers spent three 24 h sessions in the laboratory under carefully controlled homeostatic and circadian conditions. At approximately midday, subjects performed either one of two word-pair learning tasks or a matched nonlearning control task, in a counterbalanced order. The two learning lists differed in the level of concreteness of the words used, resulting in an easier and a more difficult associative encoding condition, as confirmed by performance at immediate cued recall. Subjects were then allowed to sleep for 4 h; afterward, delayed cued recall was tested. Compared with the control condition, sleep EEG spectral activity in the low spindle frequency range and the density of low-frequency sleep spindles (11.25-13.75 Hz) were both significantly increased in the left frontal cortex after the difficult but not after the easy encoding condition. Furthermore, we found positive correlations between these EEG changes during sleep and changes in memory performance between pre-nap and post-nap recall sessions. These results indicate that, like during nocturnal sleep, daytime sleep EEG oscillations including spindle activity are modified after declarative learning of word pairs. Furthermore, we demonstrate here that the nature of the learning material is a determinant factor for sleep-related alterations after declarative learning.
Human accomplishments depend on learning, and effective learning depends on consolidation. Consolidation is the process whereby new memories are gradually stored in an enduring way in the brain so that they can be available when needed. For factual or event knowledge, consolidation is thought to progress during sleep as well as during waking states, and to be mediated by interactions between hippocampal and neocortical networks. However, consolidation is difficult to observe directly, but rather is inferred through behavioral observations. Here, we investigated overnight memory change by measuring electrical activity in and near the hippocampus. Electroencephalographic (EEG) recordings were made in five patients from electrodes implanted to determine whether a surgical treatment could relieve their seizure disorders. One night, while each patient slept in a hospital monitoring room, we recorded electrophysiological responses to 10-20 specific sounds that were presented very quietly,...
Sleep Spindle Refractoriness Segregates Periods of Memory Reactivation
Current Biology, 2018
Highlights d Reactivating memories with auditory cues during sleep benefited retention d Sleep spindle power increased after cues and predicted subsequent memory d Cue efficacy was impaired when cues fell within the spindle refractory period d The importance of spindle timing was confirmed using realtime spindle tracking
Memory Consolidation Is Linked to Spindle-Mediated Information Processing during Sleep
Highlights d We cued memory reactivation in sleep to investigate the functional role of spindles d Memory cueing bolstered retrieval performance the following day d Relative to control stimuli, memory cues evoked a surge in fast spindle activity d Memory content could be reliably decoded during this spindle increase In Brief Sleep spindles play a crucial role in memory consolidation, but the underlying mechanisms are not well understood. Using an auditory memory-cueing technique and EEG analysis in humans, Cairney et al. show that sleep spindles mediate the informational content of reactivated memory traces in service of offline mnemonic processing.
Memory reactivation and consolidation during sleep
Learning & Memory, 2004
Do our memories remain static during sleep, or do they change? We argue here that memory change is not only a natural result of sleep cognition, but further, that such change constitutes a fundamental characteristic of declarative memories. In general, declarative memories change due to retrieval events at various times after initial learning and due to the formation and elaboration of associations with other memories, including memories formed after the initial learning episode. We propose that declarative memories change both during waking and during sleep, and that such change contributes to enhancing binding of the distinct representational components of some memories, and thus to a gradual process of cross-cortical consolidation. As a result of this special form of consolidation, declarative memories can become more cohesive and also more thoroughly integrated with other stored information. Further benefits of this memory reprocessing can include developing complex networks of interrelated memories, aligning memories with long-term strategies and goals, and generating insights based on novel combinations of memory fragments. A variety of research findings are consistent with the hypothesis that cross-cortical consolidation can progress during sleep, although further support is needed, and we suggest some potentially fruitful research directions. Determining how processing during sleep can facilitate memory storage will be an exciting focus of research in the coming years.
Memory stabilization with targeted reactivation during human slow-wave sleep
Proceedings of the National Academy of Sciences, 2012
It is believed that neural representations of recent experiences become reactivated during sleep, and that this process serves to stabilize associated memories in long-term memory. Here, we initiated this reactivation process for specific memories during slow-wave sleep. Participants studied 50 object-location associations with object-related sounds presented concurrently. For half of the associations, the related sounds were re-presented during subsequent slow-wave sleep while participants underwent functional MRI. Compared with control sounds, related sounds were associated with increased activation of right parahippocampal cortex. Postsleep memory accuracy was positively correlated with sound-related activation during sleep in various brain regions, including the thalamus, bilateral medial temporal lobe, and cerebellum. In addition, postsleep memory accuracy was also positively correlated with pre-to postsleep changes in parahippocampal-medial prefrontal connectivity during retrieval of reactivated associations. Our results suggest that the brain is differentially activated by studied and unstudied sounds during deep sleep and that the thalamus and medial temporal lobe are involved in establishing the mnemonic consequences of externally triggered reactivation of associative memories. consolidation | neuroimaging | EEG-functional MRI | replay
Memory consolidation during sleep involves context reinstatement in humans
SummaryNew memories aren’t quarantined from each other when first encoded; rather, they are interlinked with memories that were encoded in temporal proximity or share semantic features. By selectively biasing memory processing during sleep, here we test whether context influences sleep-consolidation. Participants first formed 18 idiosyncratic narratives, each linking four objects together. Before sleep,they also memorized an on-screen position for each object. During sleep, 12 object-specific sounds were unobtrusively presented, thereby cuing the corresponding spatial memories and impacting spatial recall as a function of initial memory strength. As hypothesized, we find that recall for non-cued objects contextually linked with cued objects also changed. Post-cue electrophysiological responses suggest that activity in the sigma band supports context reinstatement and predicts context-related memory benefits. Concurrently, context-specific electrophysiological activity patterns emerg...