Targeted memory reactivation of face-name learning depends on ample and undisturbed slow-wave sleep.
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ABSTRACT:
SUBMITTER: Whitmore NW
PROVIDER: S-EPMC8755782 | biostudies-literature |
REPOSITORIES: biostudies-literature
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Project description:STUDY OBJECTIVES:To investigate the mechanisms by which auditory targeted memory reactivation (TMR) during slow wave sleep (SWS) influences the consolidation of emotionally negative and neutral memories. DESIGN:Each of 72 (36 negative, 36 neutral) picture-location associations were encoded with a semantically related sound. During a subsequent nap, half of the sounds were replayed in SWS, before picture-location recall was examined in a final test. SETTING:Manchester Sleep Laboratory, University of Manchester. PARTICIPANTS:15 adults (3 male) mean age = 20.40 (standard deviation ± 3.07). INTERVENTIONS:TMR with auditory cues during SWS. MEASUREMENTS AND RESULTS:Performance was assessed by memory accuracy and recall response times (RTs). Data were analyzed with a 2 (sound: replayed/not replayed) × 2 (emotion: negative/neutral) repeated measures analysis of covariance with SWS duration, and then SWS spindles, as the mean-centered covariate. Both analyses revealed a significant three-way interaction for RTs but not memory accuracy. Critically, SWS duration and SWS spindles predicted faster memory judgments for negative, relative to neutral, picture locations that were cued with TMR. CONCLUSIONS:TMR initiates an enhanced consolidation process during subsequent SWS, wherein sleep spindles mediate the selective enhancement of reactivated emotional memories.
| S-EPMC3954173 | biostudies-literature
Project description: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.
| S-EPMC3387124 | biostudies-other
Project description:Poor sleep in college students compromises the memory consolidation processes necessary to retain course materials. A solution may lie in targeting reactivation of memories during sleep (TMR). Fifty undergraduate students completed a college-level microeconomics lecture (mathematics-based) while listening to distinctive classical music (Chopin, Beethoven, and Vivaldi). After they fell asleep, we re-played the classical music songs (TMR) or a control noise during slow wave sleep. Relative to the control condition, the TMR condition showed an 18% improvement for knowledge transfer items that measured concept integration (d = 0.63), increasing the probability of "passing" the test with a grade of 70 or above (OR = 4.68, 95%CI: 1.21, 18.04). The benefits of TMR did not extend to a 9-month follow-up test when performance dropped to floor levels, demonstrating that long-term-forgetting curves are largely resistant to experimentally-consolidated memories. Spectral analyses revealed greater frontal theta activity during slow wave sleep in the TMR condition than the control condition (d = 0.87), and greater frontal theta activity across conditions was associated with protection against long-term-forgetting at the next-day and 9-month follow-up tests (rs = 0.42), at least in female students. Thus, students can leverage instrumental music-which they already commonly pair with studying-to help prepare for academic tests, an approach that may promote course success and persistence.
| S-EPMC7198365 | biostudies-literature
Project description:Memory reprocessing following acquisition enhances memory consolidation. Specifically, neural activity during encoding is thought to be 'replayed' during subsequent slow-wave sleep. Such memory replay is thought to contribute to the functional reorganization of neural memory traces. In particular, memory replay may facilitate the exchange of information across brain regions by inducing a reconfiguration of connectivity across the brain. Memory reactivation can be induced by external cues through a procedure known as "targeted memory reactivation". Here, we analysed data from a published study with auditory cues used to reactivate visual object-location memories during slow-wave sleep. We characterized effects of memory reactivation on brain network connectivity using graph-theory. We found that cue presentation during slow-wave sleep increased global network integration of occipital cortex, a visual region that was also active during retrieval of object locations. Although cueing did not have an overall beneficial effect on the retention of cued versus uncued associations, individual differences in overnight memory stabilization were related to enhanced network integration of occipital cortex. Furthermore, occipital cortex displayed enhanced connectivity with mnemonic regions, namely the hippocampus, parahippocampal gyrus, thalamus and medial prefrontal cortex during cue sound presentation. Together, these results suggest a neural mechanism where cue-induced replay during sleep increases integration of task-relevant perceptual regions with mnemonic regions. This cross-regional integration may be instrumental for the consolidation and long-term storage of enduring memories.
| S-EPMC6240046 | biostudies-literature
Project description:Interaction between hippocampal sharp-wave ripples (SWRs) and UP states, possibly by coordinated reactivation of memory traces, is conjectured to play an important role in memory consolidation. Recently, it was reported that SWRs were differentiated into multiple subtypes. However, whether cortical UP states can also be classified into subtypes is not known. Here, we analysed neural ensemble activity from the medial prefrontal cortex from rats trained to run a spatial sequence-memory task. Application of the hidden Markov model (HMM) with three states to epochs of UP-DOWN oscillations identified DOWN states and two subtypes of UP state (UP-1 and UP-2). The two UP subtypes were distinguished by differences in duration, with UP-1 having a longer duration than UP-2, as well as differences in the speed of population vector (PV) decorrelation, with UP-1 decorrelating more slowly than UP-2. Reactivation of recent memory sequences predominantly occurred in UP-2. Short-duration reactivating UP states were dominated by UP-2 whereas long-duration ones exhibit transitions from UP-1 to UP-2. Thus, recent memory reactivation, if it occurred within long-duration UP states, typically was preceded by a period of slow PV evolution not related to recent experience, and which we speculate may be related to previously encoded information. If that is the case, then the transition from UP-1 to UP-2 subtypes may help gradual integration of recent experience with pre-existing cortical memories by interleaving the two in the same UP state. This article is part of the Theo Murphy meeting issue 'Memory reactivation: replaying events past, present and future'.
| S-EPMC7209915 | biostudies-literature
Project description:It is assumed that slow oscillatory up-states represent crucial time windows for memory reactivation and consolidation during sleep. We tested this assumption by utilizing closed-loop targeted memory reactivation: Participants were re-exposed to prior learned foreign vocabulary during up- and down-states of slow oscillations. While presenting memory cues during slow oscillatory up-states improved recall performance, down-state cueing did not result in a clear behavioral benefit. Still, no robust behavioral benefit of up- as compared to down-state cueing was observable. At the electrophysiological level however, successful memory reactivation during up-states was associated with a characteristic power increase in the theta and sleep spindle band. No oscillatory changes were observable for down-state cues. Our findings provide experimental support for the assumption that slow oscillatory up-states may represent privileged time windows for memory reactivation, while the interplay of slow oscillations, theta and sleep spindle activity promotes successful memory consolidation during sleep.
| S-EPMC6389952 | biostudies-literature
Project description:Brain-machine interfaces can allow neural control over assistive devices. They also provide an important platform for studying neural plasticity. Recent studies have suggested that optimal engagement of learning is essential for robust neuroprosthetic control. However, little is known about the neural processes that may consolidate a neuroprosthetic skill. On the basis of the growing body of evidence linking slow-wave activity (SWA) during sleep to consolidation, we examined whether there is 'offline' processing after neuroprosthetic learning. Using a rodent model, we found that, after successful learning, task-related units specifically experienced increased locking and coherency to SWA during sleep. Moreover, spike-spike coherence among these units was substantially enhanced. These changes were not present with poor skill acquisition or after control awake periods, demonstrating the specificity of our observations to learning. Notably, the time spent in SWA predicted the performance gains. Thus, SWA appears to be involved in offline processing after neuroprosthetic learning.
| S-EPMC5568667 | biostudies-literature
Project description:Slow-wave sleep (SWS) has been shown to promote long-term consolidation of episodic memories in hippocampo-neocortical networks. Previous research has aimed to modulate cortical sleep slow-waves and spindles to facilitate episodic memory consolidation. Here, we instead aimed to modulate hippocampal activity during slow-wave sleep using transcranial direct current stimulation in 18 healthy humans. A pair-associate episodic memory task was used to evaluate sleep-dependent memory consolidation with face-occupation stimuli. Pre- and post-nap retrieval was assessed as a measure of memory performance. Anodal stimulation with 2 mA was applied bilaterally over the lateral temporal cortex, motivated by its particularly extensive connections to the hippocampus. The participants slept in a magnetic resonance (MR)-simulator during the recordings to test the feasibility for a future MR-study. We used a sham-controlled, double-blind, counterbalanced randomized, within-subject crossover design. We show that stimulation vs. sham significantly increased slow-wave density and the temporal coupling of fast spindles and slow-waves. While retention of episodic memories across sleep was not affected across the entire sample of participants, it was impaired in participants with below-average pre-sleep memory performance. Hence, bi-temporal anodal direct current stimulation applied during sleep enhanced sleep parameters that are typically involved in memory consolidation, but it failed to improve memory consolidation and even tended to impair consolidation in poor learners. These findings suggest that artificially enhancing memory-related sleep parameters to improve memory consolidation can actually backfire in those participants who are in most need of memory improvement.
| S-EPMC8064104 | biostudies-literature
Project description:The neurotransmitter acetylcholine is considered essential for proper functioning of the hippocampus-dependent declarative memory system, and it represents a major neuropharmacological target for the treatment of memory deficits, such as those in Alzheimer's disease. During slow-wave sleep (SWS), however, declarative memory consolidation is particularly strong, while acetylcholine levels in the hippocampus drop to a minimum. Observations in rats led to the hypothesis that the low cholinergic tone during SWS is necessary for the replay of new memories in the hippocampus and their long-term storage in neocortical networks. However, this low tone should not affect nondeclarative memory systems. In this study, increasing central nervous cholinergic activation during SWS-rich sleep by posttrial infusion of 0.75 mg of the cholinesterase inhibitor physostigmine completely blocked SWS-related consolidation of declarative memories for word pairs in human subjects. The treatment did not interfere with consolidation of a nondeclarative mirror tracing task. Also, physostigmine did not alter memory consolidation during waking, when the endogenous central nervous cholinergic tone is maximal. These findings are in line with predictions that a low cholinergic tone during SWS is essential for declarative memory consolidation.
| S-EPMC357065 | biostudies-literature
Project description:It has been proposed that sleep's contribution to memory consolidation is to reactivate prior encoded information. To elucidate the neural mechanisms carrying reactivation-related mnemonic information, we investigated whether content-specific memory signatures associated with memory reactivation during wakefulness reoccur during subsequent sleep. We show that theta oscillations orchestrate the reactivation of memories during both wakefulness and sleep. Reactivation patterns during sleep autonomously re-emerged at a rate of ?1 Hz, indicating a coordination by slow oscillatory activity.
| S-EPMC6198287 | biostudies-literature