Increased neuronal signatures of targeted memory reactivation during slow-wave up states.
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ABSTRACT:
SUBMITTER: Goldi M
PROVIDER: S-EPMC6389952 | biostudies-literature | 2019 Feb
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.
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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.
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Project description:Face memory, including the ability to recall a person's name, is of major importance in social contexts. Like many other memory functions, it may rely on sleep. We investigated whether targeted memory reactivation during sleep could improve associative and perceptual aspects of face memory. Participants studied 80 face-name pairs, and then a subset of spoken names with associated background music was presented unobtrusively during a daytime nap. This manipulation preferentially improved name recall and face recognition for those reactivated face-name pairs, as modulated by two factors related to sleep quality; memory benefits were positively correlated with the duration of stage N3 sleep (slow-wave sleep) and negatively correlated with measures of sleep disruption. We conclude that (a) reactivation of specific face-name memories during sleep can strengthen these associations and the constituent memories, and that (b) the effectiveness of this reactivation depends on uninterrupted N3 sleep.
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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:Sleep constitutes a privileged state for new memories to reactivate and consolidate. Previous work has demonstrated that consolidation can be bolstered experimentally either via delivery of reminder cues (targeted memory reactivation [TMR]) or via noninvasive brain stimulation geared toward enhancing endogenous sleep rhythms. Here, we combined both approaches, controlling the timing of TMR cues with respect to ongoing slow-oscillation (SO) phases. Prior to sleep, participants learned associations between unique words and a set of repeating images (e.g., car) while hearing a prototypical image sound (e.g., engine starting). Memory performance on an immediate test vs. a test the next morning quantified overnight memory consolidation. Importantly, two image sounds were designated as TMR cues, with one cue delivered at SO UP states and the other delivered at SO DOWN states. A novel sound was used as a TMR control condition. Behavioral results revealed a significant reduction of overnight forgetting for words associated with UP-state TMR compared with words associated with DOWN-state TMR. Electrophysiological results showed that UP-state cueing led to enhancement of the ongoing UP state and was followed by greater spindle power than DOWN-state cueing. Moreover, UP-state (and not DOWN-state) cueing led to reinstatement of target image representations. Together, these results unveil the behavioral and mechanistic effects of delivering reminder cues at specific phases of endogenous sleep rhythms and mark an important step for the endeavor to experimentally modulate memories during sleep.
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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:Slow oscillations are a pattern of synchronized network activity generated by the cerebral cortex. They consist of Up and Down states, which are periods of activity interspersed with periods of silence, respectively. However, even when this is a unique dynamic regime of transitions between Up and Down states, this pattern is not constant: there is a range of oscillatory frequencies (0.1-4 Hz), and the duration of Up vs. Down states during the cycles is variable. This opens many questions. Is there a constant relationship between the duration of Up and Down states? How much do they vary across conditions and oscillatory frequencies? Are there different sub regimes within the slow oscillations? To answer these questions, we aimed to explore a concrete aspect of slow oscillations, Up and Down state durations, across three conditions: deep anesthesia, light anesthesia, and slow-wave sleep (SWS), in the same chronically implanted rats. We found that light anesthesia and SWS have rather similar properties, occupying a small area of the Up and Down state duration space. Deeper levels of anesthesia occupy a larger region of this space, revealing that a large variety of Up and Down state durations can emerge within the slow oscillatory regime. In a network model, we investigated the network parameters that can explain the different points within our bifurcation diagram in which slow oscillations are expressed.
| S-EPMC7900541 | biostudies-literature
Project description:It is now well established that memories can reactivate during non-rapid eye movement (non-REM) sleep, but the question of whether equivalent reactivation can be detected in rapid eye movement (REM) sleep is hotly debated. To examine this, we used a technique called targeted memory reactivation (TMR) in which sounds are paired with learned material in wake, and then re-presented in subsequent sleep, in this case REM, to trigger reactivation. We then used machine learning classifiers to identify reactivation of task-related motor imagery from wake in REM sleep. Interestingly, the strength of measured reactivation positively predicted overnight performance improvement. These findings provide the first evidence for memory reactivation in human REM sleep after TMR that is directly related to brain activity during wakeful task performance.
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Project description:A widely accepted view in memory research is that previously acquired information can be reactivated during sleep, leading to persistent memory storage. Targeted memory reactivation (TMR) was developed as a technique whereby specific memories can be reactivated during sleep using a sensory stimulus linked to prior learning. As a research tool, TMR can improve memory, raising the possibility that it may be useful for cognitive enhancement and clinical therapy. A major challenge for the expanded use of TMR is that a skilled operator must manually control stimulation, which is impractical in many settings. To address this limitation, we developed the SleepStim system for automated TMR in the home. SleepStim includes a smartwatch to collect movement and heart-rate data, plus a smartphone to emit auditory cues. A machine-learning model identifies periods of deep sleep and triggers TMR sounds within these periods. We tested whether this system could replicate the spatial-memory benefit of in-laboratory TMR. Participants learned locations of objects on a grid, and then half of the object locations were reactivated during sleep over 3 nights. Recall was tested each morning. In an experiment with 61 participants, the TMR effect was not significant but varied systematically with stimulus intensity; low-intensity but not high-intensity stimuli produced memory benefits. In a second experiment with 24 participants, we limited stimulus intensity and found that TMR reliably improved spatial memory, consistent with effects observed in laboratory studies. We conclude that SleepStim can effectively accomplish automated TMR, and that avoiding sleep disruption is critical for TMR benefits.
| S-EPMC9649863 | biostudies-literature