Browse
Submit Data
Databases
API
Help

Dataset Information

26 Views

0 Connections

0 Citations

0 Reanalyses

0 Downloads

Omics score: 0

Neuronal reactivation during post-learning sleep consolidates long-term memory in Drosophila.

ABSTRACT: Animals consolidate some, but not all, learning experiences into long-term memory. Across the animal kingdom, sleep has been found to have a beneficial effect on the consolidation of recently formed memories into long-term storage. However, the underlying mechanisms of sleep dependent memory consolidation are poorly understood. Here, we show that consolidation of courtship long-term memory in Drosophila is mediated by reactivation during sleep of dopaminergic neurons that were earlier involved in memory acquisition. We identify specific fan-shaped body neurons that induce sleep after the learning experience and activate dopaminergic neurons for memory consolidation. Thus, we provide a direct link between sleep, neuronal reactivation of dopaminergic neurons, and memory consolidation.

SUBMITTER: Dag U

PROVIDER: S-EPMC6428568 | biostudies-literature | 2019 Feb

REPOSITORIES: biostudies-literature

ACCESS DATA

Json Xml

Publications

Neuronal reactivation during post-learning sleep consolidates long-term memory in Drosophila.

Dag Ugur U Lei Zhengchang Z Le Jasmine Q JQ Wong Allan A Bushey Daniel D Keleman Krystyna K

eLife 20190225

Animals consolidate some, but not all, learning experiences into long-term memory. Across the animal kingdom, sleep has been found to have a beneficial effect on the consolidation of recently formed memories into long-term storage. However, the underlying mechanisms of sleep dependent memory consolidation are poorly understood. Here, we show that consolidation of courtship long-term memory in Drosophila is mediated by reactivation during sleep of dopaminergic neurons that were earlier inv ...[more]

PMID: 30801246

Similar Datasets

Long term effects of cueing procedural memory reactivation during NREM sleep.

Project description:Targeted memory reactivation (TMR) has recently emerged as a promising tool to manipulate and study the sleeping brain. Although the technique is developing rapidly, only a few studies have examined how the effects of TMR develop over time. Here, we use a bimanual serial reaction time task (SRTT) to investigate whether the difference between the cued and un-cued sequence of button presses persists long-term. We further explore the relationship between the TMR benefit and sleep spindles, as well as their coupling with slow oscillations. Our behavioural analysis shows better performance for the dominant hand. Importantly, there was a strong effect of TMR, with improved performance on the cued sequence after sleep. Closer examination revealed a significant benefit of TMR at 10 days post-encoding, but not 24 h or 6 weeks post-encoding. Time spent in stage 2, but not stage 3, of NREM sleep predicted cueing benefit. We also found a significant increase in spindle density and SO-spindle coupling during the cue period, when compared to the no-cue period. Together, our results demonstrate that TMR effects evolve over several weeks post-cueing, as well as emphasising the importance of stage 2, spindles and the SO-spindle coupling in procedural memory consolidation.

| S-EPMC8591408 | biostudies-literature

Cued memory reactivation during sleep influences skill learning.

Project description:Information acquired during waking can be reactivated during sleep, promoting memory stabilization. After people learned to produce two melodies in time with moving visual symbols, we enhanced relative performance by presenting one melody during an afternoon nap. Electrophysiological signs of memory processing during sleep corroborated the notion that appropriate auditory stimulation that does not disrupt sleep can nevertheless bias memory consolidation in relevant brain circuitry.

| S-EPMC3498459 | biostudies-literature

Developmental emergence of sleep rhythms enables long-term memory in Drosophila.

Project description:In adulthood, sleep-wake rhythms are one of the most prominent behaviors under circadian control. However, during early life, sleep is spread across the 24-hour day. The mechanism through which sleep rhythms emerge, and consequent advantage conferred to a juvenile animal, is unknown. In the second-instar Drosophila larvae (L2), like in human infants, sleep is not under circadian control. We identify the precise developmental time point when the clock begins to regulate sleep in Drosophila, leading to emergence of sleep rhythms in early third-instars (L3). At this stage, a cellular connection forms between DN1a clock neurons and arousal-promoting Dh44 neurons, bringing arousal under clock control to drive emergence of circadian sleep. Last, we demonstrate that L3 but not L2 larvae exhibit long-term memory (LTM) of aversive cues and that this LTM depends upon deep sleep generated once sleep rhythms begin. We propose that the developmental emergence of circadian sleep enables more complex cognitive processes, including the onset of enduring memories.

| S-EPMC10491288 | biostudies-literature

Reactivation during sleep with incomplete reminder cues rather than complete ones stabilizes long-term memory in humans.

Project description:Reactivation by reminder cues labilizes memories during wakefulness, requiring reconsolidation to persist. In contrast, during sleep, cued reactivation seems to directly stabilize memories. In reconsolidation, incomplete reminders are more effective in reactivating memories than complete reminders by inducing a mismatch, i.e. a discrepancy between expected and actual events. Whether mismatch is likewise detected during sleep is unclear. Here we test whether cued reactivation during sleep is more effective for mismatch-inducing incomplete than complete reminders. We first establish that only incomplete but not complete reminders labilize memories during wakefulness. When complete or incomplete reminders are presented during 40-min sleep, both reminders are equally effective in stabilizing memories. However, when extending the retention interval for another 7?hours (following 40-min sleep), only incomplete but not complete reminders stabilize memories, regardless of the extension containing wakefulness or sleep. We propose that, during sleep, only incomplete reminders initiate long-term memory stabilization via mismatch detection.

| S-EPMC7718244 | biostudies-literature

Fatty-acid binding proteins modulate sleep and enhance long-term memory consolidation in Drosophila.

Project description:Sleep is thought to be important for memory consolidation, since sleep deprivation has been shown to interfere with memory processing. However, the effects of augmenting sleep on memory formation are not well known, and testing the role of sleep in memory enhancement has been limited to pharmacological and behavioral approaches. Here we test the effect of overexpressing the brain-type fatty acid binding protein (Fabp7) on sleep and long-term memory (LTM) formation in Drosophila melanogaster. Transgenic flies carrying the murine Fabp7 or the Drosophila homologue dFabp had reduced baseline sleep but normal LTM, while Fabp induction produced increases in both net sleep and LTM. We also define a post-training consolidation "window" that is sufficient for the observed Fabp-mediated memory enhancement. Since Fabp overexpression increases consolidated daytime sleep bouts, these data support a role for longer naps in improving memory and provide a novel role for lipid-binding proteins in regulating memory consolidation concurrently with changes in behavioral state.

| S-EPMC3029266 | biostudies-literature

Sleep Consolidates Motor Learning of Complex Movement Sequences in Mice.

Project description:IntroductionSleep-dependent consolidation of motor learning has been extensively studied in humans, but it remains unclear why some, but not all, learned skills benefit from sleep.Aims and methodsHere, we compared 2 different motor tasks, both requiring the mice to run on an accelerating device. In the rotarod task, mice learn to maintain balance while running on a small rod, while in the complex wheel task, mice run on an accelerating wheel with an irregular rung pattern.ResultsIn the rotarod task, performance improved to the same extent after sleep or after sleep deprivation (SD). Overall, using 7 different experimental protocols (41 sleep deprived mice, 26 sleeping controls), we found large interindividual differences in the learning and consolidation of the rotarod task, but sleep before/after training did not account for this variability. By contrast, using the complex wheel, we found that sleep after training, relative to SD, led to better performance from the beginning of the retest session, and longer sleep was correlated with greater subsequent performance. As in humans, the effects of sleep showed large interindividual variability and varied between fast and slow learners, with sleep favoring the preservation of learned skills in fast learners and leading to a net offline gain in the performance in slow learners. Using Fos expression as a proxy for neuronal activation, we also found that complex wheel training engaged motor cortex and hippocampus more than the rotarod training.ConclusionsSleep specifically consolidates a motor skill that requires complex movement sequences and strongly engages both motor cortex and hippocampus.

| S-EPMC6084756 | biostudies-literature

The ERM protein Moesin is essential for neuronal morphogenesis and long-term memory in Drosophila.

Project description:Moesin is a cytoskeletal adaptor protein that plays an important role in modification of the actin cytoskeleton. Rearrangement of the actin cytoskeleton drives both neuronal morphogenesis and the structural changes in neurons that are required for long-term memory formation. Moesin has been identified as a candidate memory gene in Drosophila, however, whether it is required for memory formation has not been evaluated. Here, we investigate the role of Moesin in neuronal morphogenesis and in short- and long-term memory formation in the courtship suppression assay, a model of associative memory. We found that both knockdown and overexpression of Moesin led to defects in axon growth and guidance as well as dendritic arborization. Moreover, reduction of Moesin expression or expression of a constitutively active phosphomimetic in the adult Drosophila brain had no effect on short term memory, but prevented long-term memory formation, an effect that was independent of its role in development. These results indicate a critical role for Moesin in both neuronal morphogenesis and long-term memory formation.

| S-EPMC5576258 | biostudies-literature

Classical music, educational learning, and slow wave sleep: A targeted memory reactivation experiment.

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

Motor Learning Consolidates Arc-Expressing Neuronal Ensembles in Secondary Motor Cortex.

Project description:Motor behaviors recruit task-specific neuronal ensembles in motor cortices, which are consolidated over subsequent learning. However, little is known about the molecules that can identify the participating neurons and predict the outcomes of the consolidation process. Using a mouse rotarod-learning task, we showed that lesion or inactivation of the secondary motor (M2) cortex disrupts learning of skilled movements. We tracked the endogenous promoter activity of the neuronal activity-regulated gene Arc in individual M2 neurons during rotarod learning by in vivo two-photon imaging of a knockin reporter. We found that task training initially recruits Arc-promoter-activated neurons and then consolidates them into a specific ensemble exhibiting persistent reactivation of Arc-promoter. The intensity of a neuron's initial Arc-promoter activation predicts its reactivation probability and neurons with weak initial Arc-promoter activation are dismissed from the ensemble during subsequent training. Our findings demonstrate a task-specific Arc-dependent cellular consolidation process in M2 cortex during motor learning.

| S-EPMC4474764 | biostudies-literature

The neuronal response at extended timescales: long-term correlations without long-term memory.

Project description:Long term temporal correlations frequently appear at many levels of neural activity. We show that when such correlations appear in isolated neurons, they indicate the existence of slow underlying processes and lead to explicit conditions on the dynamics of these processes. Moreover, although these slow processes can potentially store information for long times, we demonstrate that this does not imply that the neuron possesses a long memory of its input, even if these processes are bidirectionally coupled with neuronal response. We derive these results for a broad class of biophysical neuron models, and then fit a specific model to recent experiments. The model reproduces the experimental results, exhibiting long term (days-long) correlations due to the interaction between slow variables and internal fluctuations. However, its memory of the input decays on a timescale of minutes. We suggest experiments to test these predictions directly.

| S-EPMC3978321 | biostudies-literature