scholarly journals Shining a Light on the Mechanisms of Sleep for Memory Consolidation

Author(s):  
Michelle A. Frazer ◽  
Yesenia Cabrera ◽  
Rockelle S. Guthrie ◽  
Gina R. Poe

Abstract Purpose of review This paper reviews all optogenetic studies that directly test various sleep states, traits, and circuit-level activity profiles for the consolidation of different learning tasks. Recent findings Inhibiting or exciting neurons involved either in the production of sleep states or in the encoding and consolidation of memories reveals sleep states and traits that are essential for memory. REM sleep, NREM sleep, and the N2 transition to REM (characterized by sleep spindles) are integral to memory consolidation. Neural activity during sharp-wave ripples, slow oscillations, theta waves, and spindles are the mediators of this process. Summary These studies lend strong support to the hypothesis that sleep is essential to the consolidation of memories from the hippocampus and the consolidation of motor learning which does not necessarily involve the hippocampus. Future research can further probe the types of memory dependent on sleep-related traits and on the neurotransmitters and neuromodulators required.

SLEEP ◽  
2020 ◽  
Author(s):  
Jun-Sang Sunwoo ◽  
Kwang Su Cha ◽  
Jung-Ick Byun ◽  
Jin-Sun Jun ◽  
Tae-Joon Kim ◽  
...  

Abstract Study Objectives We investigated electroencephalographic (EEG) slow oscillations (SOs), sleep spindles (SSs), and their temporal coordination during nonrapid eye movement (NREM) sleep in patients with idiopathic rapid eye movement (REM) sleep behavior disorder (iRBD). Methods We analyzed 16 patients with video-polysomnography-confirmed iRBD (age, 65.4 ± 6.6 years; male, 87.5%) and 10 controls (age, 62.3 ± 7.5 years; male, 70%). SSs and SOs were automatically detected during stage N2 and N3. We analyzed their characteristics, including density, frequency, duration, and amplitude. We additionally identified SO-locked spindles and examined their phase distribution and phase locking with the corresponding SO. For inter-group comparisons, we used the independent samples t-test or Wilcoxon rank-sum test, as appropriate. Results The SOs of iRBD patients had significantly lower amplitude, longer duration (p = 0.005 for both), and shallower slope (p < 0.001) than those of controls. The SS power of iRBD patients was significantly lower than that of controls (p = 0.002), although spindle density did not differ significantly. Furthermore, SO-locked spindles of iRBD patients prematurely occurred during the down-to-up-state transition of SOs, whereas those of controls occurred at the up-state peak of SOs (p = 0.009). The phase of SO-locked spindles showed a positive correlation with delayed recall subscores (p = 0.005) but not with tonic or phasic electromyography activity during REM sleep. Conclusions In this study, we found abnormal EEG oscillations during NREM sleep in patients with iRBD. The impaired temporal coupling between SOs and SSs may reflect early neurodegenerative changes in iRBD.


2017 ◽  
Author(s):  
Elizaveta Solomonova ◽  
Simon Dubé ◽  
Cloé Blanchette-Carrière ◽  
Arnaud Samson-Richer ◽  
Michelle Carr ◽  
...  

Study objectives: Rapid eye movement (REM) sleep, non-rapid eye movement (NREM) sleep, and sleep spindles are all implicated in the consolidation of procedural memories. The relative contributions of sleep stages and sleep spindles was previously shown to depend on individual differences in task processing. Experience with Vipassana meditation is one such individual difference that has not been investigated in relation to sleep. Vipassana meditation is a form of mental training that enhances proprioceptive and somatic awareness and alters attentional style. The goal was thus to examine a potential moderating role for Vipassana meditation experience on sleep-dependent procedural memory consolidation.Methods: Groups of Vipassana meditation practitioners (N=20) and matched meditation-naïve controls (N=20) slept for a single daytime nap in the laboratory. Before and after the nap they completed a procedural task on the Wii Fit balance platform.Results: Meditators performed slightly better on the task before the nap, but the two groups improved similarly after sleep. The groups showed different patterns of sleep-dependent procedural memory consolidation: in meditators task learning was negatively correlated with density of fast and positively correlated with density of slow occipital spindles, while in controls task improvement was associated with increases in REM sleep. Meditation practitioners had a lower density of sleep spindles, especially in occipital regions.Conclusions: Results suggest that neuroplastic changes associated with sustained meditation practice may alter overall sleep architecture and reorganize sleep-dependent patterns of memory consolidation. The lower density of spindles in meditators may mean that meditation practice compensates for some of the memory functions of sleep.


Neuroforum ◽  
2020 ◽  
Vol 0 (0) ◽  
Author(s):  
Maryam Ghorbani ◽  
Lisa Marshall

AbstractSleep contributes actively to the consolidation of many forms of memory. This review describes the neural oscillations of non-rapid eye movement (NREM) sleep, the structures underlying these oscillations and their relation to hippocampus-dependent memory consolidation. A main focus lies on the relation between inter- and intraregional interactions and their electrophysiological representation. Methods for modulating neural oscillations with the intent of affecting memory consolidation are presented.


2013 ◽  
Vol 25 (10) ◽  
pp. 1597-1610 ◽  
Author(s):  
Erik J. Kaestner ◽  
John T. Wixted ◽  
Sara C. Mednick

Sleep affects declarative memory for emotional stimuli differently than it affects declarative memory for nonemotional stimuli. However, the interaction between specific sleep characteristics and emotional memory is not well understood. Recent studies on how sleep affects emotional memory have focused on rapid eye movement sleep (REM) but have not addressed non-REM sleep, particularly sleep spindles. This is despite the fact that sleep spindles are implicated in declarative memory as well as neural models of memory consolidation (e.g., hippocampal neural replay). Additionally, many studies examine a limited range of emotional stimuli and fail to disentangle differences in memory performance because of variance in valence and arousal. Here, we experimentally increase non-REM sleep features, sleep spindle density, and SWS, with pharmacological interventions using zolpidem (Ambien) and sodium oxybate (Xyrem) during daytime naps. We use a full spread of emotional stimuli to test all levels of valence and arousal. We find that increasing sleep spindle density increases memory discrimination (da) for highly arousing and negative stimuli without altering measures of bias (ca). These results indicate a broader role for sleep in the processing of emotional stimuli with differing effects based on arousal and valence, and they raise the possibility that sleep spindles causally facilitate emotional memory consolidation. These findings are discussed in terms of the known use of hypnotics in individuals with emotional mood disorders.


2021 ◽  
Author(s):  
Felipe A. Torres ◽  
Patricio Orio ◽  
María-José Escobar

AbstractSlow-wave sleep cortical brain activity, conformed by slow-oscillations and sleep spindles, plays a key role in memory consolidation. The increase of the power of the slow-wave events, obtained by auditory sensory stimulation, positively correlates to memory consolidation performance. However, little is known about the experimental protocol maximizing this effect, which could be induced by the power of slow-oscillation, the number of sleep spindles, or the timing of both events’ co-occurrence. Using a mean-field model of thalamocortical activity, we studied the effect of several stimulation protocols, varying the pulse shape, duration, amplitude, and frequency, as well as a target-phase using a closed-loop approach. We evaluated the effect of these parameters on slow-oscillations (SO) and sleep-spindles (SP), considering: (i) the power at the frequency bands of interest, (ii) the number of SO and SP, (iii) co-occurrences between SO and SP, and (iv) synchronization of SP with the up-peak of the SO. The first three targets are maximized using a decreasing ramp pulse with a pulse duration of 50 ms. Also, we observed a reduction in the number of SO when increasing the stimulus energy by rising its amplitude. To assess the target-phase parameter, we applied closed-loop stimulation at 0º, 45º, and 90º of the phase of the narrow-band filtered ongoing activity, at 0.85 Hz as central frequency. The 0º stimulation produces better results in the power and number of SO and SP than the rhythmic or aleatory stimulation. On the other hand, stimulating at 45º or 90º change the timing distribution of spindles centers but with fewer co-occurrences than rhythmic and 0º phase. Finally, we propose the application of closed-loop stimulation at the rising zero-cross point using pulses with a decreasing ramp shape and 50 ms of duration for future experimental work.Author summaryDuring the non-REM (NREM) phase of sleep, events that are known as slow oscillations (SO) and spindles (SP) can be detected by EEG. These events have been associated with the consolidation of declarative memories and learning. Thus, there is an ongoing interest in promoting them during sleep by non-invasive manipulations such as sensory stimulation. In this paper, we used a computational model of brain activity that generates SO and SP, to investigate which type of sensory stimulus –shape, amplitude, duration, periodicity– would be optimal for increasing the events’ frequency and their co-occurrence. We found that a decreasing ramp of 50 ms duration is the most effective. The effectiveness increases when the stimulus pulse is delivered in a closed-loop configuration triggering the pulse at a target phase of the ongoing SO activity. A desirable secondary effect is to promote SPs at the rising phase of the SO oscillation.


SLEEP ◽  
2020 ◽  
Vol 43 (Supplement_1) ◽  
pp. A35-A35
Author(s):  
E van Rijn ◽  
S A Walker ◽  
V C Knowland ◽  
S A Cairney ◽  
A D Gouws ◽  
...  

Abstract Introduction Memory for novel words benefits from sleep, particularly non-rapid eye movement (NREM) sleep and its features, such as sleep spindles and slow oscillations. This is consistent with systems consolidation models, in which sleep supports transfer from hippocampal to neocortical memory networks. Larger amounts of slow wave sleep in children has been proposed to account for enhanced consolidation effects, but such studies have typically focused on nocturnal sleep. We examined whether daytime naps benefit word retention in adults and children aged 10–12 years, and whether this relationship in children is affected by differences in white matter pathway microstructure. We hypothesized that the link between memory consolidation and structural brain connectivity will be mediated by the degree of sleep spindles during the nap. Methods Adults (N = 31; mean age = 20.91, SD = 1.55) and children (N = 38; mean age = 11.95, SD = 0.88) learned spoken novel words, followed by a 90-minute nap opportunity monitored with polysomnography. Memory for the words was tested pre- and post-nap. Children’s structural brain connectivity was measured using diffusion tensor imaging (DTI). Results Word memory was preserved following sleep in adults, while an adult wake control condition showed deterioration. Similarly, in children memory performance was stable over the nap, with wake control data currently being collected. Analyses relating behavioral changes over the nap to NREM sleep features and structural brain connectivity will be presented. Conclusion In line with sleep-dependent memory consolidation models, daytime naps protect novel words from forgetting in adults and children. Examining potential relationships between nap-based consolidation and structural integrity has important theoretical implications, given the increase in brain connectivity in language areas during childhood, as well as white matter alterations in developmental populations. Support This research was supported by the UK Economic and Social Research Council, grant no. ES/N009924/1.


SLEEP ◽  
2020 ◽  
Vol 43 (12) ◽  
Author(s):  
Jules Schneider ◽  
Penelope A Lewis ◽  
Dominik Koester ◽  
Jan Born ◽  
Hong-Viet V Ngo

Abstract Study Objectives Cortical slow oscillations (SOs) and thalamocortical sleep spindles hallmark slow wave sleep and facilitate memory consolidation, both of which are reduced with age. Experiments utilizing auditory closed-loop stimulation to enhance these oscillations showed great potential in young and older subjects. However, the magnitude of responses has yet to be compared between these age groups. We examined the possibility of enhancing SOs and performance on different memory tasks in a healthy middle-aged population using this stimulation and contrast effects to younger adults. Methods In a within-subject design, 17 subjects (55.7 ± 1.0 years) received auditory stimulation in synchrony with SO up-states, which was compared to a no-stimulation sham condition. Overnight memory consolidation was assessed for declarative word-pairs and procedural finger-tapping skill. Post-sleep encoding capabilities were tested with a picture recognition task. Electrophysiological effects of stimulation were compared to a previous younger cohort (n = 11, 24.2 ± 0.9 years). Results Overnight retention and post-sleep encoding performance of the older cohort revealed no beneficial effect of stimulation, which contrasts with the enhancing effect the same stimulation protocol had in our younger cohort. Auditory stimulation prolonged endogenous SO trains and induced sleep spindles phase-locked to SO up-states in the older population. However, responses were markedly reduced compared to younger subjects. Additionally, the temporal dynamics of stimulation effects on SOs and spindles differed between age groups. Conclusions Our findings suggest that the susceptibility to auditory stimulation during sleep drastically changes with age and reveal the difficulties of translating a functional protocol from younger to older populations.


2017 ◽  
Author(s):  
Mohsen Naji ◽  
Giri P. Krishnan ◽  
Elizabeth A McDevitt ◽  
Maxim Bazhenov ◽  
Sara C. Mednick

AbstractWhile anatomical pathways between forebrain cognitive and brainstem autonomic nervous centers are well defined, autonomic–central interactions during sleep and their contribution to waking performance are not understood. Here, we analyzed simultaneous central activity via electroencephalography (EEG) and autonomic heart beat-to-beat intervals (RR intervals) from electrocardiography (ECG) during wake and daytime sleep. We identified bursts of ECG activity that lasted 4-5 seconds and predominated in non-rapid-eye-movement sleep (NREM). Using event-based analysis of NREM sleep, we found an increase in delta (0.5-4Hz) and sigma (12-15Hz) power and an elevated density of slow oscillations (0.5-1Hz) about 5 secs prior to peak of the heart rate burst, as well as a surge in vagal activity, assessed by high-frequency (HF) component of RR intervals. Using regression framework, we show that these Autonomic/Central Events (ACE) positively predicted post-nap improvement in a declarative memory task after controlling for the effects of spindles and slow oscillations from sleep periods without ACE. No such relation was found between memory performance and a control nap. Additionally, NREM ACE negatively correlated with REM sleep and learning in a non-declarative memory task. These results provide the first evidence that coordinated autonomic and central events play a significant role in declarative memory consolidation.


Author(s):  
Jules Schneider ◽  
Penelope A. Lewis ◽  
Dominik Koester ◽  
Jan Born ◽  
Hong-Viet V. Ngo

AbstractBackgroundCortical slow oscillations (SOs) and thalamo-cortical sleep spindles hallmark slow wave sleep and facilitate sleep-dependent memory consolidation. Experiments utilising auditory closed-loop stimulation to enhance these oscillations have shown great potential in young and older subjects. However, the magnitude of responses has yet to be compared between these age groups.ObjectiveWe examined the possibility of enhancing SOs and performance on different memory tasks in a healthy older population using auditory closed-loop stimulation and contrast effects to a young adult cohort.MethodsIn a within-subject design, subjects (n = 17, 55.7 ± 1.0 years, 9 female) received auditory click stimulation in synchrony with SO up-states, which was compared to a no-stimulation sham condition. Overnight memory consolidation was assessed for declarative word-pairs and procedural finger-tapping skill. Post-sleep encoding capabilities were tested with a picture recognition task. Electrophysiological effects of stimulation were compared to those reported previously in a younger cohort (n = 11, 24.2 ± 0.9 years, 8 female).ResultsOvernight retention and post-sleep encoding performance of the older cohort revealed no beneficial effect of stimulation, which contrasts with the enhancing effect the same stimulation protocol had in our younger cohort. Auditory stimulation prolonged endogenous SO trains and induced sleep spindles phase-locked to SO up-states in the older population. However, responses were markedly reduced compared to younger subjects. Additionally, the temporal dynamics of stimulation effects on SOs and spindles differed between age groups.ConclusionsOur findings suggest that the susceptibility to auditory stimulation during sleep drastically changes with age and reveal the difficulties of translating a functional protocol from younger to older populations.HighlightsAuditory closed-loop stimulation induced SOs and sleep spindles in older subjectsStimulation effects were reduced and overall susceptibility diminished with ageSlow oscillation and sleep spindle dynamics deviated from those in younger subjectsStimulation shows no evidence for memory effect in older subjects


2021 ◽  
Author(s):  
Aurelie Brecier ◽  
Melodie Borel ◽  
Nadia Urbain ◽  
Luc J Gentet

GABAergic inhibitory neurons, through their molecular, anatomic and physiological diversity, provide a substrate for the modulation of ongoing cortical circuit activity throughout the sleep-wake cycle. Here, we investigated neuronal activity dynamics of parvalbumin (PV), vasoactive intestinal polypeptide (VIP) and somatostatin (SST) neurons in naturally-sleeping head-restrained mice at the level of layer 2/3 of the primary somatosensory barrel cortex of mice. Through calcium-imaging and targeted single-unit loose-patch or whole-cell recordings, we found that PV action potential (AP) firing activity was largest during both NREM (non-rapid eye movement) and REM sleep stages, that VIP neurons were activated during REM sleep and that the overall activity of SST neurons remained stable throughout the sleep/wake cycle. Analysis of neuronal activity dynamics uncovered rapid decreases in PV cell firing at wake onset followed by a progressive recovery during wake. Simultaneous local field potential (LFP) recordings further revealed that, except for SST neurons, a large proportion of neurons were modulated by ongoing delta and theta waves. During NREM sleep spindles, PV and SST activity increased and decreased, respectively. Finally, we uncovered the presence of whisking behavior in mice during REM sleep and show that the activity of VIP and SST is differentially modulated during awake and sleeping whisking bouts, which may provide a neuronal substrate for internal brain representations occurring during sleep.


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