scholarly journals Visuomotor adaptation modulates the clustering of sleep spindles into trains

2021 ◽  
Author(s):  
Agustin Solano ◽  
Luis A Riquelme ◽  
Daniel Perez-Chada ◽  
Valeria Della-Maggiore
Keyword(s):  
Memory Consolidation ◽  
Visuomotor Adaptation ◽  
Temporal Organization ◽  
Sleep Spindles ◽  
Memory Retention ◽  
Contralateral Hemisphere ◽  
Slow Oscillations ◽  
Organization Of Sleep ◽  
Train Length ◽  
Biological Advantage

Sleep spindles are thought to promote memory consolidation. Recently, we have shown that visuomotor adaptation (VMA) learning increases the density of spindles and promotes the coupling between spindles and slow oscillations, locally, with the level of spindle-SO synchrony predicting overnight memory retention. Yet, growing evidence suggests that the rhythmicity in spindle occurrence may also influence the stabilization of declarative and procedural memories. Here, we examined if VMA learning promotes the temporal organization of sleep spindles into trains. We found that VMA increased the proportion of spindles and spindle-SO couplings in trains. In agreement with our previous work, this modulation was observed over the contralateral hemisphere to the trained hand, and predicted overnight memory retention. Interestingly, spindles grouped in a cluster showed greater amplitude and duration than isolated spindles. The fact that these features increased as a function of train length, provides evidence supporting a biological advantage of this temporal arrangement. Our work opens the possibility that the periodicity of NREM oscillations may be relevant in the stabilization of procedural memories.

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

2021 ◽  
Author(s):  
Michelle A. Frazer ◽  
Yesenia Cabrera ◽  
Rockelle S. Guthrie ◽  
Gina R. Poe
Keyword(s):  
Rem Sleep ◽  
Neural Activity ◽  
Memory Consolidation ◽  
Strong Support ◽  
Nrem Sleep ◽  
Future Research ◽  
Sleep Spindles ◽  
Slow Oscillations ◽  
Theta Waves ◽  
Learning Tasks

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.

scholarly journals Selection of stimulus parameters for enhancing slow wave sleep events with a Neural-field theory thalamocortical computational model

2021 ◽  
Author(s):  
Felipe A. Torres ◽  
Patricio Orio ◽  
María-José Escobar
Keyword(s):  
Computational Model ◽  
Slow Wave ◽  
Memory Consolidation ◽  
Closed Loop ◽  
Slow Wave Sleep ◽  
Brain Activity ◽  
Sensory Stimulation ◽  
Sleep Spindles ◽  
Slow Oscillations ◽  
Closed Loop Stimulation

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.

scholarly journals Susceptibility to auditory closed-loop stimulation of sleep slow oscillations changes with age

SLEEP ◽  
2020 ◽  
Vol 43 (12) ◽  
Author(s):  
Jules Schneider ◽  
Penelope A Lewis ◽  
Dominik Koester ◽  
Jan Born ◽  
Hong-Viet V Ngo
Keyword(s):  
Memory Consolidation ◽  
Closed Loop ◽  
Temporal Dynamics ◽  
Age Groups ◽  
Recognition Task ◽  
Auditory Stimulation ◽  
Sleep Spindles ◽  
Slow Oscillations ◽  
Up States ◽  
Closed Loop Stimulation

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.

scholarly journals Susceptibility to auditory closed-loop stimulation of sleep slow oscillations changes with age

2019 ◽  
Author(s):  
Jules Schneider ◽  
Penelope A. Lewis ◽  
Dominik Koester ◽  
Jan Born ◽  
Hong-Viet V. Ngo
Keyword(s):  
Memory Consolidation ◽  
Closed Loop ◽  
Age Groups ◽  
Auditory Stimulation ◽  
Sleep Spindles ◽  
Older Population ◽  
Slow Oscillations ◽  
Up States ◽  
Older Subjects ◽  
Closed Loop Stimulation

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

scholarly journals Differential roles of sleep spindles and sleep slow oscillations in memory consolidation

2017 ◽  
Author(s):  
Yina Wei ◽  
Giri P Krishnan ◽  
Maxim Komarov ◽  
Maxim Bazhenov
Keyword(s):  
Memory Consolidation ◽  
Testable Hypothesis ◽  
State Transitions ◽  
Sleep Stages ◽  
Sleep Spindles ◽  
Slow Oscillations ◽  
Natural Sleep ◽  
Sleep Rhythms ◽  
Spike Sequence

AbstractSleep plays an important role in consolidation of recent memories. However, the mechanisms of consolidation remain poorly understood. In this study, using a realistic computational model of the thalamocortical network, we demonstrated that sleep spindles (the hallmark of N2 stage sleep) and slow oscillations (the hallmark of N3 stage sleep) both facilitate spike sequence replay as necessary for consolidation. When multiple memories were trained, the local nature of spike sequence replay during spindles allowed replay of the memories independently, while during slow oscillations replay of the weak memory was competing to the strong memory replay. This led to the weak memory extinction unless when sleep spindles (N2 sleep) preceded slow oscillations (N3 sleep), as observed during natural sleep. Our study presents a mechanistic explanation for the role of sleep rhythms in memory consolidation and proposes a testable hypothesis how the natural structure of sleep stages provides an optimal environment to consolidate memories.Significant StatementNumerous studies suggest importance of NREM sleep rhythms – spindles and slow oscillations - in sleep related memory consolidation. However, synaptic mechanisms behind the role of these rhythms in memory and learning are still unknown. Our new study predicts that sleep replay - the neuronal substrate of memory consolidation - is organized within the sleep spindles and coordinated by the Down to Up state transitions of the slow oscillation. For multiple competing memories, slow oscillations facilitated only strongest memory replay, while sleep spindles allowed a consolidation of the multiple competing memories independently. Our study predicts how the basic structure of the natural sleep stages provides an optimal environment for consolidation of multiple memories.

scholarly journals Selection of stimulus parameters for enhancing slow wave sleep events with a neural-field theory thalamocortical model

2021 ◽  
Vol 17 (7) ◽  
pp. e1008758
Author(s):  
Felipe A. Torres ◽  
Patricio Orio ◽  
María-José Escobar
Keyword(s):  
Slow Wave ◽  
Memory Consolidation ◽  
Closed Loop ◽  
Slow Wave Sleep ◽  
Brain Activity ◽  
Sleep Spindles ◽  
Mean Field Model ◽  
Cross Point ◽  
Slow Oscillations ◽  
Closed Loop Stimulation

Slow-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 0°, 45°, and 90° of the phase of the narrow-band filtered ongoing activity, at 0.85 Hz as central frequency. The 0° stimulation produces better results in the power and number of SO and SP than the rhythmic or random stimulation. On the other hand, stimulating at 45° or 90° change the timing distribution of spindles centers but with fewer co-occurrences than rhythmic and 0° 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.

scholarly journals The Overnight Retention of Novel Metaphors Associates With Slow Oscillation–Spindle Coupling but Not With Respiratory Phase at Encoding

2021 ◽  
Vol 15 ◽  
Author(s):  
Risto Halonen ◽  
Liisa Kuula ◽  
Minea Antila ◽  
Anu-Katriina Pesonen
Keyword(s):  
Neural Activity ◽  
Memory Consolidation ◽  
Memory Task ◽  
Slow Oscillation ◽  
Sleep Spindles ◽  
Memory Retention ◽  
Mixed Design ◽  
Respiratory Phase ◽  
Local Nature ◽  
Temporal Overlap

Accumulating evidence emphasizes the relevance of oscillatory synchrony in memory consolidation during sleep. Sleep spindles promote memory retention, especially when occurring in the depolarized upstate of slow oscillation (SO). A less studied topic is the inter-spindle synchrony, i.e. the temporal overlap and phasic coherence between spindles perceived in different electroencephalography channels. In this study, we examined how synchrony between SOs and spindles, as well as between simultaneous spindles, is associated with the retention of novel verbal metaphors. Moreover, we combined the encoding of the metaphors with respiratory phase (inhalation/exhalation) with the aim of modulating the strength of memorized items, as previous studies have shown that inhalation entrains neural activity, thereby benefiting memory in a waking condition. In the current study, 27 young adults underwent a two-night mixed-design study with a 12-h delayed memory task during both sleep and waking conditions. As expected, we found better retention over the delay containing sleep, and this outcome was strongly associated with the timing of SO–spindle coupling. However, no associations were observed regarding inter-spindle synchrony or respiratory phase. These findings contribute to a better understanding of the importance of SO–spindle coupling for memory. In contrast, the observed lack of association with inter-spindle synchrony may emphasize the local nature of spindle-related plasticity.

scholarly journals Local coupling between sleep spindles and slow oscillations supports the consolidation of motor memories

2020 ◽  
Author(s):  
Agustín Solano ◽  
Luis A. Riquelme ◽  
Daniel Perez-Chada ◽  
Valeria Della-Maggiore
Keyword(s):  
Motor Learning ◽  
Memory Consolidation ◽  
Nrem Sleep ◽  
Motor Memory ◽  
Common Mechanism ◽  
Long Term Memory ◽  
Memory Retention ◽  
Term Memory ◽  
Slow Oscillations

AbstractThe precise coupling between slow oscillations (SO) and spindles is critical for sleep-dependent consolidation of declarative memories. Here, we examined whether this mechanism also operates in the stabilization of human motor memories during NREM sleep. We hypothesized that if the coupling of these oscillations is instrumental to motor memory consolidation then only SO-coupled spindles would predict long-term memory. We found that sleep enhanced long-term memory retention by 34%. Motor learning increased the density of spindles but not their frequency, duration or amplitude during NREM sleep. This modulation was manifested locally over the hemisphere contralateral to the trained hand. Although motor learning did not affect the density of SOs, it substantially modulated the spindle-SO coupling in an inter-hemispheric manner, suggesting it may rather increase the ability of slow oscillations to promote thalamic spindles. The fact that only coupled spindles predicted long-term memory points to the association of these oscillations as a fundamental signature of motor memory consolidation. Our work provides evidence in favor of a common mechanism at the basis of the stabilization of declarative and non-declarative memories.

scholarly journals Differential roles of sleep spindles and sleep slow oscillations in memory consolidation

2018 ◽  
Vol 14 (7) ◽  
pp. e1006322 ◽  
Author(s):  
Yina Wei ◽  
Giri P. Krishnan ◽  
Maxim Komarov ◽  
Maxim Bazhenov
Keyword(s):  
Memory Consolidation ◽  
Sleep Spindles ◽  
Slow Oscillations
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