scholarly journals Stimulation augments spike sequence replay and memory consolidation during slow-wave sleep

2019 ◽  
Author(s):  
Yina Wei ◽  
Giri P Krishnan ◽  
Lisa Marshall ◽  
Thomas Martinetz ◽  
Maxim Bazhenov
Keyword(s):  
Slow Wave ◽  
Memory Consolidation ◽  
Temporal Pattern ◽  
Slow Wave Sleep ◽  
Sensory Stimulation ◽  
Slow Waves ◽  
Memory Traces ◽  
Spatio Temporal ◽  
Synaptic Level

AbstractNewly acquired memory traces are spontaneously reactivated during slow-wave sleep (SWS), leading to the consolidation of recent memories. Empirical studies found that sensory stimulation during SWS selectively enhances memory consolidation and the effect depends on the phase of stimulation. In this new study, we aimed to understand the mechanisms behind the role of sensory stimulation on memory consolidation using computational models implementing effects of neuromodulators to simulate transitions between awake and SWS sleep, and synaptic plasticity to allow the change of synaptic connections due to the training in awake or replay during sleep. We found that when closed-loop stimulation was applied during the Down states (900-2700) of sleep slow oscillation, particularly right before transition from Down to Up state, it significantly affected the spatio-temporal pattern of the slow-waves and maximized memory replay. In contrast, when the stimulation was presented during the Up states (2700-3600 and 00-900), it did not have a significant impact on the slow-waves or memory performance after sleep. For multiple memories trained in awake, presenting stimulation cues associated with specific memory trace could selectively augment replay and enhance consolidation of that memory and interfere with consolidation of the others (particularly weak) memories. Our study proposes a synaptic level mechanism of how memory consolidation is affected by sensory stimulation during sleep.Significance statementStimulation, such as training-associated cues or auditory stimulation, during sleep can augment consolidation of the newly encoded memories. In this study, we used a computational model of the thalamocortical system to describe the mechanisms behind the role of stimulation in memory consolidation during slow-wave sleep. Our study suggested that stimulation preferentially strengthens the memory traces when delivered at specific phase of slow oscillations just before Down to Up state transition when it makes the largest impact on the spatio-temporal pattern of sleep slow waves. In the presence of multiple memories, presenting sensory cues during sleep could selectively strengthen selected memories. Our study proposes a synaptic level mechanism of how memory consolidation is affected by sensory stimulation during sleep.

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 Bidirectional Interaction of Hippocampal Ripples and Cortical Slow Waves Leads to Coordinated Spiking Activity During NREM Sleep

2020 ◽  
Vol 31 (1) ◽  
pp. 324-340
Author(s):  
Pavel Sanda ◽  
Paola Malerba ◽  
Xi Jiang ◽  
Giri P Krishnan ◽  
Jorge Gonzalez-Martinez ◽  
...  
Keyword(s):  
Slow Wave ◽  
Memory Consolidation ◽  
Slow Wave Sleep ◽  
Nrem Sleep ◽  
Slow Waves ◽  
Slow Oscillation ◽  
Cortical Input ◽  
Sharp Wave ◽  
Up States ◽  
Intracranial Recordings

Abstract The dialogue between cortex and hippocampus is known to be crucial for sleep-dependent memory consolidation. During slow wave sleep, memory replay depends on slow oscillation (SO) and spindles in the (neo)cortex and sharp wave-ripples (SWRs) in the hippocampus. The mechanisms underlying interaction of these rhythms are poorly understood. We examined the interaction between cortical SO and hippocampal SWRs in a model of the hippocampo–cortico–thalamic network and compared the results with human intracranial recordings during sleep. We observed that ripple occurrence peaked following the onset of an Up-state of SO and that cortical input to hippocampus was crucial to maintain this relationship. A small fraction of ripples occurred during the Down-state and controlled initiation of the next Up-state. We observed that the effect of ripple depends on its precise timing, which supports the idea that ripples occurring at different phases of SO might serve different functions, particularly in the context of encoding the new and reactivation of the old memories during memory consolidation. The study revealed complex bidirectional interaction of SWRs and SO in which early hippocampal ripples influence transitions to Up-state, while cortical Up-states control occurrence of the later ripples, which in turn influence transition to Down-state.

scholarly journals 0084 Sleep Consolidates Incidentally Encoded Information After Deep but Not Shallow Encoding

SLEEP ◽  
2020 ◽  
Vol 43 (Supplement_1) ◽  
pp. A34-A34
Author(s):  
E M Wernette ◽  
K M Fenn
Keyword(s):  
Slow Wave ◽  
Memory Consolidation ◽  
Slow Wave Sleep ◽  
Declarative Memory ◽  
Memory Performance ◽  
Memory Test ◽  
Memory Traces ◽  
Incidental Encoding ◽  
The Relationship ◽  
With Memory

Abstract Introduction Slow wave sleep (SWS) strengthens declarative memory for information studied for a later test. However, research on the effect of sleep on information that is not intentionally remembered is scare. Previous research from our lab suggests sleep consolidates some, but not all, information that has been encoded incidentally, meaning that it has been acted on but not intentionally remembered. It remains unclear what determines which information benefits from sleep-dependent consolidation processes and what aspects of sleep are related to these mnemonic benefits. In two experiments, we test the hypothesis that sleep consolidates strong but not weak memory traces following incidental encoding, and assess the relationship between memory performance and objective sleep characteristics. Methods In Experiment 1, participants rated words one (weak traces) or three times (strong traces) in a deep or shallow incidental encoding task. Participants either rated words on a scale from ‘concrete’ to ‘abstract’ (deep) or counted the vowels in the words (shallow). Following a 12-hour period containing sleep or wakefulness, participants took a surprise memory test. In Experiment 2, participants rated words one or three times in the deep encoding task, received an 8-hour sleep opportunity with polysomnography, and took the surprise memory test. Results In Experiment 1, participants remembered words better after sleep than wake regardless of whether words were encoded one or three times, but only after deep encoding. Sleep did not consolidate information following shallow encoding. Experiment 2 is ongoing, but we predict that the amount of SWS will correlate positively with memory. Conclusion Results thus far suggest sleep may have consolidated information based on the strength of memory traces. Because deep encoding results in stronger memory traces than shallow encoding, this work is broadly consistent with theories of memory consolidation that predict sleep is more beneficial for strong memory traces than weak, such as the synaptic downscaling hypothesis. Support N/A

scholarly journals The role of slow-wave sleep rhythms in the cortical-hippocampal loop for memory consolidation

2020 ◽  
Vol 32 ◽  
pp. 102-110
Author(s):  
Miguel Navarrete ◽  
Mario Valderrama ◽  
Penelope A Lewis
Keyword(s):  
Slow Wave ◽  
Memory Consolidation ◽  
Slow Wave Sleep ◽  
Sleep Rhythms

scholarly journals Replay of large-scale spatio-temporal patterns from waking during subsequent slow-wave sleep in human cortex

2017 ◽  
Author(s):  
Xi Jiang ◽  
Isaac Shamie ◽  
Werner Doyle ◽  
Daniel Friedman ◽  
Patricia Dugan ◽  
...  
Keyword(s):  
Slow Wave ◽  
Memory Consolidation ◽  
Animal Studies ◽  
Large Scale ◽  
Slow Wave Sleep ◽  
Cognitive Task ◽  
Human Memory ◽  
Sharp Wave ◽  
Direct Demonstration ◽  
Spatio Temporal

AbstractAnimal studies support the hypothesis that in slow-wave sleep, replay of waking neocortical activity under hippocampal guidance leads to memory consolidation. However, no intracranial electrophysiological evidence for replay exists in humans. We identified consistent sequences of population firing peaks across widespread cortical regions during complete waking periods. The occurrence of these Motifs were compared between sleeps preceding the waking period (Sleep-Pre) when the Motifs were identified, and those following (Sleep-Post). In all subjects, the majority of waking Motifs (most of which were novel) had more matches in Sleep-Post than in Sleep-Pre. In rodents, hippocampal replay occurs during local sharp-wave ripples, and the associated neocortical replay tends to occur during local sleep spindles and down-to-up transitions. These waves may facilitate consolidation by sequencing cell-firing and encouraging plasticity. Similarly, we found that Motifs were coupled to neocortical spindles, down-to-up transitions, theta bursts, and hippocampal sharp-wave ripples. While Motifs occurring during cognitive task performance were more likely to have more matches in subsequent sleep, our studies provide no direct demonstration that the replay of Motifs contributes to consolidation. Nonetheless, these results confirm a core prediction of the dominant neurobiological theory of human memory consolidation.

032 Sleep Consolidates Memory for Strong but not Weak Information After Incidental Encoding

SLEEP ◽  
2021 ◽  
Vol 44 (Supplement_2) ◽  
pp. A14-A15
Author(s):  
Elle Wernette ◽  
Kimberly Fenn
Keyword(s):  
Slow Wave ◽  
Response Latency ◽  
Memory Consolidation ◽  
Slow Wave Sleep ◽  
Memory Performance ◽  
Memory Test ◽  
Memory Strength ◽  
Memory Traces ◽  
Incidental Encoding ◽  
The Relationship

Abstract Introduction Slow wave sleep (SWS) strengthens memory for studied information, but research on the effect of sleep on information that is not intentionally remembered is scarce. Previous research from our lab suggests sleep consolidates some information that has been encoded incidentally, meaning that it has been acted on but not intentionally remembered. It remains unclear what determines which information is consolidated during sleep after incidental encoding and what aspects of sleep are related to this mnemonic benefit. In two experiments, we test the hypothesis that sleep consolidates strong but not weak memory traces following incidental encoding and assess the relationship between memory performance and sleep attributes. Methods In Experiment 1, we manipulated memory strength within- and between-subjects. Participants rated words one or three times (within) in a shallow or deep incidental encoding task (between). In the shallow task, participants counted vowels in each word; in the deep task, participants rated each word on a scale from ‘concrete’ to ‘abstract’. Following a 12-hour period containing sleep or wakefulness, participants took a surprise memory test. In Experiment 2, participants rated words one or three times in the deep encoding task, received an 8-hour sleep opportunity with partial PSG, and took the surprise memory test. Results In Experiment 1, participants remembered words better after sleep than wake regardless of number of encoding trials, but only after deep encoding. There was not an effect of sleep following shallow encoding. In Experiment 2, SWS correlated negatively with response latency for correctly recognized words encoded once, but not those encoded three times. That is, participants who received more SWS showed faster performance. Conclusion Results suggest sleep consolidated information based on the depth of encoding, and this benefit was related to SWS. This work is broadly consistent with theories of memory consolidation that predict sleep is more beneficial for strong than weak memory traces, such as the synaptic downscaling hypothesis. Support (if any):

scholarly journals Cholinergic Switch between Two Types of Slow Waves in Cerebral Cortex

2020 ◽  
Vol 30 (6) ◽  
pp. 3451-3466 ◽  
Author(s):  
Trang-Anh E Nghiem ◽  
Núria Tort-Colet ◽  
Tomasz Górski ◽  
Ulisse Ferrari ◽  
Shayan Moghimyfiroozabad ◽  
...  
Keyword(s):  
Slow Wave ◽  
Memory Consolidation ◽  
Acetylcholine Receptors ◽  
Computational Models ◽  
Slow Wave Sleep ◽  
Slow Waves ◽  
Wave Dynamics ◽  
Positive Effects

Abstract Sleep slow waves are known to participate in memory consolidation, yet slow waves occurring under anesthesia present no positive effects on memory. Here, we shed light onto this paradox, based on a combination of extracellular recordings in vivo, in vitro, and computational models. We find two types of slow waves, based on analyzing the temporal patterns of successive slow-wave events. The first type is consistently observed in natural slow-wave sleep, while the second is shown to be ubiquitous under anesthesia. Network models of spiking neurons predict that the two slow wave types emerge due to a different gain on inhibitory versus excitatory cells and that different levels of spike-frequency adaptation in excitatory cells can account for dynamical distinctions between the two types. This prediction was tested in vitro by varying adaptation strength using an agonist of acetylcholine receptors, which demonstrated a neuromodulatory switch between the two types of slow waves. Finally, we show that the first type of slow-wave dynamics is more sensitive to external stimuli, which can explain how slow waves in sleep and anesthesia differentially affect memory consolidation, as well as provide a link between slow-wave dynamics and memory diseases.

scholarly journals Cholinergic switch between two types of slow waves in cerebral cortex

2018 ◽  
Author(s):  
Trang-Anh E Nghiem ◽  
Núria Tort-Colet ◽  
Tomasz Górski ◽  
Ulisse Ferrari ◽  
Shayan Moghimyfiroozabad ◽  
...  
Keyword(s):  
Slow Wave ◽  
Memory Consolidation ◽  
Acetylcholine Receptors ◽  
Computational Models ◽  
Slow Wave Sleep ◽  
Slow Waves ◽  
Wave Dynamics ◽  
Positive Effects

AbstractSleep slow waves are known to participate in memory consolidation, yet slow waves occurring under anesthesia present no positive effects on memory. Here, we shed light onto this paradox, based on a combination of extracellular recordings in vivo, in vitro, and computational models. We find two types of slow waves, based on analyzing the temporal patterns of successive slow-wave events. The first type is consistently observed in natural slow-wave sleep, while the second is shown to be ubiquitous under anesthesia. Network models of spiking neurons predict that the two slow wave types emerge due to a different gain on inhibitory vs excitatory cells and that different levels of spike-frequency adaptation in excitatory cells can account for dynamical distinctions between the two types. This prediction was tested in vitro by varying adaptation strength using an agonist of acetylcholine receptors, which demonstrated a neuromodulatory switch between the two types of slow waves. Finally, we show that the first type of slow-wave dynamics is more sensitive to external stimuli, which can explain how slow waves in sleep and anesthesia differentially affect memory consolidation, as well as provide a link between slow-wave dynamics and memory diseases.

Sign in / Sign up

Export Citation Format

Share Document