scholarly journals Coupling between slow waves and sharp-wave ripples engages distributed neural activity during sleep in humans

2021 ◽  
Vol 118 (21) ◽  
pp. e2012075118
Author(s):  
Ivan Skelin ◽  
Haoxin Zhang ◽  
Jie Zheng ◽  
Shiting Ma ◽  
Bryce A. Mander ◽  
...  
Keyword(s):  
Slow Wave ◽  
Memory Consolidation ◽  
Temporal Cortex ◽  
Neuronal Ensembles ◽  
Neuronal Populations ◽  
Sharp Wave ◽  
Regional Coordination ◽  
Electrophysiological Recordings ◽  
High Frequency Activity

Hippocampal-dependent memory consolidation during sleep is hypothesized to depend on the synchronization of distributed neuronal ensembles, organized by the hippocampal sharp-wave ripples (SWRs, 80 to 150 Hz), subcortical/cortical slow-wave activity (SWA, 0.5 to 4 Hz), and sleep spindles (SP, 7 to 15 Hz). However, the precise role of these interactions in synchronizing subcortical/cortical neuronal activity is unclear. Here, we leverage intracranial electrophysiological recordings from the human hippocampus, amygdala, and temporal and frontal cortices to examine activity modulation and cross-regional coordination during SWRs. Hippocampal SWRs are associated with widespread modulation of high-frequency activity (HFA, 70 to 200 Hz), a measure of local neuronal activation. This peri-SWR HFA modulation is predicted by the coupling between hippocampal SWRs and local subcortical/cortical SWA or SP. Finally, local cortical SWA phase offsets and SWR amplitudes predicted functional connectivity between the frontal and temporal cortex during individual SWRs. These findings suggest a selection mechanism wherein hippocampal SWR and cortical slow-wave synchronization governs the transient engagement of distributed neuronal populations supporting hippocampal-dependent memory consolidation.

scholarly journals Coupling between slow-waves and sharp-wave ripples organizes distributed neural activity during sleep in humans

2020 ◽  
Author(s):  
Ivan Skelin ◽  
Haoxin Zhang ◽  
Jie Zheng ◽  
Shiting Ma ◽  
Bryce A. Mander ◽  
...  
Keyword(s):  
Slow Wave ◽  
Memory Consolidation ◽  
Temporal Cortex ◽  
Slow Waves ◽  
Wave Interactions ◽  
Neuronal Ensembles ◽  
Neuronal Populations ◽  
Sharp Wave ◽  
Regional Coordination ◽  
Electrophysiological Recordings

AbstractHippocampal-dependent memory consolidation during sleep is hypothesized to depend on the synchronization of distributed neuronal ensembles, organized by the hippocampal sharp-wave ripples (SWRs, 80-150 Hz) and subcortical/cortical slow-waves (0.5-4 Hz). However, the precise role of SWR-slow-wave interactions in synchronizing subcortical/cortical neuronal activity is unclear. Here, we leverage intracranial electrophysiological recordings from the human hippocampus, amygdala, temporal and frontal cortices, to examine activity modulation and cross-regional coordination during SWRs. Hippocampal SWRs are associated with widespread modulation of high frequency activity (HFA; 70-200 Hz) a measure of local neuronal activation. This peri-SWR HFA modulation is predicted by the coupling between hippocampal SWRs and local subcortical/cortical slow-waves. Finally, local cortical slow-wave phase offsets during SWRs predicted functional connectivity between the frontal and temporal cortex. These findings suggest a selection mechanism wherein hippocampal SWR and cortical slow-wave synchronization governs the transient engagement of distributed neuronal populations supporting hippocampal-dependent memory consolidation.

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 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.

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.

Hippocampal ripples down-regulate synapses

Science ◽  
2018 ◽  
Vol 359 (6383) ◽  
pp. 1524-1527 ◽  
Author(s):  
Hiroaki Norimoto ◽  
Kenichi Makino ◽  
Mengxuan Gao ◽  
Yu Shikano ◽  
Kazuki Okamoto ◽  
...  
Keyword(s):  
Synaptic Plasticity ◽  
Neuronal Activity ◽  
Slow Wave ◽  
Down Regulation ◽  
Sharp Wave ◽  
Specific Effects ◽  
Aspartate Receptor ◽  
Specific Input ◽  
Wave States

The specific effects of sleep on synaptic plasticity remain unclear. We report that mouse hippocampal sharp-wave ripple oscillations serve as intrinsic events that trigger long-lasting synaptic depression. Silencing of sharp-wave ripples during slow-wave states prevented the spontaneous down-regulation of net synaptic weights and impaired the learning of new memories. The synaptic down-regulation was dependent on the N-methyl-d-aspartate receptor and selective for a specific input pathway. Thus, our findings are consistent with the role of slow-wave states in refining memory engrams by reducing recent memory-irrelevant neuronal activity and suggest a previously unrecognized function for sharp-wave ripples.

Sign in / Sign up

Export Citation Format

Share Document