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 Interaction of Hippocampal Ripples and Cortical Slow Waves Leads to Coordinated Large-Scale Sleep Rhythm

2019 ◽  
Author(s):  
Pavel Sanda ◽  
Paola Malerba ◽  
Xi Jiang ◽  
Giri P. Krishnan ◽  
Sydney Cash ◽  
...  
Keyword(s):  
Slow Wave ◽  
Large Scale ◽  
State Transition ◽  
Slow Wave Sleep ◽  
Slow Waves ◽  
Spatiotemporal Pattern ◽  
Spatiotemporal Structure ◽  
Cortical Input ◽  
Up States ◽  
Intracranial Recordings

AbstractThe dialogue between cortex and hippocampus is known to be crucial for sleep dependent consolidation of long lasting memories. During slow wave sleep memory replay depends on slow oscillation (SO) and spindles in the (neo)cortex and sharp wave-ripple complexes (SWR) in the hippocampus, however, the mechanisms underlying interaction of these rhythms are poorly understood. Here, we examined the interaction between cortical SOs and hippocampal SWRs in a computational 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 SO (Down-to-Up-state transition) and that cortical input to hippocampus was crucial to maintain this relationship. Ripples influenced the spatiotemporal structure of cortical SO and duration of the Up/Down-states. In particular, ripples were capable of synchronizing Up-to-Down state transition events across the cortical network. Slow waves had a tendency to initiate at cortical locations receiving hippocampal ripples, and these “initiators” were able to influence sequential reactivation within cortical Up states. We concluded that during slow wave sleep, hippocampus and neocortex maintain a complex interaction, where SOs bias the onset of ripples, while ripples influence the spatiotemporal pattern of SOs.

scholarly journals Hippocampal Sharp Wave-Ripples Linked to Slow Oscillations in Rat Slow-Wave Sleep

2006 ◽  
Vol 96 (1) ◽  
pp. 62-70 ◽  
Author(s):  
Matthias Mölle ◽  
Oxana Yeshenko ◽  
Lisa Marshall ◽  
Susan J. Sara ◽  
Jan Born
Keyword(s):  
Slow Wave ◽  
Slow Wave Sleep ◽  
Temporal Dynamics ◽  
Slow Oscillation ◽  
Network Activity ◽  
Event Correlation ◽  
Slow Oscillations ◽  
Sharp Wave ◽  
Neuronal Network Activity ◽  
Up And Down States

Slow oscillations originating in the prefrontal neocortex during slow-wave sleep (SWS) group neuronal network activity and thereby presumably support the consolidation of memories. Here, we investigated whether the grouping influence of slow oscillations extends to hippocampal sharp wave-ripple (SPW) activity thought to underlie memory replay processes during SWS. The prefrontal surface EEG and multiunit activity (MUA), along with hippocampal local field potentials (LFP) from CA1, were recorded in rats during sleep. Average spindle and ripple activity and event correlation histograms of SPWs were calculated, time-locked to half-waves of slow oscillations. Results confirm decreased prefrontal MUA and spindle activity during EEG slow oscillation negativity and increases in this activity during subsequent positivity. A remarkably close temporal link was revealed between slow oscillations and hippocampal activity, with ripple activity and SPWs being also distinctly decreased during negative half-waves and increased during slow oscillation positivity. Fine-grained analyses of temporal dynamics revealed for the slow oscillation a phase delay of approximately 90 ms with reference to up and down states of prefrontal MUA, and of only approximately 60 ms with reference to changes in SPWs, indicating that up and down states in prefrontal MUA precede corresponding changes in hippocampal SPWs by approximately 30 ms. Results support the notion that the depolarizing surface-positive phase of the slow oscillation and the associated up state of prefrontal excitation promotes hippocampal SPWs via efferent pathways. The preceding disfacilitation of hippocampal events temporally coupled to the negative slow oscillation half-wave appears to serve a synchronizing role in this neocorticohippocampal interplay.

scholarly journals Schizophrenia-associated variation at ZNF804A correlates with altered experience-dependent dynamics of sleep slow-waves and spindles in healthy young adults

2020 ◽  
Author(s):  
Ullrich Bartsch ◽  
Laura J Corbin ◽  
Charlotte Hellmich ◽  
Michelle Taylor ◽  
Kayleigh E Easey ◽  
...  
Keyword(s):  
Slow Wave ◽  
Memory Consolidation ◽  
Neural Circuit ◽  
Activity Patterns ◽  
Nrem Sleep ◽  
Slow Waves ◽  
Network Activity ◽  
Healthy Population ◽  
Adult Males ◽  
Performance Improvements

ABSTRACTBackgroundThe rs1344706 polymorphism in ZNF804A is robustly associated with schizophrenia (SZ), yet brain and behavioral phenotypes related to this variant have not been extensively characterized. In turn, SZ is associated with abnormal non-rapid eye movement (NREM) sleep neurophysiology. To examine whether rs1344706 is associated with intermediate neurophysiological traits in the absence of disease, we assessed the relationship between genotype, sleep neurophysiology, and sleep-dependent memory consolidation in healthy participants.MethodsWe recruited healthy adult males, with no history of psychiatric disorder, from the Avon Longitudinal Study of Parents and Children (ALSPAC) birth cohort. Participants were homozygous for either the SZ-associated ‘A’ allele (N=25) or the alternative ‘C’ allele (N=22) at rs1344706. Actigraphy, polysomnography (PSG) and a motor sequencing task (MST) were used to characterize daily activity patterns, sleep neurophysiology and sleep-dependent memory consolidation.ResultsAverage MST learning and sleep-dependent performance improvements were similar across genotype groups, but with increased variability in the AA group. CC participants showed increased slow-wave and spindle amplitudes, plus augmented coupling of slow-wave activity across recording electrodes after learning. Slow-waves and spindles in those with the AA genotype were insensitive to learning, whilst slow-wave coherence decreased following MST training.ConclusionWe describe evidence that rs1344706 polymorphism in ZNF804A is associated with changes in experience- and sleep-dependent, local and distributed neural network activity that supports offline information processing during sleep in a healthy population. These findings highlight the utility of sleep neurophysiology in mapping the impacts of SZ-associated variants on neural circuit oscillations and function.

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 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 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 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 0352 A Large-Scale EEG Study at Home to Objectivise Effects of Ageing on Slow Wave Sleep and Process S

SLEEP ◽  
2020 ◽  
Vol 43 (Supplement_1) ◽  
pp. A133-A134
Author(s):  
K El Kanbi ◽  
V Thorey ◽  
L Artemis ◽  
A Chouraki ◽  
T Trichet ◽  
...  
Keyword(s):  
Slow Wave ◽  
Large Scale ◽  
Slow Wave Sleep ◽  
Large Population ◽  
Nrem Sleep ◽  
Slow Waves ◽  
High Signal ◽  
Eeg Signals ◽  
Sleep Complaints ◽  
Loop Procedure

Abstract Introduction Several studies have shown slow wave sleep (SWS) is altered with ageing. However, most of these studies have been conducted in-lab and usually over a single night. In this study, we assessed the evolution of process S with ageing by analysing the dynamics of endogenous and auditory-evoked slow waves in a large population. Methods 300 participants (200 M, 20 - 70 y.o.) were selected from volunteers users wearing a sleep headband for at least 3 nights, meeting the criteria of high signal quality and having no subjective sleep complaints nor being shift-workers. The Dreem headband is a connected device able to monitor EEG signals as well as pulse and movement and performs sleep staging in real-time automatically. Slow waves were detected as large negative deflections on the filtered EEG signals during NREM sleep. The auditory evoked slow waves were done using a previously validated closed-loop procedure. Results In our study, age was strongly correlated with N3 sleep duration (r=-0.34, p<0.0001), slow wave amplitude (r=-0.25, p<0.0001), and slow wave density (r=-0.40, p<0.0001). The slope of the slow wave activity, representing the process S here, was significantly decreased (r=-0.32, p<0.0001). This effect was mainly due to changes in the density of slow waves in the first 2 hours of sleep (r=-0.41, p<0.0001). Finally, our results show a decrease in the probability of auditory evoked slow waves (r=-0.43, p<0.0001). Conclusion These results confirmed the in-lab studies showing a heterogeneous alteration of homoeostatic process S with age, as well as a general decrease of slow wave occurrences, that is observed in parallel of a decrease of the probability of evoking slow waves, suggesting a global change in the system responsible for slow wave generation. Support This study was supported by Dreem sas and ANR, FLAG ERA 2015, HPB SLOW-Dyn

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.

scholarly journals Intra- and interregional cortical interactions related to sharp-wave ripples and dentate spikes

2017 ◽  
Vol 117 (2) ◽  
pp. 556-565 ◽  
Author(s):  
Drew B. Headley ◽  
Vasiliki Kanta ◽  
Denis Paré
Keyword(s):  
Memory Consolidation ◽  
Cortical Neurons ◽  
Slow Wave Sleep ◽  
Dorsal Hippocampus ◽  
Gamma Oscillations ◽  
Sharp Wave ◽  
Up States ◽  
Gamma Coherence ◽  
Cortical Regions ◽  
The Relationship

The hippocampus generates population events termed sharp-wave ripples (SWRs) and dentate spikes (DSs). While little is known about DSs, SWR-related hippocampal discharges during sleep are thought to replay prior waking activity, reactivating the cortical networks that encoded the initial experience. During slow-wave sleep, such reactivations likely occur during up-states, when most cortical neurons are depolarized. However, most studies have examined the relationship between SWRs and up-states measured in single neocortical regions. As a result, it is currently unclear whether SWRs are associated with particular patterns of widely distributed cortical activity. Additionally, no such investigation has been carried out for DSs. The present study addressed these questions by recording SWRs and DSs from the dorsal hippocampus simultaneously with prefrontal, sensory (visual and auditory), perirhinal, and entorhinal cortices in naturally sleeping rats. We found that SWRs and DSs were associated with up-states in all cortical regions. Up-states coinciding with DSs and SWRs exhibited increased unit activity, power in the gamma band, and intraregional gamma coherence. Unexpectedly, interregional gamma coherence rose much more strongly in relation to DSs than to SWRs. Whereas the increase in gamma coherence was time locked to DSs, that seen in relation to SWRs was not. These observations suggest that SWRs are related to the strength of up-state activation within individual regions throughout the neocortex but not so much to gamma coherence between different regions. Perhaps more importantly, DSs coincided with stronger periods of interregional gamma coherence, suggesting that they play a more important role than previously assumed. NEW & NOTEWORTHY Off-line cortico-hippocampal interactions are thought to support memory consolidation. We surveyed the relationship between hippocampal sharp-wave ripples (SWRs) and dentate spikes (DSs) with up-states across multiple cortical regions. SWRs and DSs were associated with increased cortical gamma oscillations. Interregional gamma coherence rose much more strongly in relation to DSs than to SWRs. Moreover, it was time locked to DSs but not SWRs. These results have important implications for current theories of systems memory consolidation during sleep.

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