Temporal interactions between non-rapid eye movement (NREM) sleep rhythms especially the coupling between cortical slow oscillations (SO, ∼1 Hz) and thalamic spindles (∼12 Hz) have been proposed to contribute to multi-regional interactions crucial for memory processing and cognitive ability. We investigated relationships between NREM sleep depth, sleep spindles and SO-spindle coupling regarding memory ability and memory consolidation in healthy humans. Findings underscore the functional relevance of spindle dynamics (slow versus fast), SO-phase, and most importantly NREM sleep depth for cognitive processing. Cross-frequency coupling analyses demonstrated stronger precise temporal coordination of slow spindles to SO down-state in N2 for subjects with higher general memory ability. A GLM model underscored this relationship, and furthermore that fast spindle properties were predictive of overnight memory consolidation. Our results suggest cognitive fingerprints dependent on conjoint fine-tuned SO-spindle temporal coupling, spindle properties, and brain sleep state.
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Differential thalamocortical interactions in slow and fast spindle generation: A computational model
Cortical slow oscillations (SOs) and thalamocortical sleep spindles are two prominent EEG rhythms of slow wave sleep. These EEG rhythms play an essential role in memory consolidation. In humans, sleep spindles are categorized into slow spindles (8–12 Hz) and fast spindles (12–16 Hz), with different properties. Slow spindles that couple with the up-to-down phase of the SO require more experimental and computational investigation to disclose their origin, functional relevance and most importantly their relation with SOs regarding memory consolidation. To examine slow spindles, we propose a biophysical thalamocortical model with two independent thalamic networks (one for slow and the other for fast spindles). Our modeling results show that fast spindles lead to faster cortical cell firing, and subsequently increase the amplitude of the cortical local field potential (LFP) during the SO down-to-up phase. Slow spindles also facilitate cortical cell firing, but the response is slower, thereby increasing the cortical LFP amplitude later, at the SO up-to-down phase of the SO cycle. Neither the SO rhythm nor the duration of the SO down state is affected by slow spindle activity. Furthermore, at a more hyperpolarized membrane potential level of fast thalamic subnetwork cells, the activity of fast spindles decreases, while the slow spindles activity increases. Together, our model results suggest that slow spindles may facilitate the initiation of the following SO cycle, without however affecting expression of the SO Up and Down states.
more » « less- Award ID(s):
- 1724405
- PAR ID:
- 10488677
- Editor(s):
- Cymbalyuk, Gennady S.
- Publisher / Repository:
- PloS
- Date Published:
- Journal Name:
- PLOS ONE
- Volume:
- 17
- Issue:
- 12
- ISSN:
- 1932-6203
- Page Range / eLocation ID:
- e0277772
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
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Abstract Study Objectives Synchronization of neural activity within local networks and between brain regions is a major contributor to rhythmic field potentials such as the EEG. On the other hand, dynamic changes in microstructure and activity are reflected in the EEG, for instance slow oscillation (SO) slope can reflect synaptic strength. SO-spindle coupling is a measure for neural communication. It was previously associated with memory consolidation, but also shown to reveal strong interindividual differences. In studies, weak electric current stimulation has modulated brain rhythms and memory retention. Here, we investigate whether SO-spindle coupling and SO slope during baseline sleep are associated with (predictive of) stimulation efficacy on retention performance. Methods Twenty-five healthy subjects participated in three experimental sessions. Sleep-associated memory consolidation was measured in two sessions, in one anodal transcranial direct current stimulation oscillating at subjects individual SO frequency (so-tDCS) was applied during nocturnal sleep. The third session was without a learning task (baseline sleep). The dependence on SO-spindle coupling and SO-slope during baseline sleep of so-tDCS efficacy on retention performance were investigated. Results Stimulation efficacy on overnight retention of declarative memories was associated with nesting of slow spindles to SO trough in deep nonrapid eye movement baseline sleep. Steepness and direction of SO slope in baseline sleep were features indicative for stimulation efficacy. Conclusions Findings underscore a functional relevance of activity during the SO up-to-down state transition for memory consolidation and provide support for distinct consolidation mechanisms for types of declarative memories.more » « less
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Abstract Brain rhythms of sleep reflect neuronal activity underlying sleep‐associated memory consolidation. The modulation of brain rhythms, such as the sleep slow oscillation (SO), is used both to investigate neurophysiological mechanisms as well as to measure the impact of sleep on presumed functional correlates. Previously, closed‐loop acoustic stimulation in humans targeted to the SO Up‐state successfully enhanced the slow oscillation rhythm and phase‐dependent spindle activity, although effects on memory retention have varied. Here, we aim to disclose relations between stimulation‐induced hippocampo‐thalamo‐cortical activity and retention performance on a hippocampus‐dependent object‐place recognition task in mice by applying acoustic stimulation at four estimated SO phases compared to sham condition. Across the 3‐h retention interval at the beginning of the light phase closed‐loop stimulation failed to improve retention significantly over sham. However, retention during SO Up‐state stimulation was significantly higher than for another SO phase. At all SO phases, acoustic stimulation was accompanied by a sharp increase in ripple activity followed by about a second‐long suppression of hippocampal sharp wave ripple and longer maintained suppression of thalamo‐cortical spindle activity. Importantly, dynamics of SO‐coupled hippocampal ripple activity distinguished SOUp‐state stimulation. Non‐rapid eye movement (NREM) sleep was not impacted by stimulation, yet preREM sleep duration was effected. Results reveal the complex effect of stimulation on the brain dynamics and support the use of closed‐loop acoustic stimulation in mice to investigate the inter‐regional mechanisms underlying memory consolidation.
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Abstract During NREM sleep, hippocampal sharp-wave ripple (SWR) events are thought to stabilize memory traces for long-term storage in downstream neocortical structures. Within the neocortex, a set of distributed networks organized around retrosplenial cortex (RS-network) interact preferentially with the hippocampus purportedly to consolidate those traces. Transient bouts of slow oscillations and sleep spindles in this RS-network are often observed around SWRs, suggesting that these two activities are related and that their interplay possibly contributes to memory consolidation. To investigate how SWRs interact with the RS-network and spindles, we combined cortical wide-field voltage imaging, Electrocorticography, and hippocampal LFP recordings in anesthetized and sleeping mice. Here, we show that, during SWR, “up-states” and spindles reliably co-occur in a cortical subnetwork centered around the retrosplenial cortex. Furthermore, retrosplenial transient activations and spindles predict slow gamma oscillations in CA1 during SWRs. Together, our results suggest that retrosplenial–hippocampal interaction may be a critical pathway of information exchange between the cortex and hippocampus.
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Sleep spindles appear to play an important role in learning new motor skills. Motor skill learning engages several brain regions with two important areas being the motor cortex (M1) and the cerebellum (CB). However, the neurophysiological processes in these areas during sleep, especially how spindle oscillations affect local and cross-region spiking, are not fully understood. We recorded an activity from the M1 and cerebellar cortex in eight rats during spontaneous activity to investigate how sleep spindles in these regions are related to local spiking as well as cross-region spiking. We found that M1 firing was significantly changed during both M1 and CB spindles, and this spiking occurred at a preferred phase of the spindle. On average, M1 and CB neurons showed most spiking at the M1 or CB spindle peaks. These neurons also developed a preferential phase locking to local or cross-area spindles with the greatest phase-locking value at spindle peaks; however, this preferential phase locking was not significant for cerebellar neurons when compared with CB spindles. Additionally, we found that the percentage of task-modulated cells in the M1 and CB that fired with nonuniform spike phase distribution during M1/CB spindle peaks were greater in the rats that learned a reach-to-grasp motor task robustly. Finally, we found that spindle band LFP coherence (for M1 and CB LFPs) showed a positive correlation with success rate in the motor task. These findings support the idea that sleep spindles in both the M1 and CB recruit neurons that participate in the awake task to support motor memory consolidation.
- Free Publicly Accessible Full Text
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Accepted Manuscript1.0
- Journal Article:
- https://doi.org/10.1371/journal.pone.0277772
