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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This content will become publicly available on November 30, 2024
Disturbed laterality of non-rapid eye movement sleep oscillations in post-stroke human sleep: a pilot study
Sleep is known to promote recovery post-stroke. However, there is a paucity of data profiling sleep oscillations in the post-stroke human brain. Recent rodent work showed that resurgence of physiologic spindles coupled to sleep slow oscillations (SOs) and concomitant decrease in pathological delta (
- Award ID(s):
- 2048231
- NSF-PAR ID:
- 10492697
- Publisher / Repository:
- Frontiers Media SA
- Date Published:
- Journal Name:
- Frontiers in Neurology
- Volume:
- 14
- ISSN:
- 1664-2295
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
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Abstract Epilepsy, a neurological disorder characterized by recurrent seizures, is known to be associated with impaired sleep and memory. Although the specific mechanisms underlying these impairments are uncertain, the known role of sleep in memory consolidation suggests a potential relationship may exist between seizure activity, disrupted sleep, and memory impairment. A possible mediator in this relationship is the sleep spindle, the characteristic electroencephalographic (EEG) feature of non‐rapid‐eye‐movement (NREM) sleep in humans and other mammals. Growing evidence supports the idea that sleep spindles, having thalamic origin, may mediate the process of long‐term memory storage and plasticity by generating neuronal conditions that favor these processes. To study this potential relationship, a single model in which memory, sleep, and epilepsy can be simultaneously observed is of necessity. Rodent models of epilepsy appear to fulfill this requirement. Not only do rodents express both sleep spindles and seizure‐induced sleep disruptions, but they also allow researchers to invasively study neurobiological processes both pre‐ and post‐ epileptic onset via the artificial induction of epilepsy (a practice that cannot be carried out in human subjects). However, the degree to which sleep architecture differs between rodents and humans makes direct comparisons between the two challenging. This review addresses these challenges and concludes that rodent sleep studies are useful in observing the functional roles of sleep and how they are affected by epilepsy.
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Differential thalamocortical interactions in slow and fast spindle generation: A computational modelCymbalyuk, Gennady S. (Ed.)more » « less
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.
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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 Objective Temporal coordination between oscillations enables intercortical communication and is implicated in cognition. Focal epileptic activity can affect distributed neural networks and interfere with these interactions. Refractory pediatric epilepsies are often accompanied by substantial cognitive comorbidity, but mechanisms and predictors remain mostly unknown. Here, we investigate oscillatory coupling across large‐scale networks in the developing brain.
Methods We analyzed large‐scale intracranial electroencephalographic recordings in children with medically refractory epilepsy undergoing presurgical workup (
n = 25, aged 3–21 years). Interictal epileptiform discharges (IEDs), pathologic high‐frequency oscillations (HFOs), and sleep spindles were detected. Spatiotemporal metrics of oscillatory coupling were determined and correlated with age, cognitive function, and postsurgical outcome.Results Children with epilepsy demonstrated significant temporal coupling of both IEDs and HFOs to sleep spindles in discrete brain regions. HFOs were associated with stronger coupling patterns than IEDs. These interactions involved tissue beyond the clinically identified epileptogenic zone and were ubiquitous across cortical regions. Increased spatial extent of coupling was most prominent in older children. Poor neurocognitive function was significantly correlated with high IED–spindle coupling strength and spatial extent; children with strong pathologic interactions additionally had decreased likelihood of postoperative seizure freedom.
Significance Our findings identify pathologic large‐scale oscillatory coupling patterns in the immature brain. These results suggest that such intercortical interactions could predict risk for adverse neurocognitive and surgical outcomes, with the potential to serve as novel therapeutic targets to restore physiologic development.
