Entrainment to sleep spindles reflects dissociable patterns of connectivity between cortex and basal ganglia

Mizrahi-Kliger, Aviv; Kaplan, Alexander; Israel, Zvi; Bergman, Hagai

doi:10.1016/j.celrep.2022.111367

Cited by 7 publications

(9 citation statements)

References 58 publications

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“…In addition, we found evidence that this pathophysiological pattern during the NREM phase may be associated with impaired sleep quality, as beta power during NREM sleep showed robust correlations with the PSQI, a validated assessment of sleep disturbance. This correlation was most robust in the NREM2 stage of sleep, potentially because N2 sleep occupied the longest duration of sleep time (over 60% in our patient cohort) and that physiologically important sleep oscillations such as spindles and K-complexes are typically most prominent in N2 sleep 26 . When comparing beta power across sleep cycles in the PD cohort, we found a relative decline in beta power from N1 sleep, where it was close to that in wakefulness, to N3 sleep, where it was more similar to that in dystonia.…”

Section: Discussionmentioning

confidence: 81%

Pathological pallidal beta activity in Parkinson’s disease is sustained during sleep and associated with sleep disturbance

Yin,

Ma,

et al. 2023

Nat Commun

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Parkinson’s disease (PD) is associated with excessive beta activity in the basal ganglia. Brain sensing implants aim to leverage this biomarker for demand-dependent adaptive stimulation. Sleep disturbance is among the most common non-motor symptoms in PD, but its relationship with beta activity is unknown. To investigate the clinical potential of beta activity as a biomarker for sleep quality in PD, we recorded pallidal local field potentials during polysomnography in PD patients off dopaminergic medication and compared the results to dystonia patients. PD patients exhibited sustained and elevated beta activity across wakefulness, rapid eye movement (REM), and non-REM sleep, which was correlated with sleep disturbance. Simulation of adaptive stimulation revealed that sleep-related beta activity changes remain unaccounted for by current algorithms, with potential negative outcomes in sleep quality and overall quality of life for patients.

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Section: Discussionmentioning

confidence: 81%

Pathological pallidal beta activity in Parkinson’s disease is sustained during sleep and associated with sleep disturbance

Yin,

Ma,

et al. 2023

Nat Commun

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“…In the context of motor sequence learning (MSL), recent EEG-fMRI sleep studies have revealed that MSL consolidation relies on the synchronized local reprocessing of new information, time-locked to spindles, across segregated but inter-connected brain regions that were involved in the initial learning process per se, such as the hippocampus, striatum, thalamus and motor-related cortical areas 7,8,11,13 . Given the anatomical selective distribution and co-occurrence of spindles in the aforementioned brain regions 8,30,31 , recent work has reported increased functional connectivity within this network by showing enhanced hippocampal-cortical and striatal-cortical communication during sleep spindles 7,[31][32][33] . More specifically, using deep brain EEG coherence analyses, Boutin and colleagues 7 revealed that oscillatory synchrony in the spindle frequency band may reflect the cross-structural reactivation and communication between learning-related brain regions during sleep consolidation.…”

Section: Introductionmentioning

confidence: 99%

Clustering and temporal organization of sleep spindles underlie motor memory consolidation

Boutin

Gabitov

Pinsard

et al. 2022

Preprint

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Sleep benefits motor memory consolidation, which is mediated by sleep spindle activity and associated memory reactivations during non-rapid eye movement (NREM) sleep. However, the particular role of NREM2 and NREM3 sleep spindles and the mechanisms triggering this memory consolidation process remain controversial. Here, simultaneous electroencephalographic and functional magnetic resonance imaging (EEGfMRI) recordings were collected during night-time sleep following the learning of a motor sequence task. Adopting a time-based clustering approach, we provide evidence that spindles iteratively occur within clustered and temporally organized patterns during both NREM2 and NREM3 sleep. However, the clustering of spindles in trains is related to motor memory consolidation during NREM2 sleep only. Altogether, our findings suggest that the clustering and rhythmic occurrence of spindles during NREM2 sleep may serve as an intrinsic rhythmic sleep mechanism for the timed reactivation and subsequent consolidation of motor memories, through synchronized oscillatory activity within a subcortical-cortical network involved during learning.

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“…Spindle events detection was performed with an algorithm which was widely applied and verified in previous studies of LFP and EEG 10,19 . Beta bursts were identified as previous illustrated 20 .…”

Section: Methodsmentioning

confidence: 99%

“…However, evidence on the role of increased beta oscillation in insomnia is still missing in human patients, as most existing studies with LFP recordings from human patients show that the beta oscillation was significantly reduced during NREM sleep compared to REM or awake 8,9 . Moreover, as wide spread sleep spindles, which were transient waxing and waning 11-16 Hz oscillations prominent during NREM stage 2 sleep, were found in different basal ganglia nucleus in healthy non-human primate 10 . Whether they are dissociable or are interfered by pathological beta bursts, the frequency of which were overlapped with spindles, remained unclear.…”

Section: Introductionmentioning

confidence: 93%

“…A recent study based on non-human primate model of Parkinson's disease suggested that beta oscillations (13-30Hz) in the basal ganglia increased during NREM sleep in Parkinsonian state, which was associated with sleep fragmentation and reduction in slow wave activities 7 . However, evidence on the role of increased beta oscillation in insomnia is still missing in human patients, as most existing studies with LFP recordings from human patients show that the beta oscillation was significantly reduced during NREM sleep compared to REM or awake 8,9 10 . Whether they are dissociable or are interfered by pathological beta bursts, the frequency of which were overlapped with spindles, remained unclear.…”

Section: Introductionmentioning

confidence: 99%

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Neurophysiological Features of STN LFP underlying Sleep Fragmentation in Parkinson’s Disease

Zhang,

Yu,

Chen

et al. 2023

Preprint

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Background Sleep fragmentation is a persistent problem throughout the course of Parkinson's disease (PD). However, the related neurophysiological patterns and the underlying mechanisms remained unclear. Method We recorded subthalamic nucleus (STN) local field potentials (LFPs) using DBS with real-time wireless recording capacity from thirteen PD patients undergoing a one-night polysomnography recording, one month after DBS surgery before initial programming and when the patients were Off-Medication. The STN LFP features that characterized different sleep stages, correlated with arousal and sleep fragmentation index, and preceded stage transitions during N2 and REM sleep were analyzed. Results Both beta and low gamma oscillations in NREM sleep increased with the severity of sleep disturbance (arousal index (ArI)-betaNREM: r=0.9,p=0.0001) and sleep fragmentation index (SFI)-betaNREM: r=0.6,p=0.0301; SFI-gammaNREM: r=0.6,p=0.0324). We next examined the low-to-high power ratio, which was the power ratio of theta oscillations to beta and low gamma oscillations, and found it to be an indicator of sleep fragmentation (ArI-LHPRNREM: r=-0.8,p=0.0053; ArI-LHPRREM: r=-0.6,p=0.0373; SFI-LHPRNREM: r=-0.7,p=0.0204; SFI-LHPRREM: r=-0.6,p=0.0428). In addition, long beta bursts (>0.25s) during NREM stage 2 were found preceding the completion of transition to stages with more cortical activities (towards Wake/N1/REM compared with towards N3 (p<0.01)) and negatively correlated with STN spindles，which were detected in STN LFPs with peak frequency distinguishable from long beta bursts (STN spindle: 11.5Hz, STN long beta bursts: 23.8Hz), in occupation during NREM sleep (beta = -0.24, p<0.001). Conclusion Features of STN LFPs help explain neurophysiological mechanisms underlying sleep fragmentations in PD, which can inform new intervention for sleep dysfunction.

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Entrainment to sleep spindles reflects dissociable patterns of connectivity between cortex and basal ganglia

Cited by 7 publications

References 58 publications

Pathological pallidal beta activity in Parkinson’s disease is sustained during sleep and associated with sleep disturbance

Pathological pallidal beta activity in Parkinson’s disease is sustained during sleep and associated with sleep disturbance

Clustering and temporal organization of sleep spindles underlie motor memory consolidation

Neurophysiological Features of STN LFP underlying Sleep Fragmentation in Parkinson’s Disease

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