Sleep spindles mediate hippocampal-neocortical coupling during long-duration ripples

Sleep is pivotal for memory consolidation. According to two-stage accounts, memory traces are gradually translocated from hippocampus to neocortex during non-rapid-eye-movement (NREM) sleep. Mechanistically, this information transfer is thought to rely on interactions between thalamocortical spindles and hippocampal ripples. To test this hypothesis, we analyzed intracranial and scalp Electroencephalography sleep recordings from pre-surgical epilepsy patients. We first observed a concurrent spindle power increase in hippocampus (HIPP) and neocortex (NC) time-locked to individual hippocampal ripple events. Coherence analysis confirmed elevated levels of hippocampal-neocortical spindle coupling around ripples, with directionality analyses indicating an influence from NC to HIPP. Importantly, these hippocampal-neocortical dynamics were particularly pronounced during long-duration compared to short-duration ripples. Together, our findings reveal a potential mechanism underlying active consolidation, comprising a neocortical-hippocampal-neocortical reactivation loop initiated by the neocortex. This hippocampal-cortical dialogue is mediated by sleep spindles and is enhanced during long-duration hippocampal ripples.

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Sleep spindles mediate hippocampal-neocortical coupling during sharp-wave ripples

10.1101/712463 ◽

2019 ◽

Cited By ~ 1

Author(s):

Hong-Viet. V. Ngo ◽

Juergen Fell ◽

Bernhard P. Staresina

Keyword(s):

Eye Movement ◽

Information Transfer ◽

Communication Channels ◽

Nrem Sleep ◽

Sleep Spindles ◽

Coherence Analysis ◽

Time Frequency ◽

Target Sites ◽

Spindle Power

AbstractSleep is pivotal for the consolidation of memories [1]. According to two-stage accounts, experiences are temporarily stored in the hippocampus and gradually translocated to neocortical sites during non-rapid-eye-movement (NREM) sleep [2,3]. Mechanistically, information transfer is thought to rely on interactions between thalamocortical spindles and hippocampal ripples. In particular, spindles may open precisely-timed communication channels, across which reactivation patterns may travel between the hippocampus and cortical target sites when ripples occur. To test this hypothesis, we first derived time-frequency representations (TFRs) in hippocampus (HIPP) and at scalp electrode Cz (neocortex, NC) time-locked to individual hippocampal ripple events. Compared to matched ripple-free intervals, results revealed a concurrent increase in spindle power both in HIPP and NC. As revealed by coherence analysis, hippocampal-neocortical coupling was indeed enhanced in the spindle band around ripples. Finally, we examined the directionality of spindle coupling and observed a strong driving effect from NC to HIPP. Specifically, ∼250 ms prior to the HIPP ripple, NC spindles emerge and entrain HIPP spindles. Both regions then remain synchronised until ∼500 ms after the ripple. Consistent with recent rodent work, these findings suggest that active consolidation is initiated by neocortex and draws on neocortical-hippocampal-neocortical reactivation loops [4], with a role of sleep spindles in mediating this process.

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Shining a Light on the Mechanisms of Sleep for Memory Consolidation

Current Sleep Medicine Reports ◽

10.1007/s40675-021-00204-3 ◽

2021 ◽

Author(s):

Michelle A. Frazer ◽

Yesenia Cabrera ◽

Rockelle S. Guthrie ◽

Gina R. Poe

Keyword(s):

Rem Sleep ◽

Neural Activity ◽

Memory Consolidation ◽

Strong Support ◽

Nrem Sleep ◽

Future Research ◽

Sleep Spindles ◽

Slow Oscillations ◽

Theta Waves ◽

Learning Tasks

Abstract Purpose of review This paper reviews all optogenetic studies that directly test various sleep states, traits, and circuit-level activity profiles for the consolidation of different learning tasks. Recent findings Inhibiting or exciting neurons involved either in the production of sleep states or in the encoding and consolidation of memories reveals sleep states and traits that are essential for memory. REM sleep, NREM sleep, and the N2 transition to REM (characterized by sleep spindles) are integral to memory consolidation. Neural activity during sharp-wave ripples, slow oscillations, theta waves, and spindles are the mediators of this process. Summary These studies lend strong support to the hypothesis that sleep is essential to the consolidation of memories from the hippocampus and the consolidation of motor learning which does not necessarily involve the hippocampus. Future research can further probe the types of memory dependent on sleep-related traits and on the neurotransmitters and neuromodulators required.

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Nonrapid eye movement sleep electroencephalographic oscillations in idiopathic rapid eye movement sleep behavior disorder: a study of sleep spindles and slow oscillations

SLEEP ◽

10.1093/sleep/zsaa160 ◽

2020 ◽

Author(s):

Jun-Sang Sunwoo ◽

Kwang Su Cha ◽

Jung-Ick Byun ◽

Jin-Sun Jun ◽

Tae-Joon Kim ◽

...

Keyword(s):

Eye Movement ◽

Rem Sleep ◽

Rem Sleep Behavior Disorder ◽

Behavior Disorder ◽

Nrem Sleep ◽

Sleep Spindles ◽

Rapid Eye Movement ◽

Sleep Behavior ◽

Slow Oscillations ◽

Lower Amplitude

Abstract Study Objectives We investigated electroencephalographic (EEG) slow oscillations (SOs), sleep spindles (SSs), and their temporal coordination during nonrapid eye movement (NREM) sleep in patients with idiopathic rapid eye movement (REM) sleep behavior disorder (iRBD). Methods We analyzed 16 patients with video-polysomnography-confirmed iRBD (age, 65.4 ± 6.6 years; male, 87.5%) and 10 controls (age, 62.3 ± 7.5 years; male, 70%). SSs and SOs were automatically detected during stage N2 and N3. We analyzed their characteristics, including density, frequency, duration, and amplitude. We additionally identified SO-locked spindles and examined their phase distribution and phase locking with the corresponding SO. For inter-group comparisons, we used the independent samples t-test or Wilcoxon rank-sum test, as appropriate. Results The SOs of iRBD patients had significantly lower amplitude, longer duration (p = 0.005 for both), and shallower slope (p < 0.001) than those of controls. The SS power of iRBD patients was significantly lower than that of controls (p = 0.002), although spindle density did not differ significantly. Furthermore, SO-locked spindles of iRBD patients prematurely occurred during the down-to-up-state transition of SOs, whereas those of controls occurred at the up-state peak of SOs (p = 0.009). The phase of SO-locked spindles showed a positive correlation with delayed recall subscores (p = 0.005) but not with tonic or phasic electromyography activity during REM sleep. Conclusions In this study, we found abnormal EEG oscillations during NREM sleep in patients with iRBD. The impaired temporal coupling between SOs and SSs may reflect early neurodegenerative changes in iRBD.

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Reply to Ludwig et al.: A potential mechanism for intracranial cerebrospinal fluid accumulation during long-duration spaceflight

Proceedings of the National Academy of Sciences ◽

10.1073/pnas.1913041116 ◽

2019 ◽

Vol 116 (41) ◽

pp. 20265-20266

Author(s):

Peter zu Eulenburg ◽

Angelique Van Ombergen ◽

Elena Tomilovskaya ◽

Floris L. Wuyts

Keyword(s):

Cerebrospinal Fluid ◽

Potential Mechanism ◽

Fluid Accumulation ◽

Long Duration

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0086 Daytime Napping and Memory Consolidation of Novel Word Learning in Children and Adults

SLEEP ◽

10.1093/sleep/zsaa056.084 ◽

2020 ◽

Vol 43 (Supplement_1) ◽

pp. A35-A35

Author(s):

E van Rijn ◽

S A Walker ◽

V C Knowland ◽

S A Cairney ◽

A D Gouws ◽

...

Keyword(s):

White Matter ◽

Memory Consolidation ◽

Slow Wave Sleep ◽

Diffusion Tensor ◽

Brain Connectivity ◽

Nrem Sleep ◽

Sleep Spindles ◽

Adults And Children ◽

Structural Brain ◽

Novel Words

Abstract Introduction Memory for novel words benefits from sleep, particularly non-rapid eye movement (NREM) sleep and its features, such as sleep spindles and slow oscillations. This is consistent with systems consolidation models, in which sleep supports transfer from hippocampal to neocortical memory networks. Larger amounts of slow wave sleep in children has been proposed to account for enhanced consolidation effects, but such studies have typically focused on nocturnal sleep. We examined whether daytime naps benefit word retention in adults and children aged 10–12 years, and whether this relationship in children is affected by differences in white matter pathway microstructure. We hypothesized that the link between memory consolidation and structural brain connectivity will be mediated by the degree of sleep spindles during the nap. Methods Adults (N = 31; mean age = 20.91, SD = 1.55) and children (N = 38; mean age = 11.95, SD = 0.88) learned spoken novel words, followed by a 90-minute nap opportunity monitored with polysomnography. Memory for the words was tested pre- and post-nap. Children’s structural brain connectivity was measured using diffusion tensor imaging (DTI). Results Word memory was preserved following sleep in adults, while an adult wake control condition showed deterioration. Similarly, in children memory performance was stable over the nap, with wake control data currently being collected. Analyses relating behavioral changes over the nap to NREM sleep features and structural brain connectivity will be presented. Conclusion In line with sleep-dependent memory consolidation models, daytime naps protect novel words from forgetting in adults and children. Examining potential relationships between nap-based consolidation and structural integrity has important theoretical implications, given the increase in brain connectivity in language areas during childhood, as well as white matter alterations in developmental populations. Support This research was supported by the UK Economic and Social Research Council, grant no. ES/N009924/1.

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Iron-Deficiency Anemia is Associated with Altered Characteristics of Sleep Spindles in NREM Sleep in Infancy

Neurochemical Research ◽

10.1007/s11064-007-9396-8 ◽

2007 ◽

Vol 32 (10) ◽

pp. 1665-1672 ◽

Cited By ~ 25

Author(s):

Patricio Peirano ◽

Cecilia Algarín ◽

Marcelo Garrido ◽

Diógenes Algarín ◽

Betsy Lozoff

Keyword(s):

Iron Deficiency ◽

Iron Deficiency Anemia ◽

Nrem Sleep ◽

Deficiency Anemia ◽

Sleep Spindles

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Sleep spindles, ripples, and interictal epileptiform discharges in the human anterior and mediodorsal thalamus

10.1101/2021.08.12.456047 ◽

2021 ◽

Author(s):

Orsolya Szalardy ◽

Peter Simor ◽

Peter Przemyslaw Ujma ◽

Zsofia Jordan ◽

Laszlo Halasz ◽

...

Keyword(s):

Neural Plasticity ◽

Nrem Sleep ◽

Cortical Activity ◽

Sleep Spindles ◽

Time Frequency ◽

Scalp Eeg ◽

Epileptiform Discharges ◽

Interictal Epileptiform Discharges ◽

Human Thalamus ◽

Result Show

Sleep spindles are major oscillatory components of Non-Rapid Eye Movement (NREM) sleep, reflecting hyperpolarization-rebound sequences of thalamocortical neurons, the inhibition of which is caused by the NREM-dependent activation of GABAergic neurons in the reticular thalamic nucleus. Reports suggest a link between sleep spindles and several forms of interictal epileptic discharges (IEDs) which are considered as expressions of pathological off-line neural plasticity in the central nervous system. Here we investigated the relationship between thalamic sleep spindles, IEDs and ripples in the anterior and mediodorsal nuclei (ANT and MD) of epilepsy patients. Whole-night LFP from the ANT and MD were co-registered with scalp EEG/polysomnography by using externalized leads in 15 epilepsy patients undergoing Deep Brain Stimulation protocol. Slow (~12 Hz) and fast (~14 Hz) sleep spindles were present in the human ANT and MD. Roughly, one third of thalamic sleep spindles were associated with IEDs or ripples. Both IED- and ripple-associated spindles were longer than pure spindles. IED-associated thalamic sleep spindles were characterized by broadband increase in thalamic and cortical activity, both below and above the spindle frequency range, whereas ripple-associated thalamic spindles exceeded pure spindles in terms of 80-200 Hz thalamic, but not cortical activity as indicated by time-frequency analysis. These result show that thalamic spindles coupled with IEDs are reflected at the scalp slow and beta-gamma oscillation as well. IED density during sleep spindles in the MD, but not in the ANT was identified as correlates of years spent with epilepsy, whereas no signs of pathological processes were correlated with measures of ripple and spindle association. Furthermore, the density of ripple-associated sleep spindles in the ANT showed a positive correlation with general intelligence. Our findings indicate the complex and multifaceted role of the human thalamus in sleep spindle-related physiological and pathological neural plasticity.

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Contribution of REM sleep and N2 sleep spindles to procedural memory consolidation in Vipassana meditators and non-meditating controls.

10.31231/osf.io/e4zr2 ◽

2017 ◽

Author(s):

Elizaveta Solomonova ◽

Simon Dubé ◽

Cloé Blanchette-Carrière ◽

Arnaud Samson-Richer ◽

Michelle Carr ◽

...

Keyword(s):

Eye Movement ◽

Rem Sleep ◽

Memory Consolidation ◽

Nrem Sleep ◽

Procedural Memory ◽

Sleep Stages ◽

Sleep Spindles ◽

Meditation Practice ◽

Rapid Eye Movement ◽

Vipassana Meditation

Study objectives: Rapid eye movement (REM) sleep, non-rapid eye movement (NREM) sleep, and sleep spindles are all implicated in the consolidation of procedural memories. The relative contributions of sleep stages and sleep spindles was previously shown to depend on individual differences in task processing. Experience with Vipassana meditation is one such individual difference that has not been investigated in relation to sleep. Vipassana meditation is a form of mental training that enhances proprioceptive and somatic awareness and alters attentional style. The goal was thus to examine a potential moderating role for Vipassana meditation experience on sleep-dependent procedural memory consolidation.Methods: Groups of Vipassana meditation practitioners (N=20) and matched meditation-naïve controls (N=20) slept for a single daytime nap in the laboratory. Before and after the nap they completed a procedural task on the Wii Fit balance platform.Results: Meditators performed slightly better on the task before the nap, but the two groups improved similarly after sleep. The groups showed different patterns of sleep-dependent procedural memory consolidation: in meditators task learning was negatively correlated with density of fast and positively correlated with density of slow occipital spindles, while in controls task improvement was associated with increases in REM sleep. Meditation practitioners had a lower density of sleep spindles, especially in occipital regions.Conclusions: Results suggest that neuroplastic changes associated with sustained meditation practice may alter overall sleep architecture and reorganize sleep-dependent patterns of memory consolidation. The lower density of spindles in meditators may mean that meditation practice compensates for some of the memory functions of sleep.

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Enhancement of hippocampal-thalamocortical temporal coordination during slow-frequency long-duration anterior thalamic spindles

10.1101/2021.10.03.462943 ◽

2021 ◽

Author(s):

Zahra Alizadeh ◽

Amin Azimi ◽

Maryam Ghorbani

Keyword(s):

Information Transfer ◽

Temporal Association ◽

Strongly Coupled ◽

Neuronal Interactions ◽

Long Duration ◽

Hippocampal Activity ◽

Spatial Exploration ◽

Shed Light ◽

Slow Frequency

AbstractTemporal nesting of cortical slow oscillations (SO), thalamic spindles and hippocampal ripples indicates the succession of regional neuronal interactions required for memory consolidation. However how the thalamic activity during spindles organizes hippocampal dynamics remains largely undetermined. We analyzed simultaneous recordings of anterodorsal thalamus and CA1 in mice to determine the contribution of thalamic spindles in cross-regional synchronization. Our results indicated that temporal hippocampo-thalamocortical coupling were more enhanced during slower and longer thalamic spindles. Additionally, spindles occurring closer to SO trough were more strongly coupled to ripples. We found that the temporal association between CA1 spiking/ripples and thalamic spindles was stronger following spatial exploration compared to baseline sleep. We further developed a hippocampal-thalamocortical model to explain the mechanism underlying the duration and frequency-dependent coupling of thalamic spindles to hippocampal activity. Our findings shed light on our understanding of the functional role of thalamic activity during spindles on multi-regional information transfer.

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0324 Effect of Sleep Restriction on Sleep Electroencephalogram Waveforms in Adolescents

SLEEP ◽

10.1093/sleep/zsaa056.321 ◽

2020 ◽

Vol 43 (Supplement_1) ◽

pp. A123-A123

Author(s):

I G Campbell ◽

A Cruz Basilio ◽

Z Y Zhang ◽

N Darchia ◽

I Feinberg

Keyword(s):

Total Sleep Time ◽

Nrem Sleep ◽

Sleep Time ◽

Sleep Restriction ◽

Sleep Spindles ◽

Alpha Power ◽

The Past ◽

Delta Power ◽

Eeg Power ◽

Eeg Recordings

Abstract Introduction Over the past 18 years, our laboratory has been carrying out longitudinal studies of sleep and sleep need across adolescence. Our current study uses a dose-response design to examine daytime performance and sleep EEG after varied sleep durations. Here we present results for 1-30 Hz EEG power in NREM and REM sleep. Methods Home EEG recording in children 10-16 years old (N=77, mean age = 13.2). Adhering to their habitual rise time participants kept an assigned TIB schedule of 7, 8.5, or 10 hours for four consecutive nights. Participants completed all three conditions each year of the 3 year study. EEG recordings from the fourth night of each condition were scored and analyzed with FFT. Results Reducing TIB from 10 to 7 hours effectively decreased total sleep time (TST) from an average of 531 min to an average of 407 min. Decreasing TIB (from 10 to 7 h) produced a small increase (4.6%, p=0.0004) in delta (1-4 Hz) power and a larger decrease (9.0%, p=0.0032) in alpha (8-11 Hz) power in the first 5 h of NREM sleep. In REM periods 2 and 3, the same TIB reduction also increased (12.1%, p<0.0001) delta power and decreased (14.2%, p<0.0001) alpha power. Decreasing TIB reduced (11%, p<0.0001) sigma (11-15 Hz) power in the first 5h of NREM sleep and reduced (28%, p<0.0001) all night NREM sigma energy. Conclusion Reducing TST changes EEG power in several frequency bands. The increase in NREM delta power, expected from homeostatic models, may be too small to be biologically significant. The larger loss of sigma power may be of greater consequence. Sigma frequency activity is an indicator of sleep spindles which have been affected in aging, learning, memory and psychopathology. The sigma response to sleep restriction could be used to study these relations. Support PHS grant R01 HL116490 supported this work.

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