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

2019 ◽  
Author(s):  
Hong-Viet. V. Ngo ◽  
Juergen Fell ◽  
Bernhard P. Staresina

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.

eLife ◽  
2020 ◽  
Vol 9 ◽  
Author(s):  
Hong-Viet Ngo ◽  
Juergen Fell ◽  
Bernhard Staresina

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.


SLEEP ◽  
2020 ◽  
Author(s):  
Jun-Sang Sunwoo ◽  
Kwang Su Cha ◽  
Jung-Ick Byun ◽  
Jin-Sun Jun ◽  
Tae-Joon Kim ◽  
...  

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.


2020 ◽  
Vol 10 (6) ◽  
pp. 343 ◽  
Author(s):  
Serena Scarpelli ◽  
Aurora D’Atri ◽  
Chiara Bartolacci ◽  
Maurizio Gorgoni ◽  
Anastasia Mangiaruga ◽  
...  

Several findings support the activation hypothesis, positing that cortical arousal promotes dream recall (DR). However, most studies have been carried out on young participants, while the electrophysiological (EEG) correlates of DR in older people are still mostly unknown. We aimed to test the activation hypothesis on 20 elders, focusing on the Non-Rapid Eye Movement (NREM) sleep stage. All the subjects underwent polysomnography, and a dream report was collected upon their awakening from NREM sleep. Nine subjects were recallers (RECs) and 11 were non-RECs (NRECs). The delta and beta EEG activity of the last 5 min and the total NREM sleep was calculated by Fast Fourier Transform. Statistical comparisons (RECs vs. NRECs) revealed no differences in the last 5 min of sleep. Significant differences were found in the total NREM sleep: the RECs showed lower delta power over the parietal areas than the NRECs. Consistently, statistical comparisons on the activation index (delta/beta power) revealed that RECs showed a higher level of arousal in the fronto-temporal and parieto-occipital regions than NRECs. Both visual vividness and dream length are positively related to the level of activation. Overall, our results are consistent with the view that dreaming and the storage of oneiric contents depend on the level of arousal during sleep, highlighting a crucial role of the temporo-parietal-occipital zone.


2021 ◽  
Author(s):  
Orsolya Szalardy ◽  
Peter Simor ◽  
Peter Przemyslaw Ujma ◽  
Zsofia Jordan ◽  
Laszlo Halasz ◽  
...  

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.


2017 ◽  
Author(s):  
Elizaveta Solomonova ◽  
Simon Dubé ◽  
Cloé Blanchette-Carrière ◽  
Arnaud Samson-Richer ◽  
Michelle Carr ◽  
...  

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.


Author(s):  
Kirstie Anderson

The diagnosis of sleep and circadian rhythm disorders provides a detailed framework to correctly diagnose the primary sleep disorders that a psychiatrist will see in daily practice, including common sleep-related movement disorders. This includes the specific sleep history, the role of sleep diaries, validated questionnaires, and how to interpret the scores and the role of both home and inpatient sleep studies (polysomnography). The most recent diagnostic criteria within the International Classification of Sleep Disorder, third edition (ICSD-3) are used for the four major categories of sleep disorder: hypersomnia, insomnia, parasomnia, and circadian rhythm disorder. Common sleep disorders such as obstructive sleep apnoea (OSA), restless legs syndrome (RLS), narcolepsy, and both non-rapid eye movement (NREM) sleep parasomnia and rapid eye movement (REM) parasomnia are described. It is written for qualified specialist doctors.


2021 ◽  
Vol 15 ◽  
Author(s):  
Yousuke Tsuneoka ◽  
Hiromasa Funato

The preoptic area (POA) has long been recognized as a sleep center, first proposed by von Economo. The POA, especially the medial POA (MPOA), is also involved in the regulation of various innate functions such as sexual and parental behaviors. Consistent with its many roles, the MPOA is composed of subregions that are identified by different gene and protein expressions. This review addresses the current understanding of the molecular and cellular architecture of POA neurons in relation to sleep and reproductive behavior. Optogenetic and pharmacogenetic studies have revealed a diverse group of neurons within the POA that exhibit different neural activity patterns depending on vigilance states and whose activity can enhance or suppress wake, non-rapid eye movement (NREM) sleep, or rapid eye movement (REM) sleep. These sleep-regulating neurons are not restricted to the ventrolateral POA (VLPO) region but are widespread in the lateral MPOA and LPOA as well. Neurons expressing galanin also express gonadal steroid receptors and regulate motivational aspects of reproductive behaviors. Moxd1, a novel marker of sexually dimorphic nuclei (SDN), visualizes the SDN of the POA (SDN-POA). The role of the POA in sleep and other innate behaviors has been addressed separately; more integrated observation will be necessary to obtain physiologically relevant insight that penetrates the different dimensions of animal behavior.


SLEEP ◽  
2019 ◽  
Vol 42 (7) ◽  
Author(s):  
Fereshteh Dehnavi ◽  
Sahar Moghimi ◽  
Shima Sadrabadi Haghighi ◽  
Mostafa Safaie ◽  
Maryam Ghorbani

Abstract Memories selectively benefit from sleep. In addition to the importance of the consolidation of relevant memories, the capacity to forget unwanted memories is also crucial. We investigated the effect of suppressing unwanted memories on electroencephalography activity of subsequent sleep using a motivated forgetting (MF) paradigm as compared with a control non-forgetting task. Subjects were randomly assigned to nap or no-nap groups. We used a modified version of the think/no-think paradigm with dominant number of no-think words cued to be forgotten and included only subjects capable of suppressing unwanted memories by performing an initial subject inclusion experiment. In both groups and conditions, the performance of the subjects in recalling the word pairs learned in the beginning of the day was evaluated in a final recall test. We found that both nap and no-nap groups recalled significantly less no-think words in the MF condition compared to the control condition. Moreover, for the nap group, in the MF compared to the control condition, spindle power and density increased during stage 2 (S2) whereas they decreased during slow wave sleep (SWS). Interestingly, recall performance of no-think words was negatively correlated with spindle power during S2 whereas it was positively correlated with spindle power during SWS. These results indicate that sleep spindles are sensitive to the previous MF experiences and suggest a differential role of sleep spindles during S2 and SWS in memory processing during sleep.


2000 ◽  
Vol 279 (5) ◽  
pp. R1590-R1598 ◽  
Author(s):  
B. Bodosi ◽  
F. Obál ◽  
J. Gardi ◽  
J. Komlódi ◽  
J. Fang ◽  
...  

Sleep alterations after a 1-min exposure to ether vapor were studied in rats to determine if this stressor increases rapid eye-movement (REM) sleep as does an immobilization stressor. Ether exposure before light onset or dark onset was followed by significant increases in REM sleep starting ∼3–4 h later and lasting for several hours. Non-REM (NREM) sleep and electroencephalographic slow-wave activity during NREM sleep were not altered. Exposure to ether vapor elicited prolactin (Prl) secretion. REM sleep was not promoted after ether exposure in hypophysectomized rats. If the hypophysectomy was partial and the rats secreted Prl after ether exposure, then increases in REM sleep were observed. Intracerebroventricular administration of an antiserum to Prl decreased spontaneous REM sleep and inhibited ether exposure-induced REM sleep. The results indicate that a brief exposure to ether vapor is followed by increases in REM sleep if the Prl response associated with stress is unimpaired. This suggests that Prl, which is a previously documented REM sleep-promoting hormone, may contribute to the stimulation of REM sleep after ether exposure.


Physiology ◽  
2018 ◽  
Vol 33 (3) ◽  
pp. 182-196 ◽  
Author(s):  
Alessandro Silvani ◽  
Matteo Cerri ◽  
Giovanna Zoccoli ◽  
Steven J. Swoap

This review compares two states that lower energy expenditure: non-rapid eye movement (NREM) sleep and torpor. Knowledge on mechanisms common to these states, and particularly on the role of adenosine in NREM sleep, may ultimately open the possibility of inducing a synthetic torpor-like state in humans for medical applications and long-term space travel. To achieve this goal, it will be important, in perspective, to extend the study to other hypometabolic states, which, unlike torpor, can also be experienced by humans.


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