Communication from the cerebellum to the neocortex during sleep spindles.
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ABSTRACT:
SUBMITTER: Xu W
PROVIDER: S-EPMC7938225 | biostudies-literature |
REPOSITORIES: biostudies-literature
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Project description:Learning and plasticity rely on fine-tuned regulation of neuronal circuits during offline periods. An unresolved puzzle is how the sleeping brain, in the absence of external stimulation or conscious effort, coordinates neuronal firing rates (FRs) and communication within and across circuits to support synaptic and systems consolidation. Using intracranial electroencephalography combined with multiunit activity recordings from the human hippocampus and surrounding medial temporal lobe (MTL) areas, we show that, governed by slow oscillation (SO) up-states, sleep spindles set a timeframe for ripples to occur. This sequential coupling leads to a stepwise increase in (1) neuronal FRs, (2) short-latency cross-correlations among local neuronal assemblies and (3) cross-regional MTL interactions. Triggered by SOs and spindles, ripples thus establish optimal conditions for spike-timing-dependent plasticity and systems consolidation. These results unveil how the sequential coupling of specific sleep rhythms orchestrates neuronal processing and communication during human sleep.
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Project description:Sleep spindles are approximately 1 s bursts of 10-16 Hz activity that occur during stage 2 sleep. Spindles are highly synchronous across the cortex and thalamus in animals, and across the scalp in humans, implying correspondingly widespread and synchronized cortical generators. However, prior studies have noted occasional dissociations of the magnetoencephalogram (MEG) from the EEG during spindles, although detailed studies of this phenomenon have been lacking. We systematically compared high-density MEG and EEG recordings during naturally occurring spindles in healthy humans. As expected, EEG was highly coherent across the scalp, with consistent topography across spindles. In contrast, the simultaneously recorded MEG was not synchronous, but varied strongly in amplitude and phase across locations and spindles. Overall, average coherence between pairs of EEG sensors was approximately 0.7, whereas MEG coherence was approximately 0.3 during spindles. Whereas 2 principle components explained approximately 50% of EEG spindle variance, >15 were required for MEG. Each PCA component for MEG typically involved several widely distributed locations, which were relatively coherent with each other. These results show that, in contrast to current models based on animal experiments, multiple asynchronous neural generators are active during normal human sleep spindles and are visible to MEG. It is possible that these multiple sources may overlap sufficiently in different EEG sensors to appear synchronous. Alternatively, EEG recordings may reflect diffusely distributed synchronous generators that are less visible to MEG. An intriguing possibility is that MEG preferentially records from the focal core thalamocortical system during spindles, and EEG from the distributed matrix system.
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Project description:In humans, some evidence suggests that there are two different types of spindles during sleep, which differ by their scalp topography and possibly some aspects of their regulation. To test for the existence of two different spindle types, we characterized the activity associated with slow (11-13 Hz) and fast (13-15 Hz) spindles, identified as discrete events during non-rapid eye movement sleep, in non-sleep-deprived human volunteers, using simultaneous electroencephalography and functional MRI. An activation pattern common to both spindle types involved the thalami, paralimbic areas (anterior cingulate and insular cortices), and superior temporal gyri. No thalamic difference was detected in the direct comparison between slow and fast spindles although some thalamic areas were preferentially activated in relation to either spindle type. Beyond the common activation pattern, the increases in cortical activity differed significantly between the two spindle types. Slow spindles were associated with increased activity in the superior frontal gyrus. In contrast, fast spindles recruited a set of cortical regions involved in sensorimotor processing, as well as the mesial frontal cortex and hippocampus. The recruitment of partially segregated cortical networks for slow and fast spindles further supports the existence of two spindle types during human non-rapid eye movement sleep, with potentially different functional significance.
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Project description:There is now ample evidence that sleep spindles play a critical role in the consolidation of newly acquired motor sequences. Previous studies have also revealed that the interplay between different types of sleep oscillations (e.g. spindles, slow waves, sharp-wave ripples) promotes the consolidation process of declarative memories. Yet the functional contribution of this type of frequency-specific interactions to motor memory consolidation remains unknown. Thus, this study sought to investigate whether spindle oscillations are associated with low- or high-frequency activity at the regional (local) and interregional (connectivity) levels. Using an olfactory-targeted memory reactivation paradigm paired to a motor sequence learning task, we compared the effect of cuing (Cond) to no-cuing (NoCond) on frequency interactions during sleep spindles. Time-frequency decomposition analyses revealed that cuing induced significant differential and localized changes in delta (1-4 Hz) and theta (4-8 Hz) frequencies before, during, and after spindles, as well as changes in high-beta (20-30 Hz) during the spindle oscillation. Finally, coherence analyses yielded significant increases in connectivity during sleep spindles in both theta and sigma (11-17 Hz) bands in the cued group only. These results support the notion that the synchrony between spindle and associated low- or high-frequency rhythmic activity is an integral part of the memory reactivation process. Furthermore, they highlight the importance of not only measuring spindles' characteristics, but to investigate such oscillations in both time and frequency domains when assessing memory consolidation-related changes.
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Project description:Sleep deficiencies and associated performance decrements are common among astronauts during spaceflight missions. Previously, sleep in space was analyzed with a focus on global measures while the intricate structure of sleep oscillations remains largely unexplored. This study extends previous findings by analyzing how spaceflight affects characteristics of sleep spindles and slow waves, two sleep oscillations associated with sleep quality and quantity, in four astronauts before, during and after two Space Shuttle missions. Analysis of these oscillations revealed significantly increased fast spindle density, elevated slow spindle frequency, and decreased slow wave amplitude in space compared to on Earth. These results reflect sleep characteristics during spaceflight on a finer electrophysiological scale and provide an opportunity for further research on sleep in space.
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Project description: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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Project description:In humans and other mammals, the stillness of sleep is punctuated by bursts of rapid eye movements (REMs) and myoclonic twitches of the limbs.1 Like the spontaneous activity that arises from the sensory periphery in other modalities (e.g., retinal waves),2 sensory feedback arising from twitches is well suited to drive activity-dependent development of the sensorimotor system.3 It is partly because of the behavioral activation of REM sleep that this state is also called active sleep (AS), in contrast with the behavioral quiescence that gives quiet sleep (QS)-the second major stage of sleep-its name. In human infants, for which AS occupies 8 h of each day,4 twitching helps to identify the state;5-8 nonetheless, we know little about the structure and functions of twitching across development. Recently, in sleeping infants,9 we documented a shift in the temporal expression of twitching beginning around 3 months of age that suggested a qualitative change in how twitches are produced. Here, we combine behavioral analysis with high-density electroencephalography (EEG) to demonstrate that this shift reflects the emergence of limb twitches during QS. Twitches during QS are not only unaccompanied by REMs, but they also occur synchronously with sleep spindles, a hallmark of QS. As QS-related twitching increases with age, sleep spindle rate also increases along the sensorimotor strip. The emerging synchrony between subcortically generated twitches and cortical oscillations suggests the development of functional connectivity among distant sensorimotor structures, with potential implications for detecting and explaining atypical developmental trajectories.
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Project description:BACKGROUND AND AIM:Predisposing factors place certain individuals at higher risk for insomnia, especially in the presence of precipitating conditions such as stressful life events. Sleep spindles have been shown to play an important role in the preservation of sleep continuity. Lower spindle density might thus constitute an objective predisposing factor for sleep reactivity to stress. The aim of this study was therefore to evaluate the relationship between baseline sleep spindle density and the prospective change in insomnia symptoms in response to a standardized academic stressor. METHODS:Twelve healthy students had a polysomnography recording during a period of lower stress at the beginning of the academic semester, along with an assessment of insomnia complaints using the insomnia severity index (ISI). They completed a second ISI assessment at the end of the semester, a period coinciding with the week prior to final examinations and thus higher stress. Spindle density, amplitude, duration, and frequency, as well as sigma power were computed from C4-O2 electroencephalography derivation during stages N2-N3 of non-rapid-eye-movement (NREM) sleep, across the whole night and for each NREM sleep period. To test for the relationship between spindle density and changes in insomnia symptoms in response to academic stress, spindle measurements at baseline were correlated with changes in ISI across the academic semester. RESULTS:Spindle density (as well as spindle amplitude and sigma power), particularly during the first NREM sleep period, negatively correlated with changes in ISI (p?<?0.05). CONCLUSION:Lower spindle activity, especially at the beginning of the night, prospectively predicted larger increases in insomnia symptoms in response to stress. This result indicates that individual differences in sleep spindle activity contribute to the differential vulnerability to sleep disturbances in the face of precipitating factors.
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Project description:Sleep features in infancy are potential biomarkers for brain maturation but poorly characterized. We describe normative values for sleep macrostructure and sleep spindles at 4-5 months of age. Healthy term infants were recruited at birth and had daytime sleep electroencephalograms (EEGs) at 4-5 months. Sleep staging was performed and five features were analyzed. Sleep spindles were annotated and seven quantitative features were extracted. Features were analyzed across sex, recording time (am/pm), infant age, and from first to second sleep cycles. We analyzed sleep recordings from 91 infants, 41% females. Median (interquartile range [IQR]) macrostructure results: sleep duration 49.0 (37.8-72.0) min (n = 77); first sleep cycle duration 42.8 (37.0-51.4) min; rapid eye movement (REM) percentage 17.4 (9.5-27.7)% (n = 68); latency to REM 36.0 (30.5-41.1) min (n = 66). First cycle median (IQR) values for spindle features: number 241.0 (193.0-286.5), density 6.6 (5.7-8.0) spindles/min (n = 77); mean frequency 13.0 (12.8-13.3) Hz, mean duration 2.9 (2.6-3.6) s, spectral power 7.8 (4.7-11.4) µV2, brain symmetry index 0.20 (0.16-0.29), synchrony 59.5 (53.2-63.8)% (n = 91). In males, spindle spectral power (µV2) was 24.5% lower (p = .032) and brain symmetry index 24.2% higher than females (p = .011) when controlling for gestational and postnatal age and timing of the nap. We found no other significant associations between studied sleep features and sex, recording time (am/pm), or age. Spectral power decreased (p < .001) on the second cycle. This normative data may be useful for comparison with future studies of sleep dysfunction and atypical neurodevelopment in infancy. Clinical Trial Registration: BABY SMART (Study of Massage Therapy, Sleep And neurodevelopMenT) (BabySMART)URL: https://clinicaltrials.gov/ct2/show/results/NCT03381027?view=results.ClinicalTrials.gov Identifier: NCT03381027.
| S-EPMC8754499 | biostudies-literature
Project description:During light slow-wave sleep, the thalamo-cortical network oscillates in waxing-and-waning patterns at about 7 to 14 Hz and lasting for 500 ms to 3 s, called spindles, with the thalamus rhythmically sending strong excitatory volleys to the cortex. Concurrently, the hippocampal activity is characterized by transient and strong excitatory events, Sharp-Waves-Ripples (SPWRs), directly affecting neocortical activity--in particular the medial prefrontal cortex (mPFC)--which receives monosynaptic fibers from the ventral hippocampus and subiculum. Both spindles and SPWRs have been shown to be strongly involved in memory consolidation. However, the dynamics of the cortical network during natural sleep spindles and how prefrontal circuits simultaneously process hippocampal and thalamo-cortical activity remain largely undetermined. Using multisite neuronal recordings in rat mPFC, we show that during sleep spindles, oscillatory responses of cortical cells are different for different cell types and cortical layers. Superficial neurons are more phase-locked and tonically recruited during spindle episodes. Moreover, in a given layer, interneurons were always more modulated than pyramidal cells, both in firing rate and phase, suggesting that the dynamics are dominated by inhibition. In the deep layers, where most of the hippocampal fibers make contacts, pyramidal cells respond phasically to SPWRs, but not during spindles. Similar observations were obtained when analyzing ?-oscillation modulation in the mPFC. These results demonstrate that during sleep spindles, the cortex is functionnaly "deafferented" from its hippocampal inputs, based on processes of cortical origin, and presumably mediated by the strong recruitment of inhibitory interneurons. The interplay between hippocampal and thalamic inputs may underlie a global mechanism involved in the consolidation of recently formed memory traces.
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