Spatiotemporal Dynamics of Sleep Spindle Sources Across NREM Sleep Cycles

Alfonsi, Valentina; D’Atri, Alessandro; Gorgoni, Maurizio; Scarpelli, Serena; Mangiaruga, Anastasia; Ferrara, Michele; Gennaro, Luigi De

doi:10.3389/fnins.2019.00727

Cited by 18 publications

(23 citation statements)

References 52 publications

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“…With these more sensitive methods we have been able to show that individual-specific fast sleep spindle features are unequivocally traveling to more posterior areas during adolescence. Considering the precuneal origin of fast sleep spindles in adult human subjects (20, 21), it seems that individualized sleep spindle analysis is a forceful tool to detect the dominant anatomical directions of brain maturation in humans.…”

Section: Discussionmentioning

confidence: 99%

“…Finally, the derivation-specific topographical distribution of the spindle parameters and their age-dependent differences were analyzed. Multiple comparisons correction was performed using a modified version of the Rüger area method (20, 21). We calculated Rüger area global significance as follows: 1/3 of the descriptive significances at p=.05/3 =.017 AND/OR half of descriptive significances at p=.05/2=.025.…”

Section: Methodsmentioning

confidence: 99%

“…A bimodal frequency and topography of sleep spindles has repeatedly been described in adults. That is, slow (∼12 Hz) sleep spindles are frontally dominant, whereas fast (∼14 Hz) sleep spindles are of parietal/precuneal origin in adult human subjects (20, 21).…”

Section: Introductionmentioning

confidence: 99%

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Topographical relocation of adolescent sleep spindles reveals a new maturational pattern in the human brain

Gombos

Bódizs

Pótári

et al. 2021

Preprint

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Current theories of human neural development and brain maturation emphasize the posterior-to-anterior or back-to-front pattern as an unequivocal ontogenetic feature that is largely due to the late maturing frontal lobes. The back-to-front pattern has received substantial support from both anatomical and electrophysiological studies, the latter looking at the age-related changes in the topography of sleep slow waves. However, the above scenario of a unidirectional developmental and anatomical route disregards the major hub of the so-called default-mode network, which is a human-specific and late maturing neural structure of the brain, undergoing significant differentiation during adolescence: the precuneus. In order to understand how the late maturation of the precuneus might modify the presently accepted large-scale maturational pattern of the human brain, here we focus on sleep spindles that are known to be involved in neural plasticity with major sources in the precuneus in adults. We provide evidence for the posteriorization in the prevailing anatomical localization of fast sleep spindles. The predominantly central maxima in density and amplitude of fast spindles at the age of 12 years becomes gradually shifted to the parietal regions until the age of 20. Similar changes, albeit at a smaller anatomical distance take place in terms of fast sleep spindle frequency. These findings indicate a front-to-back pattern of brain maturation and correspond with reports on an increased differentiation of the precuneus during adolescence.

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Section: Discussionmentioning

confidence: 99%

Section: Methodsmentioning

confidence: 99%

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Topographical relocation of adolescent sleep spindles reveals a new maturational pattern in the human brain

Gombos

Bódizs

Pótári

et al. 2021

Preprint

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“…Refs. 3 , 64 , 65 ). A reliable investigation of overnight changes in sleep spindles was however not possible in our sample for several reasons.…”

Section: Discussionmentioning

confidence: 99%

Role of corpus callosum in sleep spindle synchronization and coupling with slow waves

Bernardi

Avvenuti

Cataldi

et al. 2021

Brain Communications

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Sleep spindles of non-REM sleep are transient, waxing-and-waning 10–16 Hz EEG oscillations, whose cortical synchronization depends on the engagement of thalamo-cortical loops. However, previous studies in animal models lacking the corpus callosum due to agenesis or total callosotomy and in humans with agenesis of the corpus callosum suggested that cortico-cortical connections may also have a relevant role in cortical (inter-hemispheric) spindle synchronization. Yet, most of these works did not provide direct quantitative analyses to support their observations. By studying a rare sample of callosotomized, split-brain patients, we recently demonstrated that the total resection of the corpus callosum is associated with a significant reduction in the inter-hemispheric propagation of non-REM slow waves. Interestingly, sleep spindles are often temporally and spatially grouped around slow waves (0.5–4 Hz), and this coordination is thought to have an important role in sleep-dependent learning and memory consolidation. Given these premises, here we set out to investigate whether total callosotomy may affect the generation and spreading of sleep spindles, as well as their coupling with sleep slow waves. To this aim, we analyzed overnight high-density EEG recordings (257 electrodes) collected in five patients who underwent total callosotomy due to drug-resistant epilepsy (age 40–53, two females), three non-callosotomized neurological patients (age 44–66, two females), and in a sample of 24 healthy adult control subjects (age 20–47, 13 females). Individual sleep spindles were automatically detected using a validated algorithm and their properties and topographic distributions were computed. All analyses were performed with and without a regression-based adjustment accounting for inter-subject age differences. The comparison between callosotomized patients and healthy subjects did not reveal systematic variations in spindle density, amplitude or frequency. However, callosotomized patients were characterized by a reduced spindle duration, which could represent the result of a faster desynchronization of spindle activity across cortical areas of the two hemispheres. In contrast with our previous findings regarding sleep slow waves, we failed to detect in callosotomized patients any clear, systematic change in the inter-hemispheric synchronization of sleep spindles. In line with this, callosotomized patients were characterized by a reduced extension of the spatial association between temporally coupled spindles and slow waves. Our findings are consistent with a dependence of spindles on thalamo-cortical rather than cortico-cortical connections in humans, but also revealed that, despite their temporal association, slow waves and spindles are independently regulated in terms of topographic expression.

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“…Spindle detection was performed by means of a customized algorithm in Matlab [ 55 , 56 , 57 , 58 , 59 ]. NREM epochs were bandpass-filtered between 11 and 15 Hz (−3 dB at 10 and 16 Hz) using a Chebyshev Type II filter.…”

Section: Methodsmentioning

confidence: 99%

Sleep-Related Declarative Memory Consolidation in Children and Adolescents with Developmental Dyslexia

et al. 2021

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Sleep has a crucial role in memory processes, and maturational changes in sleep electrophysiology are involved in cognitive development. Albeit both sleep and memory alterations have been observed in Developmental Dyslexia (DD), their relation in this population has been scarcely investigated, particularly concerning topographical aspects. The study aimed to compare sleep topography and associated sleep-related declarative memory consolidation in participants with DD and normal readers (NR). Eleven participants with DD and 18 NR (9–14 years old) underwent a whole-night polysomnography. They were administered a word pair task before and after sleep to assess for declarative memory consolidation. Memory performance and sleep features (macro and microstructural) were compared between the groups, and the intercorrelations between consolidation rate and sleep measures were assessed. DD showed a deeper worsening in memory after sleep compared to NR and reduced slow spindles in occipito-parietal and left fronto-central areas. Our results suggest specific alterations in local sleep EEG (i.e., sleep spindles) and in sleep-dependent memory consolidation processes in DD. We highlight the importance of a topographical approach, which might shed light on potential alteration in regional cortical oscillation dynamics in DD. The latter might represent a target for therapeutic interventions aimed at enhancing cognitive functioning in DD.

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Spatiotemporal Dynamics of Sleep Spindle Sources Across NREM Sleep Cycles

Cited by 18 publications

References 52 publications

Topographical relocation of adolescent sleep spindles reveals a new maturational pattern in the human brain

Topographical relocation of adolescent sleep spindles reveals a new maturational pattern in the human brain

Role of corpus callosum in sleep spindle synchronization and coupling with slow waves

Sleep-Related Declarative Memory Consolidation in Children and Adolescents with Developmental Dyslexia

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