Sex and Pubertal Differences in the Maturational Trajectories of Sleep Spindles in the Transition from Childhood to Adolescence: A Population-Based Study

Ricci, Anna; He, Fan; Calhoun, Susan L.; Fang, Jidong; Vgontzas, Alexandros N.; Liao, Duanping; Bixler, Edward O.; Younes, Magdy; Fernández-Mendoza, Julio

doi:10.1523/eneuro.0257-21.2021

Cited by 13 publications

(5 citation statements)

References 57 publications

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“…Regarding slow wave activity, previous studies reported a developmental shift in the topography from posterior to anterior areas for maximum slow wave activity, possibly reflecting the occipital to frontal pathway of cortical maturation (Feinberg et al, 2011; Kurth et al, 2010), which corresponds to the findings in the present sample of children showing the smallest age-dependent decline in slow wave activity at the frontal recording sites. Recently, evidence has been provided that age-dependent changes in slow wave activity and spindle activity might differ between girls and boys with girls showing, for example, an earlier start of the decline in slow wave activity with age than boys (Ricci, He, Calhoun, et al, 2021; Ricci, He, Fang, et al, 2021) that might be driven by the earlier pubertal development in girls. Unfortunately, we did not assess pubertal status and the uneven distribution of male and female participants in our study (with >70% of the participants being male) prevented any solid conclusions regarding sex differences.…”

Section: Discussionmentioning

confidence: 99%

Sleep electroencephalogram (EEG) oscillations and associated memory processing during childhood and early adolescence.

Kurz¹,

Zinke²,

Born³

2023

Developmental Psychology

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The architecture of sleep undergoes distinct changes during childhood and early adolescence. Slow wave sleep is involved in memory processing and may support active consolidation of newly encoded representations to support the formation of abstracted “gist” memories. Here, we examined sleep and overnight memory formation in German school children (n = 33) between 7 and 15 years of age, after the encoding phase of a verbal Deese-Roediger-McDermott (DRM) task. Effects of age were analyzed on sleep electroencephalogram (EEG) signatures of memory processing during nonrapid eye movement (NonREM) sleep, and the overnight formation of veridical and gist-based memories. Increasing age decreases time spent in slow wave sleep, and slow wave activity, whereas density and amplitude of fast sleep spindles in NonREM sleep were increased. Moreover, fast spindles were more consistently and more closely coupled to the upstate of the slow oscillation in the older children. Also, veridical and gist-based recall of words after sleep increased with age. Notably, a closer slow oscillation upstate-fast spindle coupling predicted veridical recall of words, and this relationship was found independent of age. Memory performance in the sleeping children did not differ from that of an age-matched control group (n = 32) tested over a daytime wake retention interval, with adolescents even showing superior veridical recall after wake. Our findings suggest that slow oscillation-spindle coupling as a mechanism of sleep-dependent memory formation becomes increasingly relevant during childhood and early adolescence. However, wake-associated mechanisms similarly effective in forming medium-term memory exist in this age as well.

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Section: Discussionmentioning

confidence: 99%

Sleep electroencephalogram (EEG) oscillations and associated memory processing during childhood and early adolescence.

Kurz¹,

Zinke²,

Born³

2023

Developmental Psychology

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“…Our findings are consistent with the previous studies reporting decreased sleep spindle density as associated with poor cognitive outcomes; however, we did not find a significant effect of OSA severity in this association, or group differences in spindles characteristics for cognition. The association between sleep spindle activity and cognitive decline in OSA may be affected by other factors, and become more evident in clinically diagnosed patients with severe OSA and cardiovascular comorbidities (Martin et al, 2013; Mohammadi et al, 2021; Muñoz‐Torres et al, 2020; Plante et al, 2013; Ricci et al, 2021).…”

Section: Discussionmentioning

confidence: 99%

“…The role of sex differences in spindle characteristics remains unclear, although a few studies have reported higher spindle density in females compared with males (Huupponen et al, 2002; Purcell et al, 2017; Ricci et al, 2021; Ujma et al, 2014). In a previous study from our laboratory, we did not find sex differences in spindle density (Guadagni et al, 2021).…”

Section: Discussionmentioning

confidence: 99%

Sex differences in the association of sleep spindle density and cognitive performance among community‐dwelling middle‐aged and older adults with obstructive sleep apnea

Pun,

Guadagni,

Longman

et al. 2023

Journal of Sleep Research

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SummaryRecent studies have found associations between obstructive sleep apnea and cognitive decline. The underlying mechanisms are still unclear. Here, we investigate the associations between changes in micro‐architecture, specifically sleep spindles, and cognitive function in community‐dwelling middle‐aged and older adults, some with obstructive sleep apnea, with a focus on sex differences. A total of 125 voluntary participants (mean age 66.0 ± 6.4 years, 64 females) from a larger cohort (participants of the Brain in Motion Studies I and II) underwent 1 night of in‐home polysomnography and a neuropsychological battery (sleep and cognitive testing were conducted within 2 weeks of each other). A semi‐automatic computerized algorithm was used to score polysomnography data and detect spindle characteristics in non‐rapid eye movement Stages 2 and 3 in both frontal and central electrodes. Based on their apnea–hypopnea index, participants were divided into those with no obstructive sleep apnea (apnea–hypopnea index < 5 per hr, n = 21), mild obstructive sleep apnea (5 ≥ apnea–hypopnea index < 15, n = 47), moderate obstructive sleep apnea (15 ≥ apnea–hypopnea index < 30, n = 34) and severe obstructive sleep apnea (apnea–hypopnea index ≥ 30, n = 23). There were no significant differences in spindle characteristics between the four obstructive sleep apnea severity groups. Spindle density and percentage of fast spindles were positively associated with some verbal fluency measures on the cognitive testing. Sex might be linked with these associations. Biological sex could play a role in the associations between spindle characteristics and some verbal fluency measures. Obstructive sleep apnea severity was not found to be a contributing factor in this non‐clinical community‐dwelling cohort.

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“…In terms of spindle characteristics, women's fast sleep spindles typically display greater density and enhanced oscillations compared to men's (Choi et al, 2019; Merikanto et al, 2017; Ricci, He, Calhoun, et al, 2021). Spectral analyses show that absolute rather than relative spectral power varies by sex, with women showing greater power densities across all frequency bands, except for Beta power, throughout the night (Yoon et al, 2021).…”

Section: Sex and Sleepmentioning

confidence: 99%

The multidimensionality of sleep in population‐based samples: a narrative review

Langenberg

Kocevska

Luik

2022

Journal of Sleep Research

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Summary The identification of optimal sleep duration recommendations for the general population has long been an important goal on the public health agenda, as both short and long sleep duration have been linked to unfavourable health outcomes. Yet, sleep is more than duration alone and can be described across multiple domains, such as timing, regularity, satisfaction, alertness, and efficiency. We reviewed observational population‐based studies that examined differences in age, sex, and origin across multiple dimensions of sleep. Reviewed literature suggests an increasing prevalence of insomnia symptoms, shorter and less deep sleep in old age. Overall, women report poorer sleep quality than men despite objective measures revealing shorter and more fragmented sleep in men. Minorities generally have poorer quantity and quality of sleep, but multi‐ethnic studies have reported mixed results regarding the subjective experience of sleep. In sum, effects of age, sex and origin differ across sleep dimensions, thereby suggesting that the multidimensionality of sleep and how these different aspects interact should be studied across individuals. Studies should include both self‐reported measures and objective assessments in diverse population‐based samples, as both aspects are important to understand sleep health in the general population. Data‐driven descriptions could provide researchers and clinicians with insights into how well individuals are sleeping and offer concrete targets for promotion of sleep health across the population.

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Sex and Pubertal Differences in the Maturational Trajectories of Sleep Spindles in the Transition from Childhood to Adolescence: A Population-Based Study

Cited by 13 publications

References 57 publications

Sleep electroencephalogram (EEG) oscillations and associated memory processing during childhood and early adolescence.

Sleep electroencephalogram (EEG) oscillations and associated memory processing during childhood and early adolescence.

Sex differences in the association of sleep spindle density and cognitive performance among community‐dwelling middle‐aged and older adults with obstructive sleep apnea

The multidimensionality of sleep in population‐based samples: a narrative review

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