Mapping of Cortical Activity in the First Two Decades of Life: A High-Density Sleep Electroencephalogram Study

Kurth, Salomé; Ringli, Maya; Geiger, Anja; LeBourgeois, Monique K.; Jenni, Oskar G.; Huber, Reto

doi:10.1523/jneurosci.2532-10.2010

Cited by 346 publications

(453 citation statements)

References 66 publications

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“…Strongest in lower frequencies with t-values up to 10 and higher, the power reduction was similar between EO and EC oscillations. Consistent with other studies (Boord et al, 2007;Kurth et al, 2010), this effect to a lower degree extended also to higher frequencies. According to previous publications, we do not believe that the observed EEG effects are massively influenced by changes of physical properties of the head (e.g., skull conductance or impedance) which change during early development, as these changes appear to be less prominent for the present age range (Hoekema et al, 2003).…”

Section: Brain Development and Eeg Maturationsupporting

confidence: 92%

Brain state regulation during normal development: Intrinsic activity fluctuations in simultaneous EEG–fMRI

et al. 2012

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Brain maturation in adolescence is mirrored by the EEG as a pronounced decrease in low frequency activity. This EEG power attenuation parallels reductions of structural and metabolic markers of neuronal maturation (i.e., gray matter loss and decrease of absolute cerebral glucose utilization). However, it is largely unknown what causes these electrophysiological changes, and how this functional reorganization relates to other functional measures such as the fMRI BOLD signal. In this study, we used simultaneously recorded EEG and fMRI to localize hemodynamic correlates of fluctuating EEG oscillations and to study the development of this EEG-BOLD coupling. Furthermore, the maturational EEG power attenuation was directly compared to BOLD signal power maturation. Both analyses were novel in their developmental perspective and aimed at providing a functional lead to EEG maturation. Data from 19 children, 18 adolescents and 18 young adults were acquired in 10min eyes-open/eyes-closed resting states. Our results revealed that both EEG and BOLD amplitudes strongly decrease between childhood and adulthood, but their functional coupling remains largely unchanged. The global reduction of absolute amplitude of spontaneous slow BOLD signal fluctuation is a novel marker for brain maturation, and parallels the globally decreasing trajectories of EEG amplitudes, gray matter and glucose metabolism during adolescence. Further, the absence of thalamocortical EEG-BOLD coupling in children together with age-related normalized thalamic BOLD power increase indicated maturational changes in brain state regulation. Abstract -Brain maturation in adolescence is mirrored by the EEG as a pronounced decrease in low frequency activity. This EEG power attenuation parallels reductions of structural and metabolic markers of neuronal maturation (i.e., gray matter loss and decrease of absolute cerebral glucose utilization). However, it is largely unknown what causes these electrophysiological changes, and how this functional reorganization relates to other functional measures such as the fMRI BOLD signal. In this study, we used simultaneously recorded EEG and fMRI to localize hemodynamic correlates of fluctuating EEG oscillations and to study the development of this EEG-BOLD coupling. Furthermore, the maturational EEG power attenuation was directly compared to BOLD signal power maturation. Both analyses were novel in their developmental perspective and aimed at providing a functional lead to EEG maturation. Data from 19 children, 18 adolescents and 18 young adults were acquired in 10 min eyes-open/eyes-closed resting states. Our results revealed that both EEG and BOLD amplitudes strongly decrease between childhood and adulthood, but their functional coupling remains largely unchanged. The global reduction of absolute amplitude of spontaneous slow BOLD signal fluctuation is a novel marker for brain maturation, and parallels the globally decreasing trajectories of EEG amplitudes, gray matter and glucose metabolism during adolescence. Furthe...

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Section: Brain Development and Eeg Maturationsupporting

confidence: 92%

Brain state regulation during normal development: Intrinsic activity fluctuations in simultaneous EEG–fMRI

et al. 2012

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“…Less intense waking neuronal activity would decrease the need (substrate) for NREM recuperation, reducing the intensity (power) of the two recuperative frequencies, delta and theta. Further indirect support for this interpretation is provided by topographic differences in the timing of the delta decline (12,13). The age of fastest NREM delta decline shows a back-to-front distribution similar to the back-to-front maturational pattern reported for structural MRI-measured cortical thinning (14).…”

Section: Discussionmentioning

confidence: 65%

Sex, puberty, and the timing of sleep EEG measured adolescent brain maturation

Campbell

Grimm

Bie

et al. 2012

Proc. Natl. Acad. Sci. U.S.A.

114

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The steep adolescent decline in the slow wave (delta, 1-4 Hz) electroencephalogram (EEG) of nonrapid eye movement (NREM) sleep is a dramatic maturational change in brain electrophysiology thought to be driven by cortical synaptic pruning. A perennial question is whether this change in brain electrophysiology is related to sexual maturation. Applying Gompertz growth models to longitudinal data spanning ages 9-18 y, we found that the timing of the delta decline was significantly (P < 0.0001) linked to timing of pubertal maturation. This timing relation remained significant when sex differences in the timing of the delta decline were statistically controlled. Sex differences and the relation to the timing of puberty jointly explained 67% of the between-subject variance in the timing of the delta decline. These data provide a demonstration of a temporal relation between puberty and an electrophysiological marker of adolescent brain development. They can guide research into whether the neuroendocrine events of puberty are mechanistically linked to cortical maturation or whether, instead, the two maturational processes are parallel but independent programs of human ontogenesis. n an ongoing longitudinal study of adolescent sleep EEG, we identified the age range 12-16.5 y as a critical period of late brain maturation (1). Centrally recorded slow wave (delta, 1-4 Hz) EEG power in nonrapid eye movement (NREM) sleep declines by >60% in this 4.5-y range. We (2) and others (3,4) have proposed that the decline in delta power reflects the cortical synaptic pruning discovered by Huttenlocher (5). The decline in delta power also bears importantly on the physiology of sleep regulation because NREM slow wave EEG seems to reflect a recuperative process (6, 7); it increases with prior waking duration and declines across the night.A recurrent question is whether the dramatic changes in sleep electrophysiology during adolescence are related to the concurrent physical changes of puberty. Previous studies have found lower levels of visually scored slow wave sleep (8) or delta power (3) in more sexually mature subjects, but these studies did not control for age. In 2006, we analyzed the data then available from our longitudinal study to examine sleep EEG changes in relation to both age and pubertal maturation (9). We reported a strong relation between the rate of the delta decline and the rate of progression through the Tanner stages of pubertal maturation. However, both rates were strongly related to age. When age was statistically controlled, the relation between delta power and Tanner stage became nonsignificant.Our 2006 article included data only from ages 9-11 and 12-14 y and evaluated the rate of delta decline but not its timing. We are now able to analyze the timing of the relation between the decline in NREM delta EEG power and pubertal maturation in an expanded longitudinal dataset, which now includes ages 9-18 y. These analyses show a highly significant relation between the timing of the delta decline and the timing of pubert...

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“…One emerging area of work that may help shed light on the role of sleep and development is through the examination of slow-wave activity (SWA) as measured by sleep EEG. Two studies have found that the pattern of changes in SWA reflects typical cortical maturation, with a shift from posterior to anterior regions across childhood and adolescence (Kurth et al, 2010(Kurth et al, , 2012. For example, a predominance of SWA in the occipital lobe in early childhood corresponds with the development of visual acuity, whereas a predominance of SWA in the frontal lobes is seen in adolescence, corresponding to the development of executive functioning.…”

Section: Critical Periods Of Development?mentioning

confidence: 99%

Future Directions in Sleep and Developmental Psychopathology

Meltzer

2016

Journal of Clinical Child & Adolescent Psychology

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Mapping of Cortical Activity in the First Two Decades of Life: A High-Density Sleep Electroencephalogram Study

Cited by 346 publications

References 66 publications

Brain state regulation during normal development: Intrinsic activity fluctuations in simultaneous EEG–fMRI

Brain state regulation during normal development: Intrinsic activity fluctuations in simultaneous EEG–fMRI

Sex, puberty, and the timing of sleep EEG measured adolescent brain maturation

Future Directions in Sleep and Developmental Psychopathology

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