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Longitudinal changes in aperiodic and periodic activity in electrophysiological recordings in the first seven months of life.

ABSTRACT: Neuronal oscillations emerge in early human development. These periodic oscillations are thought to rapidly change in infancy and stabilize during maturity. Given their numerous connections to physiological and cognitive processes, understanding the trajectory of oscillatory development is important for understanding healthy human brain development. This understanding is complicated by recent evidence that assessment of periodic neuronal oscillations is confounded by aperiodic neuronal activity, an inherent feature of electrophysiological recordings. Recent cross-sectional evidence shows that this aperiodic signal progressively shifts from childhood through early adulthood, and from early adulthood into later life. None of these studies, however, have been performed in infants, nor have they been examined longitudinally. Here, we analyzed longitudinal non-invasive EEG data from 22 typically developing infants, ranging between 38 and 203 days old. We show that the progressive flattening of the EEG power spectrum begins in very early development, continuing through the first months of life. These results highlight the importance of separating the periodic and aperiodic neuronal signals, because the aperiodic signal can bias measurement of neuronal oscillations. Given the infrequent, bursting nature of oscillations in infants, we recommend using quantitative time domain approaches that isolate bursts and uncover changes in waveform properties of oscillatory bursts.

SUBMITTER: Schaworonkow N

PROVIDER: S-EPMC7734223 | biostudies-literature | 2020 Dec

REPOSITORIES: biostudies-literature

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Longitudinal changes in aperiodic and periodic activity in electrophysiological recordings in the first seven months of life.

Schaworonkow Natalie N Voytek Bradley B

Developmental cognitive neuroscience 20201210

Neuronal oscillations emerge in early human development. These periodic oscillations are thought to rapidly change in infancy and stabilize during maturity. Given their numerous connections to physiological and cognitive processes, understanding the trajectory of oscillatory development is important for understanding healthy human brain development. This understanding is complicated by recent evidence that assessment of periodic neuronal oscillations is confounded by aperiodic neuronal activity, ...[more]

PMID: 33316695

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Project description:BackgroundLittle is known about the temporospatial shape characteristics of human lateral ventricles (LVs) during the first two years of life. This study aimed to delineate the morphological growth characteristics of LVs during early infancy using longitudinally acquired MR images in normal healthy infants.Methods24 healthy infants were MR imaged starting from 2 weeks old every 3 months during the first and every 6 months during the second year. Bilateral LVs were segmented and longitudinal morphological and shape analysis were conducted using longitudinal mixed effect models.ResultsA significant bilateral ventricular volume increase (p<0.0001) is observed in year one (Left: 126±51% and Right: 145±62%), followed by a significant reduction (p<0.02) during the second year of life (Left: -24±27% and Right: -20±18%) despite the continuing increase of intracranial volume. Morphological analysis reveals that the ventricular growth is spatially non-uniform, and that the most significant growth occurs during the first 6 months. The first 3 months of life exhibit a significant (p<0.01) bilateral lengthening of the anterior lateral ventricle and a significant increase of radius (p<0.01) and area (p<0.01) at the posterior portion of the ventricle. Shape analysis shows that the horns exhibit a faster growth rate than the mid-body. Finally, bilateral significant age effects (p<0.01) are observed for the growth of LVs whereas gender effects are more subtle and significant effects (p<0.01) only present at the left anterior and posterior horns. More importantly, both the age and gender effects are growth directionally dependent.ConclusionsWe have demonstrated the temporospatial shape growth characteristics of human LVs during the first two years of life using a unique longitudinal MR data set. A temporally and spatially non-uniform growth pattern was reported. These normative results could provide invaluable information to discern abnormal growth patterns in patients with neurodevelopmental disorders.

Project description:Measures of intrinsic brain function at rest show promise as predictors of cognitive decline in humans, including EEG metrics such as individual alpha peak frequency (IAPF) and the aperiodic exponent, reflecting the strongest frequency of alpha oscillations and the relative balance of excitatory:inhibitory neural activity, respectively. Both IAPF and the aperiodic exponent decrease with age and have been associated with worse executive function and working memory. However, few studies have jointly examined their associations with cognitive function, and none have examined their association with longitudinal cognitive decline rather than cross-sectional impairment. In a preregistered secondary analysis of data from the longitudinal Midlife in the United States (MIDUS) study, we tested whether IAPF and aperiodic exponent measured at rest predict cognitive function ( N = 234; age at EEG recording M = 54.86, SD = 10.76) over 10 years. The IAPF and the aperiodic exponent interacted to predict decline in overall cognitive ability, even after controlling for age, sex, education, and lag between data collection timepoints. Post-hoc tests showed that "mismatched" IAPF and aperiodic exponents (e.g., higher exponent with lower IAPF) predicted greater cognitive decline compared to "matching" IAPF and aperiodic exponents (e.g., higher exponent with higher IAPF; lower IAPF with lower aperiodic exponent). These effects were largely driven by measures of executive function. Our findings provide the first evidence that IAPF and the aperiodic exponent are joint predictors of cognitive decline from midlife into old age and thus may offer a useful clinical tool for predicting cognitive risk in aging.Significance statementMeasures of intrinsic brain function at rest assessed noninvasively from the scalp using electroencephalography (EEG) show promise as predictors of cognitive decline in humans. Using data from 234 participants from the Midlife in the United States (MIDUS) longitudinal study, we found two resting EEG markers (individual peak alpha frequency and aperiodic exponent) interacted to predict cognitive decline over a span of 10 years. Follow-up analyses revealed that "mismatched" markers (i.e., high in one and low in the other) predicted greater cognitive decline compared to "matching" markers. Because of the low cost and ease of collecting EEG data at rest, the current research provides evidence for possible scalable clinical applications for identifying individuals at risk for accelerated cognitive decline.

Dataset Information

Longitudinal changes in aperiodic and periodic activity in electrophysiological recordings in the first seven months of life.

Publications

Longitudinal changes in aperiodic and periodic activity in electrophysiological recordings in the first seven months of life.

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