Characterization of the Functional Dynamics in the Neonatal Brain during REM and NREM Sleep States by means of Microstate Analysis

Abstract

Neonates spend most of their life sleeping. During sleep, their brain experiences fast changes in its functional organization. Microstate analysis permits to capture the rapid dynamical changes occurring in the functional organization of the brain by representing the changing spatio-temporal features of the electroencephalogram (EEG) as a sequence of short-lasting scalp topographies—the microstates. In this study, we modeled the ongoing neonatal EEG into sequences of a limited number of microstates and investigated whether the extracted microstate features are altered in REM and NREM sleep (usually known as active and quiet sleep states—AS and QS—in the newborn) and depend on the EEG frequency band. 19-channel EEG recordings from 60 full-term healthy infants were analyzed using a modified version of the k-means clustering algorithm. The results show that ~ 70% of the variance in the datasets can be described using 7 dominant microstate templates. The mean duration and mean occurrence of the dominant microstates were significantly different in the two sleep states. Microstate syntax analysis demonstrated that the microstate sequences characterizing AS and QS had specific non-casual structures that differed in the two sleep states. Microstate analysis of the neonatal EEG in specific frequency bands showed a clear dependence of the explained variance on frequency. Overall, our findings demonstrate that (1) the spatio-temporal dynamics of the neonatal EEG can be described by non-casual sequences of a limited number of microstate templates; (2) the brain dynamics described by these microstate templates depends on frequency; (3) the features of the microstate sequences can well differentiate the physiological conditions characterizing AS and QS.

The Arch Electrode: A Novel Dry Electrode Concept for Improved Wearing Comfort

“…EEG is widely used for medical diagnostics, e.g., in epilepsy, sleep disorders, coma, anesthesia, and stroke ( Niedermeyer and Lopes da Silva, 2005 ; Puce and Hämäläinen, 2017 ; Seeck et al, 2017 ). In the last two decades, its applications extended to an ever-increasing number of areas that include monitoring of motor rehabilitation ( Comani et al, 2015 ; Renton et al, 2017 ), neurodevelopment in preterm infants ( Hayashi-Kurahashi et al, 2012 ; Berchicci and Comani, 2015 ; Khazaei et al, 2021 ), cognitive decline including Alzheimer’s ( Paulsen et al, 2012 ), professional sports training ( Cheron et al, 2016 ; di Fronso et al, 2019 ), mental states ( Al-Barrak et al, 2017 ; di Flumeri et al, 2019 ), microstates ( Michel and Koenig, 2018 ), sleep states ( Khazaei et al, 2021 ), cognitive load ( Ortiz et al, 2020 ), and brain computer interfaces (BCI) ( Miranda et al, 2015 ; Stegman et al, 2020 ). Most new applications require specific characteristics of the EEG equipment so their full potential can be explored in real-life, mobile environments.…”

Characterizing the temporal dynamics and maturation of resting-state activity: an EEG microstate study in preterm and full-term infants

“…Initially proposed for investigating adult brain activity (Lehmann et al, 1987 Recently, the interest in using the microstate approach in infants has emerged, while eliciting various methodological questions (Bagdasarov et al, 2024;Brown et al, 2024;Khazaei et al, 2021). But studies in neonates are rare, focusing on the impact of sleep states on brain dynamics (Khazaei et al, 2021) and on habituation mechanisms to pain (Rupawala et al, 2023), with recent reports indicating MS dynamics change in the preterm period towards the termage (Hermans et al, 2023).…”

“…Initially proposed for investigating adult brain activity (Lehmann et al, 1987 Recently, the interest in using the microstate approach in infants has emerged, while eliciting various methodological questions (Bagdasarov et al, 2024;Brown et al, 2024;Khazaei et al, 2021). But studies in neonates are rare, focusing on the impact of sleep states on brain dynamics (Khazaei et al, 2021) and on habituation mechanisms to pain (Rupawala et al, 2023), with recent reports indicating MS dynamics change in the preterm period towards the termage (Hermans et al, 2023). In particular, the period of the first months after the term birth remains unexplored with microstate approach so far, whereas maturational processes including myelination and growth of short corticocortical connections show intense progression that potentially relates to accelerated brain functional dynamics and evolution of network spatial distributions.…”

Microstate Analysis of Infant EEG: Tutorial and Reliability

“…While microstate analysis has proven to be a highly informative method for studying brain function and organization at the millisecond-level in adults, very few studies using this approach in infants have been published. More speci cally, of the six publications that we identi ed, four used the microstate analytic approach to examine event-related data (Bucsea et al, 2023;Gui et al, 2021;Maitre et al, 2020;Rupawala et al, 2023), one examined microstates during sleep (Khazaei et al, 2021), and one used microstate analysis to examine spontaneous EEG data collected from infants (i.e., 34, 6-10-month-olds) during video-watching (Brown & Gartstein, 2023). Unfortunately, none of this prior work investigated the reliability of microstate-related measures at this age, a critical step in understanding the potential use of microstates to study individual differences in behavior and development (Lopez et al, 2023).…”