Emergence of mature cortical activity in wakefulness and sleep in healthy preterm and full-term infants

Abstract

Study ObjectivesCortical activity patterns develop rapidly over the equivalent of the last trimester of gestation, in parallel with the establishment of sleep architecture. However, the emergence of mature cortical activity in wakefulness compared with sleep states in healthy preterm infants is poorly understood.MethodsTo investigate whether the cortical activity has a different developmental profile in each sleep–wake state, we recorded 11-channels electroencephalography (EEG), electrooculography (EOG), and respiratory movement for 1 hr from 115 infants 34 to 43 weeks–corrected age, with 0.5–17 days of postnatal age. We characterized the trajectory of δ, θ, and α-β oscillations in wakefulness, rapid eye movement (REM) sleep, and non-REM sleep by calculating the power spectrum of the EEG, averaged across artifact-free epochs.Resultsδ-Oscillations in wakefulness and REM sleep decrease with corrected age, particularly in the temporal region, but not in non-REM sleep. θ-Oscillations increase with corrected age in sleep, especially non-REM sleep, but not in wakefulness. On the other hand, α-β oscillations decrease predominantly with postnatal age, independently of sleep–wake state, particularly in the occipital region.ConclusionsThe developmental trajectory of δ and θ rhythms is state-dependent and results in changed cortical activity patterns between states with corrected age, which suggests that these frequency bands may have particular functional roles in each state. Interestingly, postnatal age is associated with a decrease in α-β oscillations overlying primary visual cortex in every sleep–wake state, suggesting that postnatal experience (including the first visual input through open eyes during periods of wakefulness) is associated with resting-state visual cortical activity changes.

EEG, behavioural and physiological recordings following a painful procedure in human neonates

“…The ECG highlights episodes of tachycardia and bradycardia which are common in pre-term infants, with bradycardia episodes often associated with apnoea and desaturation 39 , 40 . Both ECG and respiratory data improve the detection of artefacts such as associated with heart rate or widespread movement 41 , and inform infant sleep staging 42 , 43 .…”

The Developing Human Connectome Project: typical and disrupted perinatal functional connectivity

“…While the fMRI preprocessing pipeline for the dHCP (Fitzgibbon et al, 2019) addresses the potential problem of head motion in rs-fMRI data (Power et al, 2012;Satterthwaite et al, 2012), motion is also a surrogate marker of the arousal state of the infant, which interacts with the underlying neural activity (Denisova, 2019;Whitehead et al, 2018). To address this issue, we opted for a conservative approach consisting in the selection of a continuous sub-sample of the data (~70%) with lowest motion for each subject, and excluding those subjects with a high level of motion from further analyses.…”

Sleep–wake regulation in preterm and term infants

“…We selected postnatal age, lower vs. higher risk of adverse neurodevelopment (see Supplementary Information), a preceding sensory perturbation, physiological stress, and position of the bout within the sleep-wake cycle (i.e. which transition occurred at bout offset) to additionally enter into the model as potential secondary explanatory variables, according to previous work 16,[37][38][39][40][41][42] . The first three variables, which were available for all data points, were entered into the overall models.…”