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

Kimberley Whitehead,Maria Pureza Laudiano-Dray,Judith Meek,Lorenzo Fabrizi

doi:10.1093/sleep/zsy096

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.

Highlights

Cortical activity patterns develop rapidly over the equivalent of the last trimester of gestation [1, 2]
The 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
Postnatal age is associated with a decrease in α-β oscillations overlying primary visual cortex in every sleep–wake state, suggesting that postnatal experience is associated with resting-state visual cortical activity changes

Summary

Introduction

Cortical activity patterns develop rapidly over the equivalent of the last trimester of gestation [1, 2]. Neural oscillations can be used as an index of cortical network maturation as they reflect the assembly of mature functional networks and predict structural brain growth [3, 4]. They thereby offer a clinically valuable window onto brain development [2]. Rapid eye movement (REM) sleep, and non-REM sleep are first associated with characteristic neural activity patterns from 31 to 34 weeks–corrected age (CA) as sleep–wake architecture emerges [13, 14], wakefulness is still extremely scarce, occupying as little as 2 per cent of preterm life [15]. By 40 weeks–CA, cyclical periods of wakefulness are well-organized around feeds on demand and electrographic correlates of sleep–wake state are clearly defined [1, 18]

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Conclusion