Abstract
Study ObjectivesIn adults, wakefulness can be markedly prolonged at the expense of sleep, e.g. to stay vigilant in the presence of a stressor. These extra-long wake bouts result in a heavy-tailed distribution (highly right-skewed) of wake but not sleep durations. In infants, the relative importance of wakefulness and sleep are reversed, as sleep is necessary for brain maturation. Here, we tested whether these developmental pressures are associated with the unique regulation of sleep–wake states.MethodsIn 175 infants of 28–40 weeks postmenstrual age (PMA), we monitored sleep–wake states using electroencephalography and behavior. We constructed survival models of sleep–wake bout durations and the effect of PMA and other factors, including stress (salivary cortisol), and examined whether sleep is resilient to nociceptive perturbations (a clinically necessary heel lance).ResultsWake durations followed a heavy-tailed distribution as in adults and lengthened with PMA and stress. However, differently from adults, active sleep durations also had a heavy-tailed distribution, and with PMA, these shortened and became vulnerable to nociception-associated awakenings.ConclusionsSleep bouts are differently regulated in infants, with especially long active sleep durations that could consolidate this state’s maturational functions. Curtailment of sleep by stress and nociception may be disadvantageous, especially for preterm infants given the limited value of wakefulness at this age. This could be addressed by environmental interventions in the future.
Highlights
In adults, positive feedback mechanisms within brainstem circuitry have likely evolved to allow wakefulness to be extensively prolonged at the expense of sleep when necessary, e.g. to t stay vigilant in the presence of a fitness-reducing stressor like a predator 1
Curtailment of sleep by stress and nociception may be disadvantageous, especially for pre-term infants given the limited value t of wakefulness at this age. This could be addressed by environmental interventions in future. rip Keywords Accepted Manusc neonate, premature, pain
The results show that sleep is differently sc regulated in human neonates to adults, leading to prolonged rapid eye movement (REM) u sleep bouts, and that clinically necessary painful procedures and physiological stress perturb n this intrinsic regulation
Summary
The mean proportion of time spent in active sleep and transitional sleep decreased with PMA, alongside an increase in the proportion of time spent in quiet sleep and awake: in particular, the proportion of wakefulness increased from just 3% in very pre-term infants to 15% in fullterm infants (Fig. 2). Ted M Physiological stress lengthened wake bout durations ep Wake bouts persisted for longer with increasing cortisol level (exp(est) per μg/10 dL 1.335 cc (95% CI: 1.019-1.749) (Fig. 5), and the addition of this variable improved PMA-only model Afit (AIC 144.688 vs 147.289; 20 wake onsets captured from 19 infants [32,33,34,35,36,37,38,39,40] weeks PMA, with offset captured in 16/20 instances). While nociception can trigger awakenings, physiological stress can prolong periods of wakefulness from at least as early as moderately pre-term age, as in older children and adults [1,40,80,81]. Wake bouts become longer, and nociception and stress sc funnel infants towards this state of heightened vigilance which will eventually u occupy two thirds of adult life, an enormous increase from the 3% occupancy in very preAccepted Man term infants
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