In this longitudinal birth cohort study, we show that (1) the proportion of daytime sleep at 12 months and IC at 30 months follows an inverted U-shaped relation, and (2) the association between time spent awake during night at 12 months and WM at 30 months is linear. By longitudinally examining the associations between infant sleep and toddler EF across the range of infant sleep outcomes, i.e. not only in those infants with sleep problems but also on those who might be labelled as “good sleepers” and “intermediate sleepers”, these findings extend the current understanding of the relationship between infant sleep and toddler EF and provide novel evidence to support a dose-dependent curvilinear relationship between sleep and EF during early childhood.
Consistent with our first hypothesis and with previous longitudinal study in infants (Bernier et al., 2010), we found that proportion of daytime sleep at 12 months was associated with IC at 30 months. While our finding of the inverted-U-shaped association between proportion of daytime sleep and IC is novel, previous cross-sectional studies with toddlers (Kocevska et al., 2017), children (Chaput et al., 2016), and adults (Leng et al., 2015) have suggested that sleep duration at both extremes is associated with negative health-related outcomes. This finding is also consistent with evidence from neuroendocrine literature, which reports inverted U-shaped associations between cortisol levels and cognition in both children (Jager et al., 2014) and adults (Schilling et al., 2013). Taken together, these findings and ours, suggest that non-linear patterns of association may describe the relationship between complex biological processes during early childhood more accurately than linear associations. Furthermore, daytime sleep time seems to be mostly determined by maturation (i.e. age) (Paavonen et al., 2020; Weissbluth, 1995), and most of the infants sleep an average of two hours during daytime. Interestingly, one recent longitudinal study reported that inappropriate amounts of daytime sleep were related to worse quality of night-time sleep in three to eight-month-old infants (Paavonen et al., 2019). Therefore, it is likely that infants with average amounts of daytime sleep most likely represent the normal ranges of the developmental stage also in other areas of development, such as cognition and/or self-regulation.
We did not find evidence to support our second hypothesis that shorter nighttime sleep is associated with lower performance in both IC and WM tasks. Such associations have been reported in two cross-sectional studies conducted in school-aged children (Cho et al., 2015; Lam et al., 2011). Our failure to confirm these previous findings could be explained by the fact that significant sleep deprivation might be quite uncommon in infants among whom sleep is strongly driven by homeostatic pressure (Jenni & LeBourgeois, 2006). Finally, we should take into account that some research supports the notion that EF in early childhood may be best described by a single factor, rather than by different aspects (Espy et al., 2011; Shing et al., 2010; Wiebe, Espy, & Charak, 2008), due to the fact that EF undergoes rapid development in infancy and that the subdomains of EF are highly interrelated at these early stages (Diamond, 2013).
Concerning our third hypothesis, this was partially confirmed as although we did not find significant associations between the number of night awakenings and IC at 30 months, we did found that time spent awake during the night at 12 months was longitudinally associated with WM performance at 30 months in a linear manner. This suggests that night awakenings are often normative in infants’ development, while long periods of time spent awake at night more likely indicates a deviance in sleep quality in early childhood. Number of night awakenings tends to remain stable during the first year of life, ranging from 0 to 3.4 episodes per night for very young infants (0–2 months), to 0-2.5 per night at the age of 12–24 months (Galland et al., 2012). Therefore, time spent awake at night might a better indicator of disturbed sleep than number of night awakenings, and thus time spent awake at night could be more harmful for the development of some EF, such as WM. Further studies on the effects of sleep fragmentation (i.e., frequency of night awakening and time awake at night) on the development of EF deficits are still needed. To the best of our knowledge, our study is the first one reporting an association between parent-reported time spent awake at night and EF in this age group.
Finally, it should be noted that the lack of association between number of night awakenings and EF could be also related to the use of parent-reported sleep measures in this study. For instance, while infants may briefly wake up during the night, many of them are able to fall back to sleep by themselves, and thus especially the very short awakenings are not necessarily noticed by their parents (Minde et al., 1993). Therefore, the use of more objective sleep measures, such as actigraphy, may be useful to measure the exact frequency of night awakenings. Furthermore, night awakenings are more frequent and more normative in infancy than later during development and, hence, they may have distinct impact on IC performance in older children.
Interestingly, our findings concerning sleep during the first year of life and EF (i.e., IC and WM) at the age of 30 months were only found when sleep was measured at the age of 12 months, while there were no associations between sleep at 6 months and EF at 30 months. One possible explanation could be that the high inter-individual variability in sleep quality which is mainly seen during the first 6 months of life, could be related to environmental factors that temporarily impair sleep in infants (Ednick et al., 2009). Therefore, the effects that sleep at 6 months exerts on later development in toddlers might be less robust. However, recent findings from our group using a different sample showed that parental reported short sleep duration at 3, 8, and 18 months was longitudinally associated with attention difficulties at the age of 5 years (Huhdanpaa et al., 2019). Nevertheless, the cognitive measures used in this previous study and our current study were different (i.e., parent-reported versus behavioral cognitive measures, respectively), and thus the results are not directly comparable
Overall, our findings support the hypothesis that sleep disruption in early childhood is longitudinally associated with later EF and that different sleep patterns in 12-month-old infants affect distinct aspects of EF (i.e., IC and WM) at the age of 30 months. Considering that EF and its associated neural circuitry experience rapid development during the ages of 2 and 5 years (Best & Miller, 2010), and that sleep plays a vital restorative role in brain functioning (Medic et al., 2017), disrupted sleep early in development could have negative longitudinal consequences for the development of EF. The findings of our study suggest that variation in sleep quality more clearly influences the variation in EF when sleep is measured at the infant age of 12 months compared to 6 months. At the age of 12 months, the most relevant sleep quality patterns from the perspective of toddler’s WM and IC are the measures related to the acquisition of the circadian rhythm (i.e. proportion of daytime sleep and time awake at night).
The main strength of our study is the large sample size and the longitudinal design, which captures the long-term consequences of early childhood sleep disturbances on IC and WM in toddlers. Moreover, we measured sleep at 6 and 12 months, which enabled us to examine the effects of sleep in very early stages of life. Furthermore, the study is population-based, and we were able to account for various confounding variables, including maternal factors and child cognitive development at 30 months. Another major strength of this study is the approach of using three different sleep groups of “good sleepers”, “intermediate sleepers” and “bad sleepers” to study the non-linear associations between sleep and EF.
Our study has some limitations. First, sleep measures were only reported using parental reports, and we did not use objective measures, such as actigraphy. While parental reports and objective reports may disagree in some cases (Molfese et al., 2015), sleep reports are still considered valid for assessing sleep in young children. Moreover, use of parental reports enables the collection of larger samples. Second, our sample was composed of relatively healthy mothers and infants; thus, generalization of the results should be made cautiously with respect to clinical populations. Third, no adjustment for current sleep at 30 months was available in this study, which may result in less accurate findings.