Effects of sleep duration on neurocognitive development in early adolescents in the USA: a propensity score matched, longitudinal, observational study

Abstract

Background: Although the American Academy of Sleep Medicine suggests at least 9 h of sleep per day for 6-12-year-olds, children in recent generations often report sleeping less than this amount. Because early adolescence is a crucial period for neurocognitive development, we aimed to investigate how insufficient sleep affects children's mental health, cognition, brain function, and brain structure over 2 years.

Methods: In this propensity score matched, longitudinal, observational cohort study, we obtained data from a population-based sample of 9-10-year-olds from 21 US study sites in the ongoing Adolescent Brain Cognitive Development (ABCD) study. Participants were categorised as having sufficient sleep or insufficient sleep on the basis of a cutoff of 9 h sleep per day. Using propensity score matching, we matched these two groups of participants on 11 key covariates, including sex, socioeconomic status, and puberty status. Participants were excluded from our analysis if they did not pass a baseline resting-state functional MRI quality check or had missing data for the covariates involved in propensity score matching. Outcome measures retrieved from the ABCD study were behavioural problems, mental health, cognition, and structural and resting-state functional brain measures, assessed at baseline and at 2-year follow-up. We examined group differences on these outcomes over those 2 years among all eligible participants. We then did mediation analyses of the neural correlates of behavioural changes induced by insufficient sleep.

Findings: Between Sept 1, 2016, and Oct 15, 2018, 11 878 individuals had baseline data collected for the ABCD study, of whom 8323 were eligible and included in this study (4142 participants in the sufficient sleep group and 4181 in the insufficient sleep group). Follow-up data were collected from July 30, 2018, to Jan 15, 2020. We identified 3021 matched sufficient sleep-insufficient sleep pairs at baseline and 749 matched pairs at 2-year follow-up, and observed similar differences between the groups in behaviour and neural measures at both timepoints; the effect sizes of between-group differences in behavioural measures at these two timepoints were significantly correlated with each other (r=0·85, 95% CI 0·73-0·92; p<0·0001). A similar pattern was observed in resting-state functional connectivity (r=0·54, 0·45-0·61; p<0·0001) and in structural measures (eg, in grey matter volume r=0·61, 0·51-0·69; p<0·0001). We found that cortico-basal ganglia functional connections mediate the effects of insufficient sleep on depression, thought problems, and crystallised intelligence, and that structural properties of the anterior temporal lobe mediate the effect of insufficient sleep on crystallised intelligence.

Interpretation: These results provide population-level evidence for the long-lasting effect of insufficient sleep on neurocognitive development in early adolescence. These findings highlight the value of early sleep intervention to improve early adolescents' long-term developmental outcomes.

Funding: National Institutes of Health.

Figure 1.. Sleep duration changes in SS and IS groups over two years.

SS (left) and IS (right) groups were identified based on the baseline assessment of sleep duration (9 hours as a cutoff) with well-matched covariates. Over two years, participants’ sleep pattern in the IS group remained relatively stable, whereas participants in the SS group slept less and less. In addition, we performed a visual illustration of how sleep duration changes with crystallized intelligence, see Figure S6. Note: SS = sufficient sleep; IS = insufficient sleep; FL1 = 1-year follow-up; FL2 = 2-year follow-up.

Figure 2.. The effects of insufficient sleep on behavioral measures.

Cohen’s d for behavior problems (blue), cognition (green), and mental health (yellow) in the comparions between SS and IS groups at baseline (A) and at FL2 (B). (C) The impact of insufficient sleep on behavioral measures at baseline are significantly correlated with that on FL2. Note: SS = sufficient sleep; IS = insufficient sleep; FL2 = 2-year follow-up; see Table S3 for variable names used in the figure. At FL2, four measures of cognition were not available: nihtbx_list_uncorrected, nihtbx_cardsort_uncorrected, nihtbx_fluidcomp_uncorrected, and nihtbx_totalcomp_uncorrected.

Figure 3.. The effects of insufficient sleep on resting-state functional connectivity.

Cohen’s d for resting-state functional connectivity measures in the comparisons between SS and IS group at baseline (A) and at FL2 (B). Red denotes SS group have higher connectivity than IS group, while blue means SS group have lower connectivity compared to IS group. (C) The impact of insufficient sleep on resting-state functional connectivity at baseline are significantly correlated with that on FL2. Note: SS = sufficient sleep; IS = insufficient sleep; FL2 = 2-year follow-up.

Figure 4.. The effects of insufficient sleep on brain structural measurements.

Cohen’s d for GMV (A, B) and cortical areas (D, E) in the comparions between SS and IS groups at baseline and at FL2. (C, F) The impact of insufficient sleep on brain structure measure at baseline are significantly correlated with that on FL2. Note: SS = sufficient sleep; IS = insufficient sleep; FL2 = 2-year follow-up.

Figure 5.. Baseline brain measures mediated the effect of insufficient sleep on behavioral problems and cognition at baseline (A & C) and FL2 (B & D).

Based on matched group comparisons, we have examined how brain measures identified with larger effect sizes in respective categories (i.e.,rs 5 rs-FC, 3 cortical areas, and 3 GMV; Y-axis) would mediate the effects of sleep duration on the 4 behavioral measures identified with a Cohen’s d greater 0.15 (i.e., depression, thought problems, picture-vocabulary test performance, and crystallized intelligence; Y-axis). Also see Figure S5 for analyses based on all behavioral variables. Color bars are coded based on log-transferred bootstrapped p-values of the mediation effects. Only the effects reached statistical significance (p < .05) using bootstrap sampling with 100,000 random-generated samples shown in the figure. Note: rs-FC: resting-state functional connectivity; au: auditory network; cerc: cingulo-opercular network; copa: cingulo-parietal network; rst: retrosplenial-temporal network; ventralDC: ventral diencephalon; ACC: anterior cingulate cortex; FL2: 2-year follow-up.