This study investigated the relationship between chronotype and cognitive function in children. Subsequently, the relationship between chronotype and specific regional brain volumes related to cognitive function was examined. The primary findings were that chronotype is (i) negatively associated with the scores on picture vocabulary and picture sequence memory tasks (Fig. 1); and (ii) negatively associated with the volumes of the left precentral gyrus, right superior parietal cortex, and right posterior cingulate cortex (Fig. 2). These findings suggest that late chronotype is associated not only with low language and episodic memory performance but also with reduced volumes of the precentral gyrus, superior parietal cortex, and posterior cingulate cortex. Furthermore, we examined the relationship between these regional brain volumes, and language and episodic memory performance, finding that the precentral gyrus and posterior cingulate cortex are positively associated with vocabulary and episodic memory skills, respectively (Fig. 3). This suggests that, in childhood, the association between late chronotype and decreased volumes in the precentral gyrus and posterior cingulate cortex may be related to a reduction in vocabulary and episodic memory skills.
In contrast to previous reports that late chronotype in adults is associated with better memory and verbal ability 8–10, this study revealed a negative association between chronotype, and picture vocabulary and picture sequence memory task performances, suggesting that late chronotype is associated with lower vocabulary and episodic memory skills in children. A possible reason for this discrepancy is age-related differences in preferred chronotype. Roenneberg et al. found that children (aged 10–12 years) exhibit an early chronotype and tend to shift toward a late chronotype around the age of 20 years 4, suggesting that early chronotype may be biologically preferred during childhood 4, 40. Thus, in children with a mean age of 11.09 years, as in the current study, early chronotype may be preferable to maintain cognitive performance. Furthermore, late chronotype is associated with larger daily sleep debt, morning sleepiness, and poorer sleep quality 41–43. As good night-time sleep has been implicated in better language and memory consolidation 44, 45, children with late chronotype may be particularly vulnerable to impaired vocabulary and episodic memory skills, possibly due to accumulated sleep debt.
Based on previous findings 14, 15, 17–19, 35–37 and our behavioral results, language-related and episodic memory-related ROI analysis revealed negative associations between chronotype, and the left precentral gyrus, right superior parietal cortex, and right posterior cingulate cortex. Moreover, larger volumes of the left precentral gyrus and right posterior cingulate cortex were associated with higher scores on the picture vocabulary and picture sequence memory tasks, respectively. These findings suggest that in children, late chronotype is associated with smaller volumes in the left precentral gyrus and right posterior cingulate cortex that in turn influence vocabulary and episodic memory skills. In contrast, a few studies have reported that early chronotypes were associated with smaller gray matter volume in the posterior parietal cortex, lateral occipital cortex, and precuneus in adults 12, 13. Because these studies considered adults who may have gradually become late chronotypes post-childhood 4, the relationship between the previous findings and our results in children cannot be clearly interpreted. Since sleep duration may be associated with structural brain health 46, the current results highlight the impact of late chronotype in children on the structural deterioration of the precentral gyrus and posterior cingulate cortex.
The precentral gyrus is involved in motor control 47 and language processing 14, 48. Schug et al. reported that bilingual children have larger gray matter volume in the left precentral gyrus compared to monolingual children 49, suggesting that such structural characteristics play an important role in speech motor control 50 and its feedback processing 51, which is required for precise vocabulary knowledge. This region is also associated with sleep deprivation 52, and is engaged in a premediated state to prepare the brain for motor execution and coordination 53. The association between late chronotype and decreased precentral gyrus volume in children may be related to a reduction in vocabulary knowledge involving speech-related motor execution.
In addition, the posterior cingulate cortex, a key node in the default mode network 54, is involved in planning for the future, internal/external thought, attention, and episodic memory (i.e., autobiographical memories) 18, 36, 55, suggesting that structural and functional anomalies in this region are associated with the suppression of self-referential processing 56. Moreover, a recent study reported that changes in functional connectivity in the posterior cingulate cortex seed predict sleepiness 57, suggesting that abnormalities in the neural network in the posterior cingulate cortex may influence the induction of sleepiness. Some studies reported that poorer sleep quality and sleep abnormality are associated with a reduction in the volume of the posterior cingulate cortex 58, 59. As late chronotype has been implicated in morning sleepiness and poorer sleep quality 41–43, the daily accumulation of late chronotype-related sleep debt may strongly influence structural anomalies in the posterior cingulate cortex. In other words, the association between late chronotype and volume reduction in the posterior cingulate cortex in children may produce episodic memory impairment on account of the daily accumulation of sleep debt.
Our study has several limitations. First, our design was cross-sectional; thus, we plan to investigate longitudinally whether late chronotype is associated with behavioral changes and brain structural development in childhood. Second, this study used a restricted cognitive assessment battery from the NIH Toolbox because of missing data on working memory-related tasks. Therefore, future research should examine associations with late chronotype using a broader spectrum of neuropsychological measures in childhood.