Sleep duration during weekdays affects hippocampal gray matter volume in healthy children
Highlights
► Sleep duration was positively correlated with gray matter volume in children. ► Those correlations were found in the bilateral hippocampus. ► Those correlations were found in sleep duration during weekdays, not weekends.
Introduction
Although the function of sleep remains debatable, sleep has been associated with the function and structure of the hippocampus. For example, one major theory about the function of sleep proposes that memory consolidation occurs predominantly during sleep, when the hippocampus sends information from memory to the neocortex for permanent storage (Axmacher et al., 2009). Additionally, sleep deprivation was shown to reduce the proliferation of cells and to suppress neurogenesis in the hippocampus of rats (Guzman-Marin et al., 2003, Guzman-Marin et al., 2005). Even human patients with primary insomnia showed significant reductions in hippocampal volume (Riemann et al., 2007). Although the correlation between sleep and the hippocampus has been elucidated in studies on animals and on human patients and although the influence of chronic sleep loss on the cognition of healthy children has been examined (Jan et al., 2010), the correlation between sleep and the hippocampal volume of healthy children has not yet been clarified. Understanding the correlation between sleep and the hippocampus of children is especially important to identify the sleeping habits associated with the development of a healthy brain and sound cognition. Therefore, we aimed to analyze the correlation between sleep duration and the hippocampal gray matter volume using brain magnetic resonance images of 290 healthy children aged 5–18 years by applying voxel-based morphometry (VBM). This approach enabled global analysis of brain structure and without bias towards any specific brain region while permitting the identification of potential differences or abnormalities in brain structures (Ashburner and Friston, 2000). We hypothesized that there would be a significant positive correlation between sleep duration and the hippocampal gray matter volume in healthy children.
Section snippets
Participants
All subjects were healthy Japanese children and the detail of the recruitment is written elsewhere (Taki et al., 2010). Briefly, we collected brain MR images from 290 subjects (145 boys, 145 girls; age range, 5.6–18.4 years) who did not have any history of malignant tumors, head traumas with a loss of consciousness lasting over 5 min, developmental disorders, epilepsy, psychiatric diseases, or claustrophobia. We announced that only right-handed children can participate in this study in an
Results
We found that the volume of the bilateral hippocampal body was significantly positively correlated with the duration of sleep during weekdays after adjusting for age, sex, and intracranial volume and after performing small-volume correction of the hippocampal ROI (left: t = 3.59, p = 0.014, family-wise error, corrected; right: t = 3.81, p = 0.007, family-wise error, corrected), as shown in Fig. 2. The whole-brain analysis showed that the duration of sleep during weekdays was substantially positively
Discussion
We demonstrated that the regional gray matter volume of the bilateral hippocampus was significantly positively correlated with the duration of sleep during weekdays. Although the mechanisms underlying this significant positive correlation have not been clarified, the findings of several studies in rats and humans have supported these results. The generation of new neurons in dentate gyrus of the hippocampus has been confirmed in several mammals, including humans (Eriksson et al., 1998, Gould et
Acknowledgments
We thank Y. Yamada for collecting MR data, and Y. Suzuki for technical support. This work was supported by a Ministry of Education, Culture, Sports, Science and Technology Grant-in-Aid for Young Scientists (B) (grant number 20790875).
References (40)
A fast diffeomorphic image registration algorithm
NeuroImage
(2007)- et al.
Voxel-based morphometry—the methods
NeuroImage
(2000) - et al.
Unified segmentation
NeuroImage
(2005) - et al.
Computing average shaped tissue probability templates
NeuroImage
(2009) - et al.
Can voxel based morphometry, manual segmentation and automated segmentation equally detect hippocampal volume differences in acute depression?
NeuroImage
(2009) - et al.
The influence of sleep quality, sleep duration and sleepiness on school performance in children and adolescents: a meta-analytic review
Sleep Med. Rev.
(2010) - et al.
A voxel-based morphometric study of ageing in 465 normal adult human brains
NeuroImage
(2001) - et al.
Synaptogenesis in human visual cortex—evidence for synapse elimination during normal development
Neurosci. Lett.
(1982) - et al.
Long-term sleep disturbances in children: a cause of neuronal loss
Eur. J. Paediatr. Neurol.
(2010) - et al.
Evaluation of 14 nonlinear deformation algorithms applied to human brain MRI registration
NeuroImage
(2009)
Development of a superior frontal-intraparietal network for visuo-spatial working memory
Neuropsychologia
An automated method for neuroanatomic and cytoarchitectonic atlas-based interrogation of fMRI data sets
NeuroImage
Differences in reported sleep need among adolescents
J. Adolesc. Health
The assessment and analysis of handedness: the Edinburgh inventory
Neuropsychologia
Mapping brain maturation and cognitive development during adolescence
Trends Cogn. Sci.
Sleep function and synaptic homeostasis
Sleep Medicine Reviews
The relationship between frontal gray matter volume and cognition varies across the healthy adult lifespan
Am. J. Geriatr. Psychiatry
Memory processes during sleep: beyond the standard consolidation theory
Cell. Mol. Life Sci.
Japanese Wechsler Intelligence Scale for Children
Working memory: looking back and looking forward
Nat. Rev. Neurosci.
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