Diurnal changes in human brain glutamate + glutamine levels in the course of development and their relationship to sleep

Sleep slow waves during non-rapid eye movement (NREM) sleep play a crucial role in maintaining cortical plasticity, a process that is especially important in the developing brain. Children show a considerably larger overnight decrease in slow wave activity (SWA; the power in the EEG frequency band b...

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Published in:NeuroImage (Orlando, Fla.) Vol. 196; pp. 269 - 275
Main Authors: Volk, Carina, Jaramillo, Valeria, Studler, Mirjam, Furrer, Melanie, O'Gorman Tuura, Ruth L., Huber, Reto
Format: Journal Article
Language:English
Published: United States Elsevier Inc 01-08-2019
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Abstract Sleep slow waves during non-rapid eye movement (NREM) sleep play a crucial role in maintaining cortical plasticity, a process that is especially important in the developing brain. Children show a considerably larger overnight decrease in slow wave activity (SWA; the power in the EEG frequency band between 1 and 4.5 ​Hz during NREM sleep), which constitutes the primary electrophysiological marker for the restorative function of sleep. We previously demonstrated in adults that this marker correlates with the overnight reduction in cortical glutamate ​+ ​glutamine (GLX) levels assessed by magnetic resonance spectroscopy (MRS), proposing GLX as a promising biomarker for the interplay between cortical plasticity and SWA. Here, we used a multimodal imaging approach of combined MRS and high-density EEG in a cross-sectional cohort of 46 subjects from 8 to 24 years of age in order to examine age-related changes in GLX and its relation to SWA. Gray matter volume, GLX levels and SWA showed the expected age-dependent decrease. Unexpectedly, the overnight changes in GLX followed opposite directions when comparing children to adults. These age-related changes could neither be explained by the overnight decrease in SWA nor by circadian factors. •Brain metabolite overnight changes were assessed by magnetic resonance spectroscopy.•The change in glutamate ​+ ​glutamine (GLX) was larger in adults than in children.•The overnight change in GLX did not correlate with the main EEG markers of sleep.•The time of day influence on GLX levels should be considered differently across age.
AbstractList Sleep slow waves during non-rapid eye movement (NREM) sleep play a crucial role in maintaining cortical plasticity, a process that is especially important in the developing brain. Children show a considerably larger overnight decrease in slow wave activity (SWA; the power in the EEG frequency band between 1 and 4.5 ​Hz during NREM sleep), which constitutes the primary electrophysiological marker for the restorative function of sleep. We previously demonstrated in adults that this marker correlates with the overnight reduction in cortical glutamate ​+ ​glutamine (GLX) levels assessed by magnetic resonance spectroscopy (MRS), proposing GLX as a promising biomarker for the interplay between cortical plasticity and SWA. Here, we used a multimodal imaging approach of combined MRS and high-density EEG in a cross-sectional cohort of 46 subjects from 8 to 24 years of age in order to examine age-related changes in GLX and its relation to SWA. Gray matter volume, GLX levels and SWA showed the expected age-dependent decrease. Unexpectedly, the overnight changes in GLX followed opposite directions when comparing children to adults. These age-related changes could neither be explained by the overnight decrease in SWA nor by circadian factors.
Sleep slow waves during non-rapid eye movement (NREM) sleep play a crucial role in maintaining cortical plasticity, a process that is especially important in the developing brain. Children show a considerably larger overnight decrease in slow wave activity (SWA; the power in the EEG frequency band between 1 and 4.5 ​Hz during NREM sleep), which constitutes the primary electrophysiological marker for the restorative function of sleep. We previously demonstrated in adults that this marker correlates with the overnight reduction in cortical glutamate ​+ ​glutamine (GLX) levels assessed by magnetic resonance spectroscopy (MRS), proposing GLX as a promising biomarker for the interplay between cortical plasticity and SWA. Here, we used a multimodal imaging approach of combined MRS and high-density EEG in a cross-sectional cohort of 46 subjects from 8 to 24 years of age in order to examine age-related changes in GLX and its relation to SWA. Gray matter volume, GLX levels and SWA showed the expected age-dependent decrease. Unexpectedly, the overnight changes in GLX followed opposite directions when comparing children to adults. These age-related changes could neither be explained by the overnight decrease in SWA nor by circadian factors. •Brain metabolite overnight changes were assessed by magnetic resonance spectroscopy.•The change in glutamate ​+ ​glutamine (GLX) was larger in adults than in children.•The overnight change in GLX did not correlate with the main EEG markers of sleep.•The time of day influence on GLX levels should be considered differently across age.
Sleep slow waves during non-rapid eye movement (NREM) sleep play a crucial role in maintaining cortical plasticity, a process that is especially important in the developing brain. Children show a considerably larger overnight decrease in slow wave activity (SWA; the power in the EEG frequency band between 1 and 4.5 ​Hz during NREM sleep), which constitutes the primary electrophysiological marker for the restorative function of sleep. We previously demonstrated in adults that this marker correlates with the overnight reduction in cortical glutamate ​+ ​glutamine (GLX) levels assessed by magnetic resonance spectroscopy (MRS), proposing GLX as a promising biomarker for the interplay between cortical plasticity and SWA. Here, we used a multimodal imaging approach of combined MRS and high-density EEG in a cross-sectional cohort of 46 subjects from 8 to 24 years of age in order to examine age-related changes in GLX and its relation to SWA. Gray matter volume, GLX levels and SWA showed the expected age-dependent decrease. Unexpectedly, the overnight changes in GLX followed opposite directions when comparing children to adults. These age-related changes could neither be explained by the overnight decrease in SWA nor by circadian factors.
Author Studler, Mirjam
O'Gorman Tuura, Ruth L.
Furrer, Melanie
Huber, Reto
Volk, Carina
Jaramillo, Valeria
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Keywords High-density EEG
GLX
Cortical plasticity
MRS
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Snippet Sleep slow waves during non-rapid eye movement (NREM) sleep play a crucial role in maintaining cortical plasticity, a process that is especially important in...
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SubjectTerms Adolescent
Adult
Adults
Age
Alcohol
Brain - anatomy & histology
Brain - growth & development
Brain - metabolism
Caffeine
Child
Children
Children & youth
Circadian Rhythm
Circadian rhythms
Cortex
Cortical plasticity
Diurnal
EEG
Electroencephalography
Female
Glutamic Acid - metabolism
Glutamine
Glutamine - metabolism
GLX
Gray Matter - anatomy & histology
High-density EEG
Humans
Magnetic resonance spectroscopy
Male
Metabolism
Metabolites
MRS
Neural plasticity
Neuroimaging
NMR
NREM sleep
Nuclear magnetic resonance
REM sleep
Scanners
Sleep
Spectrum analysis
Substantia grisea
Teenagers
Young Adult
Title Diurnal changes in human brain glutamate + glutamine levels in the course of development and their relationship to sleep
URI https://dx.doi.org/10.1016/j.neuroimage.2019.04.040
https://www.ncbi.nlm.nih.gov/pubmed/30991127
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