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 |
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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. |
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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 |
Author_xml | – sequence: 1 givenname: Carina surname: Volk fullname: Volk, Carina organization: Children's Research Center, University Children's Hospital Zurich, Steinwiesstrasse 75, 8032, Zurich, Switzerland – sequence: 2 givenname: Valeria surname: Jaramillo fullname: Jaramillo, Valeria organization: Children's Research Center, University Children's Hospital Zurich, Steinwiesstrasse 75, 8032, Zurich, Switzerland – sequence: 3 givenname: Mirjam surname: Studler fullname: Studler, Mirjam organization: Children's Research Center, University Children's Hospital Zurich, Steinwiesstrasse 75, 8032, Zurich, Switzerland – sequence: 4 givenname: Melanie surname: Furrer fullname: Furrer, Melanie organization: Children's Research Center, University Children's Hospital Zurich, Steinwiesstrasse 75, 8032, Zurich, Switzerland – sequence: 5 givenname: Ruth L. surname: O'Gorman Tuura fullname: O'Gorman Tuura, Ruth L. organization: Children's Research Center, University Children's Hospital Zurich, Steinwiesstrasse 75, 8032, Zurich, Switzerland – sequence: 6 givenname: Reto surname: Huber fullname: Huber, Reto email: reto.huber@kispi.uzh.ch organization: Children's Research Center, University Children's Hospital Zurich, Steinwiesstrasse 75, 8032, Zurich, Switzerland |
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CitedBy_id | crossref_primary_10_1093_cercor_bhae046 crossref_primary_10_1016_j_neuroimage_2021_118281 crossref_primary_10_1016_j_neuroimage_2023_120087 crossref_primary_10_1093_sleep_zsaa038 crossref_primary_10_1016_j_neuroimage_2021_118420 crossref_primary_10_3390_cells13110970 crossref_primary_10_3389_fnins_2023_1266766 |
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Keywords | High-density EEG GLX Cortical plasticity MRS |
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Title | Diurnal changes in human brain glutamate + glutamine levels in the course of development and their relationship to sleep |
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