Increased coupling between global grey matter and CSF-derived fMRI signal in young adults after partial sleep deprivation – evidence from the sleepy brain study
Cornelius Berberich , Leander Müller , Benedikt Zott , Rachel Nuttal , Gerhard Schneider , Claus Zimmer , Christian Sorg , Dennis M. Hedderich , Juliana Zimmermann
{"title":"Increased coupling between global grey matter and CSF-derived fMRI signal in young adults after partial sleep deprivation – evidence from the sleepy brain study","authors":"Cornelius Berberich , Leander Müller , Benedikt Zott , Rachel Nuttal , Gerhard Schneider , Claus Zimmer , Christian Sorg , Dennis M. Hedderich , Juliana Zimmermann","doi":"10.1016/j.neuroimage.2025.121420","DOIUrl":null,"url":null,"abstract":"<div><div>Evidence indicates that brain waste clearance happens more efficiently during sleep. Recent studies suggest that the correlation, i.e., coupling, between the cortical grey matter (gGM) blood oxygenation level-dependent signal and cerebrospinal fluid (CSF) signal in the foramen magnum, measured via resting-state functional MRI (fMRI), serves as a non-invasive measure of the ventricular CSF system. Sleep deprivation has been demonstrated to affect brain function and health. Our aim is to assess gGM-CSF coupling after partial sleep deprivation, hypothesizing a change in the coupling measure relative to normal sleep.</div><div>To test this hypothesis, we analyzed resting-state fMRI data from 63 healthy participants in the “The Stockholm Sleepy Brain Study”, grouped according to age: younger (20 - 29 years) and older (65 - 75 years) adults. We examined gGM-CSF coupling twice in each subject, in the evening following a night of normal sleep and after a night of partial sleep deprivation (≤ 3 h of sleep).</div><div>Our results revealed significantly increased gGM-CSF coupling after sleep deprivation compared to normal sleep (mean <em>r</em> = -0.30 ± 0.19 vs. -0.25 ± 0.14; t(62) = 2.05, <em>p</em> = 0.045). A linear mixed model demonstrated a significant interaction of age with the sleep condition (β = 0.0031, <em>t</em> = 2.73, <em>p</em> = 0.0083), showing significant changes only in the younger subgroup (t(35) = 2.99, <em>p</em> = 0.0050).</div><div>These findings indicate that gGM-CSF coupling increases after partial sleep deprivation in younger adults, which may reflect compensatory mechanisms in response to reduced sleep duration. Furthermore, the results suggest that this compensatory response could be diminished in older adults.</div></div>","PeriodicalId":19299,"journal":{"name":"NeuroImage","volume":"318 ","pages":"Article 121420"},"PeriodicalIF":4.5000,"publicationDate":"2025-08-15","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":"0","resultStr":null,"platform":"Semanticscholar","paperid":null,"PeriodicalName":"NeuroImage","FirstCategoryId":"3","ListUrlMain":"https://www.sciencedirect.com/science/article/pii/S1053811925004239","RegionNum":2,"RegionCategory":"医学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":null,"EPubDate":"","PubModel":"","JCR":"Q1","JCRName":"NEUROIMAGING","Score":null,"Total":0}
引用次数: 0
Abstract
Evidence indicates that brain waste clearance happens more efficiently during sleep. Recent studies suggest that the correlation, i.e., coupling, between the cortical grey matter (gGM) blood oxygenation level-dependent signal and cerebrospinal fluid (CSF) signal in the foramen magnum, measured via resting-state functional MRI (fMRI), serves as a non-invasive measure of the ventricular CSF system. Sleep deprivation has been demonstrated to affect brain function and health. Our aim is to assess gGM-CSF coupling after partial sleep deprivation, hypothesizing a change in the coupling measure relative to normal sleep.
To test this hypothesis, we analyzed resting-state fMRI data from 63 healthy participants in the “The Stockholm Sleepy Brain Study”, grouped according to age: younger (20 - 29 years) and older (65 - 75 years) adults. We examined gGM-CSF coupling twice in each subject, in the evening following a night of normal sleep and after a night of partial sleep deprivation (≤ 3 h of sleep).
Our results revealed significantly increased gGM-CSF coupling after sleep deprivation compared to normal sleep (mean r = -0.30 ± 0.19 vs. -0.25 ± 0.14; t(62) = 2.05, p = 0.045). A linear mixed model demonstrated a significant interaction of age with the sleep condition (β = 0.0031, t = 2.73, p = 0.0083), showing significant changes only in the younger subgroup (t(35) = 2.99, p = 0.0050).
These findings indicate that gGM-CSF coupling increases after partial sleep deprivation in younger adults, which may reflect compensatory mechanisms in response to reduced sleep duration. Furthermore, the results suggest that this compensatory response could be diminished in older adults.
期刊介绍:
NeuroImage, a Journal of Brain Function provides a vehicle for communicating important advances in acquiring, analyzing, and modelling neuroimaging data and in applying these techniques to the study of structure-function and brain-behavior relationships. Though the emphasis is on the macroscopic level of human brain organization, meso-and microscopic neuroimaging across all species will be considered if informative for understanding the aforementioned relationships.