{"title":"Effects of acute sleep deprivation on the brain function of individuals with migraine: a resting-state functional magnetic resonance imaging study.","authors":"Shuqing Wang, Longteng Ma, Song Wang, Caohui Duan, Xinyu Wang, Xiangbing Bian, Deqi Zhai, Yin Sun, Siyuan Xie, Shuhua Zhang, Yingyuan Liu, Xiaoxue Lin, Ruobing Wang, Xiu Liu, Shengyuan Yu, Xin Lou, Zhao Dong","doi":"10.1186/s10194-025-02004-4","DOIUrl":null,"url":null,"abstract":"<p><strong>Background: </strong>Sleep deprivation can trigger acute headache attacks in individuals with migraine; however, the underlying mechanism remains poorly understood. The aim of this study was to investigate the effects of acute sleep deprivation (ASD) on brain function in individuals with migraine without aura (MWoA) via functional magnetic resonance imaging (fMRI).</p><p><strong>Methods: </strong>Twenty three MWoA individuals and 23 healthy controls (HCs) were fairly included in this study. All participants underwent two MRI scans: one at baseline (prior to sleep deprivation) and another following 24 h of ASD. Images were obtained with blood-oxygen-level-dependent and T1-weighted sequences on a Siemens 7.0 T MRI scanner. We conducted analyses of changes in the low-frequency fluctuations (ALFF) values and functional connectivity (FC) between brain networks and within network before and after ASD in both MWoA group and HC group. Additionally, we investigated the relationship between the changes in ALFF before and after ASD and the clinical features (VAS and monthly headache days).</p><p><strong>Results: </strong>In the HC group, ASD led to a significant increase in ALFF values in the left parahippocampal gyrus compared to baseline (p-FDR = 0.01). In the MWoA group, ALFF values were significantly greater in 64 brain regions after ASD than at baseline. The most significant change in ALFF before and after ASD in the MWoA group was detected in the right medial pulvinar of the thalamus (p-FDR = 0.017), which showed a significant negative correlation with monthly headache days. Moreover, seed-based connectivity (SBC) analysis using the right medial pulvinar of the thalamus as the seed point revealed significantly increased connectivity with the cerebellar vermis (p-FWE = 0.035) after ASD in individuals with MWoA, whereas connectivity with the right postcentral gyrus was significantly decreased (p-FWE = 0.048). Furthermore, we performed analyses of between-network connectivity (BNC) and within-network connectivity across 17 brain networks, utilizing the Yeo-17 atlas. Both MWoA individuals and HCs showed no significant changes in BNC after ASD compared to baseline. However, our analysis in within-network revealed that MWoA individuals exhibited a reduced within-network FC in dorsal attention network (DAN) after ASD compared to baseline (p-FDR = 0.031), whereas HCs showed no significant differences in within-network FC across all networks before and after ASD.</p><p><strong>Conclusions: </strong>In comparison to HCs, MWoA individuals exhibited significant alterations in brain function after ASD, particularly within the thalamus, and MWoA individuals exhibited a reduced within-network FC in DAN after ASD compared to baseline. Brain regions and networks in MWoA individuals were more susceptible to the effects of ASD.</p>","PeriodicalId":16013,"journal":{"name":"Journal of Headache and Pain","volume":"26 1","pages":"60"},"PeriodicalIF":7.3000,"publicationDate":"2025-03-28","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11954264/pdf/","citationCount":"0","resultStr":null,"platform":"Semanticscholar","paperid":null,"PeriodicalName":"Journal of Headache and Pain","FirstCategoryId":"3","ListUrlMain":"https://doi.org/10.1186/s10194-025-02004-4","RegionNum":1,"RegionCategory":"医学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":null,"EPubDate":"","PubModel":"","JCR":"Q1","JCRName":"CLINICAL NEUROLOGY","Score":null,"Total":0}
引用次数: 0
Abstract
Background: Sleep deprivation can trigger acute headache attacks in individuals with migraine; however, the underlying mechanism remains poorly understood. The aim of this study was to investigate the effects of acute sleep deprivation (ASD) on brain function in individuals with migraine without aura (MWoA) via functional magnetic resonance imaging (fMRI).
Methods: Twenty three MWoA individuals and 23 healthy controls (HCs) were fairly included in this study. All participants underwent two MRI scans: one at baseline (prior to sleep deprivation) and another following 24 h of ASD. Images were obtained with blood-oxygen-level-dependent and T1-weighted sequences on a Siemens 7.0 T MRI scanner. We conducted analyses of changes in the low-frequency fluctuations (ALFF) values and functional connectivity (FC) between brain networks and within network before and after ASD in both MWoA group and HC group. Additionally, we investigated the relationship between the changes in ALFF before and after ASD and the clinical features (VAS and monthly headache days).
Results: In the HC group, ASD led to a significant increase in ALFF values in the left parahippocampal gyrus compared to baseline (p-FDR = 0.01). In the MWoA group, ALFF values were significantly greater in 64 brain regions after ASD than at baseline. The most significant change in ALFF before and after ASD in the MWoA group was detected in the right medial pulvinar of the thalamus (p-FDR = 0.017), which showed a significant negative correlation with monthly headache days. Moreover, seed-based connectivity (SBC) analysis using the right medial pulvinar of the thalamus as the seed point revealed significantly increased connectivity with the cerebellar vermis (p-FWE = 0.035) after ASD in individuals with MWoA, whereas connectivity with the right postcentral gyrus was significantly decreased (p-FWE = 0.048). Furthermore, we performed analyses of between-network connectivity (BNC) and within-network connectivity across 17 brain networks, utilizing the Yeo-17 atlas. Both MWoA individuals and HCs showed no significant changes in BNC after ASD compared to baseline. However, our analysis in within-network revealed that MWoA individuals exhibited a reduced within-network FC in dorsal attention network (DAN) after ASD compared to baseline (p-FDR = 0.031), whereas HCs showed no significant differences in within-network FC across all networks before and after ASD.
Conclusions: In comparison to HCs, MWoA individuals exhibited significant alterations in brain function after ASD, particularly within the thalamus, and MWoA individuals exhibited a reduced within-network FC in DAN after ASD compared to baseline. Brain regions and networks in MWoA individuals were more susceptible to the effects of ASD.
期刊介绍：
The Journal of Headache and Pain, a peer-reviewed open-access journal published under the BMC brand, a part of Springer Nature, is dedicated to researchers engaged in all facets of headache and related pain syndromes. It encompasses epidemiology, public health, basic science, translational medicine, clinical trials, and real-world data.
With a multidisciplinary approach, The Journal of Headache and Pain addresses headache medicine and related pain syndromes across all medical disciplines. It particularly encourages submissions in clinical, translational, and basic science fields, focusing on pain management, genetics, neurology, and internal medicine. The journal publishes research articles, reviews, letters to the Editor, as well as consensus articles and guidelines, aimed at promoting best practices in managing patients with headaches and related pain.
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