Increased spindle-related brain activation in right middle temporal gyrus during N2 than N3 among healthy sleepers: Initial discovery and independent sample replication

The association between spindle metrics and sleep architecture differs during N2 vs. N3 sleep, the underlying neural mechanism is not clearly illustrated. Here, we tested the discrepancy in spindle-related brain activation between N2 and N3 within healthy college students (dataset 1: n = 27, 59 % fe...

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Main Authors: Yan Shao, Yupeng Guo, Yun Chen, Guangyuan Zou, Jie Chen, Xuejiao Gao, Panpan Lu, Yujie Tong, Yuezhen Li, Ping Yao, Jiayi Liu, Shuqin Zhou, Jing Xu, Jia-Hong Gao, Qihong Zou, Hongqiang Sun
Format: Article
Language:English
Published: Elsevier 2025-01-01
Series:NeuroImage
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Online Access:http://www.sciencedirect.com/science/article/pii/S1053811924004737
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author Yan Shao
Yupeng Guo
Yun Chen
Guangyuan Zou
Jie Chen
Xuejiao Gao
Panpan Lu
Yujie Tong
Yuezhen Li
Ping Yao
Jiayi Liu
Shuqin Zhou
Jing Xu
Jia-Hong Gao
Qihong Zou
Hongqiang Sun
author_facet Yan Shao
Yupeng Guo
Yun Chen
Guangyuan Zou
Jie Chen
Xuejiao Gao
Panpan Lu
Yujie Tong
Yuezhen Li
Ping Yao
Jiayi Liu
Shuqin Zhou
Jing Xu
Jia-Hong Gao
Qihong Zou
Hongqiang Sun
author_sort Yan Shao
collection DOAJ
description The association between spindle metrics and sleep architecture differs during N2 vs. N3 sleep, the underlying neural mechanism is not clearly illustrated. Here, we tested the discrepancy in spindle-related brain activation between N2 and N3 within healthy college students (dataset 1: n = 27, 59 % females, median age 23 years), using simultaneous electroencephalography-functional magnetic resonance imaging (EEG-fMRI). To assess the replicability of the finding, we repeated the analysis among normal adults (independent dataset 2: n = 30, 50 % females, median age 32 years). The finding from dataset 1 indicated significantly increased blood-oxygen level-dependent signal in the right middle temporal gyrus during N2 compared with N3, which was well replicated in dataset 2. Furthermore, correlation analysis was performed to explore the association between this spindle-related brain activation and N2, N3 sleep duration during EEG-fMRI. We conducted the correlation analysis in N2 and N3, respectively. The negative association between spindle-related brain activation in the right middle temporal gyrus and sleep duration was only observed in N2. Our findings emphasize the unique role of spindle-related brain activation in the right middle temporal gyrus during N2 in shortening N2 sleep duration.
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spelling doaj-art-ed3c7036b4c9441ebd99a6ead0c4c0fe2025-01-11T06:38:33ZengElsevierNeuroImage1095-95722025-01-01305120976Increased spindle-related brain activation in right middle temporal gyrus during N2 than N3 among healthy sleepers: Initial discovery and independent sample replicationYan Shao0Yupeng Guo1Yun Chen2Guangyuan Zou3Jie Chen4Xuejiao Gao5Panpan Lu6Yujie Tong7Yuezhen Li8Ping Yao9Jiayi Liu10Shuqin Zhou11Jing Xu12Jia-Hong Gao13Qihong Zou14Hongqiang Sun15Peking University Sixth Hospital, Peking University Institute of Mental Health, NHC Key Laboratory of Mental Health (Peking University), National Clinical Research Center for Mental Disorders (Peking University Sixth Hospital), Peking University, Beijing, PR ChinaPeking University Sixth Hospital, Peking University Institute of Mental Health, NHC Key Laboratory of Mental Health (Peking University), National Clinical Research Center for Mental Disorders (Peking University Sixth Hospital), Peking University, Beijing, PR ChinaPeking University Sixth Hospital, Peking University Institute of Mental Health, NHC Key Laboratory of Mental Health (Peking University), National Clinical Research Center for Mental Disorders (Peking University Sixth Hospital), Peking University, Beijing, PR ChinaBeijing City Key Lab for Medical Physics and Engineering, Institute of Heavy Ion Physics, School of Physics, Peking University, Beijing, PR China; Center for MRI Research, Academy for Advanced Interdisciplinary Studies, Peking University, Beijing, PR ChinaPeking University Sixth Hospital, Peking University Institute of Mental Health, NHC Key Laboratory of Mental Health (Peking University), National Clinical Research Center for Mental Disorders (Peking University Sixth Hospital), Peking University, Beijing, PR ChinaPeking University Sixth Hospital, Peking University Institute of Mental Health, NHC Key Laboratory of Mental Health (Peking University), National Clinical Research Center for Mental Disorders (Peking University Sixth Hospital), Peking University, Beijing, PR ChinaPeking University Sixth Hospital, Peking University Institute of Mental Health, NHC Key Laboratory of Mental Health (Peking University), National Clinical Research Center for Mental Disorders (Peking University Sixth Hospital), Peking University, Beijing, PR ChinaPeking University Sixth Hospital, Peking University Institute of Mental Health, NHC Key Laboratory of Mental Health (Peking University), National Clinical Research Center for Mental Disorders (Peking University Sixth Hospital), Peking University, Beijing, PR ChinaPeking University Sixth Hospital, Peking University Institute of Mental Health, NHC Key Laboratory of Mental Health (Peking University), National Clinical Research Center for Mental Disorders (Peking University Sixth Hospital), Peking University, Beijing, PR China; Department of Neuropsychiatry, Behavioral Neurology and Sleep Center, Beijing Tian Tan Hospital, Capital Medical University, Beijing, PR ChinaMental Health Institute of Inner Mongolia Autonomous Region, The Third Hospital of Inner Mongolia Autonomous Region, Hohhot 010010, PR ChinaBeijing City Key Lab for Medical Physics and Engineering, Institute of Heavy Ion Physics, School of Physics, Peking University, Beijing, PR China; Center for MRI Research, Academy for Advanced Interdisciplinary Studies, Peking University, Beijing, PR ChinaBeijing City Key Lab for Medical Physics and Engineering, Institute of Heavy Ion Physics, School of Physics, Peking University, Beijing, PR ChinaBeijing City Key Lab for Medical Physics and Engineering, Institute of Heavy Ion Physics, School of Physics, Peking University, Beijing, PR China; Laboratory of Applied Brain and Cognitive Sciences, College of International Business, Shanghai International Studies University, Shanghai, PR ChinaBeijing City Key Lab for Medical Physics and Engineering, Institute of Heavy Ion Physics, School of Physics, Peking University, Beijing, PR China; Center for MRI Research, Academy for Advanced Interdisciplinary Studies, Peking University, Beijing, PR China; McGovern Institute for Brain Research, Peking University, Beijing, PR China; Correspondence authors at: Peking University Sixth Hospital, Peking University Institute of Mental Health, NHC Key Laboratory of Mental Health (Peking University), National Clinical Research Center for Mental Disorders (Peking University Sixth Hospital), Peking University, 51 Huayuan Bei Road, Haidian District, Beijing 100191, PR ChinaBeijing City Key Lab for Medical Physics and Engineering, Institute of Heavy Ion Physics, School of Physics, Peking University, Beijing, PR China; Center for MRI Research, Academy for Advanced Interdisciplinary Studies, Peking University, Beijing, PR China; Correspondence authors at: Peking University Sixth Hospital, Peking University Institute of Mental Health, NHC Key Laboratory of Mental Health (Peking University), National Clinical Research Center for Mental Disorders (Peking University Sixth Hospital), Peking University, 51 Huayuan Bei Road, Haidian District, Beijing 100191, PR ChinaPeking University Sixth Hospital, Peking University Institute of Mental Health, NHC Key Laboratory of Mental Health (Peking University), National Clinical Research Center for Mental Disorders (Peking University Sixth Hospital), Peking University, Beijing, PR China; Correspondence authors at: Peking University Sixth Hospital, Peking University Institute of Mental Health, NHC Key Laboratory of Mental Health (Peking University), National Clinical Research Center for Mental Disorders (Peking University Sixth Hospital), Peking University, 51 Huayuan Bei Road, Haidian District, Beijing 100191, PR ChinaThe association between spindle metrics and sleep architecture differs during N2 vs. N3 sleep, the underlying neural mechanism is not clearly illustrated. Here, we tested the discrepancy in spindle-related brain activation between N2 and N3 within healthy college students (dataset 1: n = 27, 59 % females, median age 23 years), using simultaneous electroencephalography-functional magnetic resonance imaging (EEG-fMRI). To assess the replicability of the finding, we repeated the analysis among normal adults (independent dataset 2: n = 30, 50 % females, median age 32 years). The finding from dataset 1 indicated significantly increased blood-oxygen level-dependent signal in the right middle temporal gyrus during N2 compared with N3, which was well replicated in dataset 2. Furthermore, correlation analysis was performed to explore the association between this spindle-related brain activation and N2, N3 sleep duration during EEG-fMRI. We conducted the correlation analysis in N2 and N3, respectively. The negative association between spindle-related brain activation in the right middle temporal gyrus and sleep duration was only observed in N2. Our findings emphasize the unique role of spindle-related brain activation in the right middle temporal gyrus during N2 in shortening N2 sleep duration.http://www.sciencedirect.com/science/article/pii/S1053811924004737Sleep spindlesBrain activationN2Sleep durationEEG-fMRI
spellingShingle Yan Shao
Yupeng Guo
Yun Chen
Guangyuan Zou
Jie Chen
Xuejiao Gao
Panpan Lu
Yujie Tong
Yuezhen Li
Ping Yao
Jiayi Liu
Shuqin Zhou
Jing Xu
Jia-Hong Gao
Qihong Zou
Hongqiang Sun
Increased spindle-related brain activation in right middle temporal gyrus during N2 than N3 among healthy sleepers: Initial discovery and independent sample replication
NeuroImage
Sleep spindles
Brain activation
N2
Sleep duration
EEG-fMRI
title Increased spindle-related brain activation in right middle temporal gyrus during N2 than N3 among healthy sleepers: Initial discovery and independent sample replication
title_full Increased spindle-related brain activation in right middle temporal gyrus during N2 than N3 among healthy sleepers: Initial discovery and independent sample replication
title_fullStr Increased spindle-related brain activation in right middle temporal gyrus during N2 than N3 among healthy sleepers: Initial discovery and independent sample replication
title_full_unstemmed Increased spindle-related brain activation in right middle temporal gyrus during N2 than N3 among healthy sleepers: Initial discovery and independent sample replication
title_short Increased spindle-related brain activation in right middle temporal gyrus during N2 than N3 among healthy sleepers: Initial discovery and independent sample replication
title_sort increased spindle related brain activation in right middle temporal gyrus during n2 than n3 among healthy sleepers initial discovery and independent sample replication
topic Sleep spindles
Brain activation
N2
Sleep duration
EEG-fMRI
url http://www.sciencedirect.com/science/article/pii/S1053811924004737
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