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      The restoration ability of a short nap after sleep deprivation on the brain cognitive function: A dynamic functional connectivity analysis

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          Abstract

          Aims

          The brain function impairment induced by sleep deprivation (SD) is temporary and can be fully reversed with sufficient sleep. However, in many cases, long‐duration recovery sleep is not feasible. Thus, this study aimed to investigate whether a short nap after SD is sufficient to restore brain function.

          Methods

          The data of 38 subjects, including resting state functional magnetic resonance imaging data collected at three timepoints (before SD, after 30 h of SD, and after a short nap following SD) and psychomotor vigilance task (PVT) data, were collected. Dynamic functional connectivity (DFC) analysis was used to evaluate changes in brain states among three timepoints, and four DFC states were distinguished across the three timepoints.

          Results

          Before SD, state 2 (a resting‐like FC matrix) was dominant (48.26%). However, after 30 h SD, the proportion of state 2 dramatically decreased, and state 3 (still resting‐like, but FCs were weakened) became dominant (40.92%). The increased proportion of state 3 positively correlated with a larger PVT “lapse” time. After a nap, the proportions of states 2 and 3 significantly increased and decreased, respectively, and the change in proportion of state 2 negatively correlated with the change in PVT “lapse” time.

          Conclusions

          Taken together, the results indicated that, after a nap, the cognitive function impairment caused by SD may be reversed to some extent. Additionally, DFC differed among timepoints, which was also associated with the extent of cognitive function impairment after SD (state 3) and the extent of recovery therefrom after a nap (state 2).

          Abstract

          Sleep deprivation (SD) will lead to temporary cognitive impairment, which can be reversed to some extent by a short nap following SD. Through dynamic functional connectivity analysis, the dominant stationary brain states that the brain trends to be in differ before and after SD. The relative proportions of these two stationary brain states affected the degree of cognitive impairment after SD and recovery after a nap, respectively.

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          Most cited references27

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          A self-assessment questionnaire to determine morningness-eveningness in human circadian rhythms.

          An English language self-assessment Morningness-Eveningness questionnaire is presented and evaluated against individual differences in the circadian vatiation of oral temperature. 48 subjects falling into Morning, Evening and Intermediate type categories regularly took their temperature. Circadian peak time were identified from the smoothed temperature curves of each subject. Results showed that Morning types and a significantly earlier peak time than Evening types and tended to have a higher daytime temperature and lower post peak temperature. The Intermediate type had temperatures between those of the other groups. Although no significant differences in sleep lengths were found between the three types, Morning types retired and arose significantly earlier than Evening types. Whilst these time significatly correlated with peak time, the questionnaire showed a higher peak time correlation. Although sleep habits are an important déterminant of peak time there are other contibutory factors, and these appear to be partly covered by the questionnaire. Although the questionnaire appears to be valid, further evaluation using a wider subject population is required.
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            Tracking whole-brain connectivity dynamics in the resting state.

            Spontaneous fluctuations are a hallmark of recordings of neural signals, emergent over time scales spanning milliseconds and tens of minutes. However, investigations of intrinsic brain organization based on resting-state functional magnetic resonance imaging have largely not taken into account the presence and potential of temporal variability, as most current approaches to examine functional connectivity (FC) implicitly assume that relationships are constant throughout the length of the recording. In this work, we describe an approach to assess whole-brain FC dynamics based on spatial independent component analysis, sliding time window correlation, and k-means clustering of windowed correlation matrices. The method is applied to resting-state data from a large sample (n = 405) of young adults. Our analysis of FC variability highlights particularly flexible connections between regions in lateral parietal and cingulate cortex, and argues against a labeling scheme where such regions are treated as separate and antagonistic entities. Additionally, clustering analysis reveals unanticipated FC states that in part diverge strongly from stationary connectivity patterns and challenge current descriptions of interactions between large-scale networks. Temporal trends in the occurrence of different FC states motivate theories regarding their functional roles and relationships with vigilance/arousal. Overall, we suggest that the study of time-varying aspects of FC can unveil flexibility in the functional coordination between different neural systems, and that the exploitation of these dynamics in further investigations may improve our understanding of behavioral shifts and adaptive processes.
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              Neurocognitive Consequences of Sleep Deprivation

              Sleep deprivation is associated with considerable social, financial, and health-related costs, in large measure because it produces impaired cognitive performance due to increasing sleep propensity and instability of waking neurobehavioral functions. Cognitive functions particularly affected by sleep loss include psychomotor and cognitive speed, vigilant and executive attention, working memory, and higher cognitive abilities. Chronic sleep-restriction experiments--which model the kind of sleep loss experienced by many individuals with sleep fragmentation and premature sleep curtailment due to disorders and lifestyle--demonstrate that cognitive deficits accumulate to severe levels over time without full awareness by the affected individual. Functional neuroimaging has revealed that frequent and progressively longer cognitive lapses, which are a hallmark of sleep deprivation, involve distributed changes in brain regions including frontal and parietal control areas, secondary sensory processing areas, and thalamic areas. There are robust differences among individuals in the degree of their cognitive vulnerability to sleep loss that may involve differences in prefrontal and parietal cortices, and that may have a basis in genes regulating sleep homeostasis and circadian rhythms. Thus, cognitive deficits believed to be a function of the severity of clinical sleep disturbance may be a product of genetic alleles associated with differential cognitive vulnerability to sleep loss. Thieme Medical Publishers.
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                Author and article information

                Contributors
                fangpeng@fmmu.edu.cn
                zhu_yq_fmmu@163.com
                Journal
                CNS Neurosci Ther
                CNS Neurosci Ther
                10.1111/(ISSN)1755-5949
                CNS
                CNS Neuroscience & Therapeutics
                John Wiley and Sons Inc. (Hoboken )
                1755-5930
                1755-5949
                22 August 2023
                February 2024
                : 30
                : 2 ( doiID: 10.1002/cns.v30.2 )
                : e14413
                Affiliations
                [ 1 ] Department of Radiology, Xijing Hospital Fourth Military Medical University Xi'an China
                [ 2 ] Department of Military Medical Psychology Fourth Military Medical University Xi'an China
                Author notes
                [*] [* ] Correspondence

                Yuanqiang Zhu, Department of Radiology, Xijing Hospital, Fourth Military Medical University, No. 127 Changle West Road, Xi'an 710032, China.

                Email: zhu_yq_fmmu@ 123456163.com

                Peng Fang, Department of Military Medical Psychology, Fourth Military Medical University, No. 169 Changle West Road, Xi'an 710032, China.

                Email: fangpeng@ 123456fmmu.edu.cn

                The first two authors contributed equally to this work.

                Author information
                https://orcid.org/0000-0002-8618-2209
                https://orcid.org/0000-0002-8448-7922
                Article
                CNS14413 CNSNT-2022-984.R1
                10.1111/cns.14413
                10848048
                37605612
                cfd43924-8093-4a96-a91c-4901f94a7fce
                © 2023 The Authors. CNS Neuroscience & Therapeutics published by John Wiley & Sons Ltd.

                This is an open access article under the terms of the http://creativecommons.org/licenses/by/4.0/ License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited.

                History
                : 07 April 2023
                : 15 November 2022
                : 05 August 2023
                Page count
                Figures: 7, Tables: 1, Pages: 9, Words: 5558
                Funding
                Funded by: Key R&D Program Projects of Shaanxi
                Award ID: 2021SF‐287
                Award ID: 2022JM‐575
                Funded by: Boost Program of Xijing Hospital
                Award ID: JSYXM28
                Award ID: JSYXZ08
                Award ID: XJZT21CM21
                Funded by: Military Medical Science and Technology Youth Training Program
                Award ID: 20QNPY049
                Funded by: National Natural Science Foundation of China , doi 10.13039/501100001809;
                Award ID: 81801772
                Award ID: 81902488
                Award ID: 82071917
                Funded by: Youth Talent Lifting Project of Shaanxi province
                Award ID: 20210304
                Categories
                Original Article
                Original Articles
                Custom metadata
                2.0
                February 2024
                Converter:WILEY_ML3GV2_TO_JATSPMC version:6.3.6 mode:remove_FC converted:07.02.2024

                Neurosciences
                dynamic functional connectivity,psychomotor vigilance task,resting state functional magnetic resonance imaging,short nap,sleep deprivation

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