Altered functional connectivity of thalamus subregions after sleep deprivation associated with impaired attention

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However, the FC between the thalamus subregions and cerebrum underlying attentional impairment after acute SD remains elusive. Here, we aimed to probe the relationship between the attentional function and the altered thalamocortical FC after acute SD. In this study, 25 healthy participants with regular sleep conducted attentional network test and received resting-state fMRI scan before and after 24 h of SD. Then, we analyzed the FC between the thalamus and cerebrum and relationships with attentional function in the enrolled subjects. Our results displayed that the participants showed the significantly lower alerting effect, higher executive effect, and a lower accuracy after acute SD. Compared to the RW state, we observed the decreased FCs between ‘somatosensory’ thalamic seed and left frontal pole, right frontal pole, left middle temporal gyrus (posterior division), and right middle temporal gyrus (posterior division). Furthermore, the reduced FC between the right middle temporal gyrus and ‘somatosensory’ thalamic seed was negatively associated with the change in orienting effect of the participants. Our findings reveal that the damaged thalamocortical FC after SD may contribute to the declined attention. Sleep deprivation Attention Thalamus Functional connectivity Imaging Figures Figure 1 Figure 2 Figure 3 Introduction Sleep deprivation (SD) is very common in society which is sleep duration less 4 hours in a typical 24-hour day (Hudson et al., 2020 ; Tobaldini et al., 2017 ). What’s more, SD is harmful to physical and mental health, including the increasing risk of cardiovascular disease, cancer, mood disorder, and cognitive impairments (Kecklund et al., 2016; Krause et al., 2017 ). Attention is an essential part of cognitive processing and acts as a “bind” and “guide” (Wolfe, 2021 ). Attention system can be divided into three subsystems: alerting, orienting and executive control, while different subsystems involve different brain regions (Petersen et al., 2012; Posner et al., 1990). Increasing evidence have indicated that SD diminishes not only attentional focus but also duration of sustained attention (Cai et al., 2021 ; Goel et al., 2009 ; Kong et al., 2012 ; Krause et al., 2017 ; Veksler et al., 2018). Functional magnetic resonance imaging (fMRI) is widely used to explore potential mechanism of attention impairment after acute SD. Functional connectivity (FC) can assess connections between different brain regions and reflect differences of network in different states (Duff et al., 2018 ). Numerous of neuroimaging researches have exhibited that aberrant FC in networks after SD, such as the dorsal and ventral attention network, default mode network, salience network, hippocampal network and some abnormalities are connected with clinic syndrome including decreased vigilance and negative emotion (W. H. Chen et al., 2018 ; Kaufmann et al., 2016 ; Long et al., 2019; Zhang et al., 2021 ; Zhang et al., 2019 ). Thalamus is regarded as a pathway of transforming sensory information to the cortex, involving in cognitive function, such as attention, memory, awareness (Cassel et al., 2021 ; Halassa et al., 2019; Perry et al., 2021 ; Saalmann et al., 2009). When sleep is restricted, the normal restorative function of nonrapid eye movement sleep is influenced, which is recognized as thalamic function, leading to cognition impairment (Brown et al., 2012 ; Jan et al., 2009 ). Prior studies have investigated that significant changes in thalamus were affected by SD (Jan et al., 2009 ; Liu et al., 2014 ; Vanrobaeys et al., 2023 ). Attention impairments after acute SD is correlated with decreased frontal-thalamus connectivity and increased frontal-visual connectivity and increased thalamus-parietal connectivity (Cai et al., 2021 ; Y. Chen et al., 2022 ). Limited by experimental paradigms or fMRI scans, the inner mechanism is still unclean. Therefore, all of these provide a possible opportunity to analyze interactions between thalamus and cerebrum and its relationship between attention function to investigate the neuroimaging mechanism of attention problems after SD. In this study, we hypothesized that the altered thalamocortical FC might be an underlying neurobiological feature of attention impairment after SD. To verify the hypothesis, thirty healthy subjects with regular sleep were enrolled to scan fMRI before and after 24 h SD. And the attention network task was applied to estimate attention function of the participants. Then, we probed the relationship between altered thalamocortical FC and reduced attention after acute SD. Methods Participants Thirty healthy subjects (16 males and 14 females) from the college, aged between 20 and 30 years (25.20 ± 2.20 years) and 18.10 ± 2.45 years education duration, were enrolled from November 2020 to August 2021. The enrolled subjects must meet the criteria as follows: (i) Pittsburgh Sleep Quality Index (PSQI) score < 5; (ii) regular sleep without excessive morning or evening types; (iii) right-handed; (ⅳ) no history of neurologic or psychiatric diseases; (ⅴ) no trauma stimuli; (ⅵ) no caffeine, smoking, alcohol or drug addictions; (ⅶ) no MRI contraindications. The Ethics Committee of Beijing Anding Hospital affiliated with Capital Medical University approved our study procedure (Number of clinical registration: ChiCTR2000039858). Before the study, the informed consent was signed by each enrolled individual. Study procedure Each enrolled participant visits our laboratory twice. They had to sign the informed consent while receiving a concise overview of this study. At the second visit, the participants had to get up at 7:00 am and returned to the laboratory before 8:00 am for 24 h SD. During the study, all recruited subjects should stay awake, not taking in tea, alcohol or coffee. To make sure each participant was awake, the researchers took turns monitoring. Our researchers would wake them up if they showed any indication of falling sleep. Each subject had to complete two MRI scans before and after 24 h SD, respectively. We conducted the 250 s T1 and 490 s resting-state scans during the first MRI scan, and the 490-s resting-state scan at the second MRI scan around 7:00 am the following day. We would remind all subjects staying awake during scanning, and exclude the subject which falls asleep during fMRI scan. Overall, the 26 of 30 participants completed the entire trail. Attentional network test The procedure of attentional network test (ANT) was used as described previously, which was programmed by E-prime software (Fan et al., 2005 ). A total of 336 trails was conducted in this task, including 24 trails in practice and 312 trails for testing. The details of each trial were displayed in Fig. 1 . The enrolled participants were required to identify the direction of an arrow (i.e. target) in the centre. Following the participants’ response, the target disappeared and a fixation period lasts for an unpredictable duration (400–1600 ms). There are three conditions when the target stimulus appears: congruent condition, neutral condition, and incongruent condition. Finally, we analyzed the variable of this task, containing alter effect, orienting effect, control conflict, reaction time, and accuracy. MRI acquisition The MRI scan was performed using a Siemens 3.0 Tesla Prisma at Beijing Anding Hospital in Beijing, China. During the MRI scan, subjects had to stay still, keep their eyes closed, and resist falling asleep. In addition, the participants needed to freeze their foam head supports to avoid head movement. A single-shot, gradient-recalled echo-planar imaging sequence was used for the resting-state fMRI data. The parameters were set in line with previously published studies (Feng et al., 2022 ). A rapid gradient-echo sequence with T1-weighted multi-echo magnetization preparation was used to acquire high-resolution structural images. Parcellation of thalamus and FC analysis Image processing was performed using DPABISurf developed by Yan et al (Li et al., 2021 ). A surface-based image preprocessing pipeline was used, as previously described (Yan et al., 2021 ). Similar to the procedure in previous studies (Behrens et al., 2003 ), the cerebral cortex comprised six bilateral cortical subregions, including the motor, somatosensory, prefrontal, parietal, temporal, and occipital cortex. These cortical subregions were defined by Harvard-Oxford probabilistic cortical atlas. The following seed-based resting-state FC analysis used the six thalamic subregions as seeds (regions of interest) using the DPABISurf toolbox. Firstly, the BOLD time series of thalamic seed and the whole cortical cortex were extracted. Then, we calculated the Pearson’s correlation coefficients between the time series of each thalamic seed and the whole cortical cortex. To improve normality, correlation coefficients were transformed to Fisher’s z-scores. Seed-to-voxel second-level analyses were performed using the paired-sample t test, and age and gender as covariates. Correlation analysis The correlation between FC change and attentional performance was also calculated. Gender, age, and head motion were included as covariates in the statistical analysis. The false discovery rate (FDR) was used to account for multiple comparisons (corrected to p < 0.05). Results Attention assessments A total of 25 participants completed the entire trail and were included in the final analysis (shown in Table 1 ). Compared to the RW state, the significant lower alerting effect (t = 2.357, p = 0.023) and higher executive effect (t = -2.174, p = 0.035) were found in the SD state. And we found that subjects showed a lower accuracy (t = 2.091, p = 0.042) after SD. There were no significant differences in orienting effect and reaction time between the RW and SD states. Table 1 Results of attentional network test (RW vs. SD) RW SD t value p value Alert effect 51.75 ± 21.5 36.54 ± 23.1 2.357 0.023 Orienting effect 52.63 ± 22.2 46.00 ± 22.1 1.038 0.305 Control conflict 99.17 ± 25.9 115.38 ± 25.7 -2.174 0.035 Reaction time (ms) 585.83 ± 66.0 601.79 ± 80.9 -0.749 0.458 Accuracy 97.63 ± 1.5 93.92 ± 8.6 2.091 0.042 RW, rested wakefulness; SD, sleep deprivation. Altered FC results after SD Compared to the RW state, we found the decreased FCs between ‘somatosensory’ thalamic seed and left frontal pole, right frontal pole, left middle temporal gyrus (posterior division), and right middle temporal gyrus (posterior division). The decreased FCs between ‘motor’ thalamic seed and left supramarginal gyrus (anterior division), right supramarginal gyrus (anterior division) were also found after SD. In addition, we found the decreased FC between left precuneus and ‘occipital’ thalamic seed after SD. The details were illustrated in Table 2 and Fig. 2 . Table 2 Altered FC between the cerebellum and cerebrum after SD T value p value Left frontal pole and ‘somatosensory’ thalamic seed 3.918 0.0005 Right frontal pole and ‘somatosensory’ thalamic seed 3.910 0.0005 Left middle temporal gyrus, posterior division and ‘somatosensory’ thalamic seed 4.415 0.0001 Right middle temporal gyrus, posterior division and ‘somatosensory’ thalamic seed 3.877 0.0006 Left supramarginal gyrus, anterior division and ‘motor’ thalamic seed 4.903 < 0.0001 Right supramarginal gyrus, anterior division and ‘motor’ thalamic seed 4.098 0.0003 Left precuneous cortex and ‘occipital’ thalamic seed 4.100 0.0003 FC, functional connectivity; SD, sleep deprivation. Correlation analysis We performed the correlation analysis between changes in ANT task and altered FC. We found that the change in orienting effect of ANT task was negatively correlated with the altered FC between the right middle temporal gyrus (posterior division) and ‘somatosensory’ thalamic seed (r = -0.406, p = 0.049, Fig. 3 ). Discussion To our knowledge, this is first study to explore the altered FC of thalamus subregions underlying impaired attention after SD. The decreased FCs between thalamus subregions and cerebral cortices were detected after acute SD. Importantly, we found the significant correlation between the change in attention performance and the altered FC, which indicated the neural mechanism underlying impaired attention after SD. The ANT is applied to evaluate the orientating, alerting and executive components of attention performance. In this study, we found the significant lower alerting effect and higher executive effect after SD, which indicated declines in alerting and executive functions. It had been confirmed that the attention performance was impaired after acute SD (Ning et al., 2022 ). In line with our study, our previous study on shift work disorder, a form of chronic SD, also showed lower alerting effect and higher executive effect compared with healthy controls (Ning et al., 2021 ). Several studies on SD revealed the same results with us (Heaton et al., 2014 ; Riontino et al., 2022). Nevertheless, in contrast to our result, one previous study on 47 participants also revealed decreased orientating effect after SD (Whitney et al., 2017 ). The inconsistent result could be due to the high inter-subject variability after SD (Banks et al., 2007). The relatively small sample size might be also the cause of no significant decrease on orienting effect after SD in our study. Moreover, our study also showed the lower accuracy after SD, which furtherly demonstrated attention declines after SD. The role of the thalamus in attention decline after acute SD has been well documented. One recent resting-state fMRI study revealed increased ALFF in the thalamus after 24h SD (Cai et al., 2021 ). Another study on acute SD indicated the increased effective connectivity from the thalamus to the nodes in the frontal–parietal attention network, which was significantly correlated with decreased lapses (Y. Chen et al., 2022 ).These findings demonstrate the important role of the thalamus in attentional maintenance after SD. Numerous studies had confirmed that the thalamus played a vital role in the sleep–wake pathway and involved in cognitive functions, such as attention, working memory(Gent et al., 2018 ; Krause et al., 2017 ). Our findings showed the altered FC in thalamus subregions involving ‘somatosensory’ thalamic seed, ‘motor’ thalamic seed and ‘occipital’ thalamic seed. The ‘somatosensory’ thalamic seed and motor’ thalamic seed selectively control the flow of sensory-motor information to the cerebral cortex during different states of the sleep-wake cycle and arousal, which are controlled through the actions of neurotransmitter systems in the cerebral cortex (McCormick et al., 1994). The ‘occipital’ thalamic seed locate in the medial and posterior group of thalamic nuclei, which is connected with the visual cortex and critical for attentional processes (Arend et al., 2015 ). In hence, we speculated that the ‘somatosensory’ thalamic seed, ‘motor’ thalamic seed and ‘occipital’ thalamic seed involved in attention deficits after SD. Our findings showed the altered FC between thalamus subregions and left frontal pole, right frontal pole, left middle temporal gyrus (posterior division), right middle temporal gyrus (posterior division), left supramarginal gyrus (anterior division), right supramarginal gyrus (anterior division), and left precuneus. It had been demonstrated that the alerting component involved the thalamic, frontal and parietal areas, the executive attention component involving anterior cingulate cortex and the lateral prefrontal cortex, and the orientating component involving the superior parietal lobe, temporo–parietal junctions and superior frontal cortex (Fan et al., 2005 ). Our results revealed the dysfunctional cerebral cortices underlying three components of attention performance declines after SD. In line with our results, one previous study revealed the decreased FC between the thalamus and right middle temporal gyrus, right superior frontal gyrus, the right medial frontal gyrus, bilateral middle temporal gyri and left superior frontal gyrus (Shao et al., 2013 ), which suggested that the thalamus had strong reciprocal connections with the cerebral cortex. Moreover, the altered FC between the right middle temporal gyrus and ‘somatosensory’ thalamic seed was negatively correlated with the change in orienting effect, which suggested the association between the thalamocortical FC and attention performance after SD. Overall, our findings revealed that the altered FC between thalamus subregions and cerebral cortices after SD was associated with impaired attention. However, there were several limitations to be noted. Firstly, only participants aged between 20 and 30 years were recruited in this study. our results could not be extrapolated to individuals in other age groups. Participants from a broader age range should be recruited in future. Secondly, the sample size was relatively small in our study, which might be the cause of no significant differences on orienting effect and reaction time after SD. Further studies with a larger sample size are needed in future. Conclusively, we found decreased FC between thalamus subregions and cerebral cortices after SD. Moreover, the altered FC between the right middle temporal gyrus and ‘somatosensory’ thalamic seed was negatively correlated with the change in orienting effect. These findings suggest disruptive changes of the thalamocortical FC after SD, which may lead to the decline of attention. Declarations Ethical approval All procedures followed were in accordance with the standards of the Ethics Committee of Beijing Anding Hospital affiliated with Capital Medical University. Informed consent was obtained from all participants for being included in this study. Funding This study was supported by Beijing Hospitals Authority Youth Program (Grant No. QML20201901), National Natural Science Foundation (Grant No. 81904120), Beijing Hospitals Authority’s Ascent Plan (Grant No. DFL20191901), and Beijing Hospitals Authority Clinical Medicine Development of Special Funding (Grant No. ZYLX202129). Conflict of interest All authors have no conflicts of interest in this study. Availability of data and materials Data are available upon reasonable request. Author Contribution Y.Z.N. and H.X.J. designed the experiment and acquired the fundings. S.T.F., Z.Y.W., S.S.Z., and L.R.D. programmed the experiment. L.R.D. and S.S.Z. acquired the data. Z.Y.W. and S.T.F. analyzed the data. S.T.F. and Z.Y.W. drafted the manuscript. All authors contributed to manuscript revision, read and approved the submitted version. References Arend, I., Henik, A., & Okon-Singer, H. (2015). Dissociating emotion and attention functions in the pulvinar nucleus of the thalamus. Neuropsychology, 29 (2), 191-196. https://doi.org/10.1037/neu0000139 Banks, S., & Dinges, D. F. (2007). Behavioral and physiological consequences of sleep restriction. J Clin Sleep Med, 3 (5), 519-528. Behrens, T. E., Johansen-Berg, H., Woolrich, M. W., Smith, S. M., Wheeler-Kingshott, C. A., Boulby, P. A., . . . Matthews, P. M. (2003). 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Front Neurosci, 13 , 134. https://doi.org/10.3389/fnins.2019.00134 Additional Declarations No competing interests reported. Cite Share Download PDF Status: Published Journal Publication published 30 Jun, 2024 Read the published version in Nature and Science of Sleep → Version 1 posted You are reading this latest preprint version Research Square lets you share your work early, gain feedback from the community, and start making changes to your manuscript prior to peer review in a journal. As a division of Research Square Company, we’re committed to making research communication faster, fairer, and more useful. We do this by developing innovative software and high quality services for the global research community. Our growing team is made up of researchers and industry professionals working together to solve the most critical problems facing scientific publishing. Also discoverable on Platform About Our Team In Review Editorial Policies Advisory Board Help Center Resources Author Services Accessibility API Access RSS feed Manage Cookie Preferences © Research Square 2026 | ISSN 2693-5015 (online) Privacy Policy Terms of Service Do Not Sell My Personal Information {"props":{"pageProps":{"initialData":{"identity":"rs-3865082","acceptedTermsAndConditions":true,"allowDirectSubmit":true,"archivedVersions":[],"articleType":"Research Article","associatedPublications":[],"authors":[{"id":267331627,"identity":"7aa3dee5-6a5d-4812-8644-abf71f38f4a2","order_by":0,"name":"Sitong Feng","email":"","orcid":"","institution":"Beijing Key Laboratory of Mental Disorders, National Clinical Research Center for Mental Disorders \u0026 National Center for Mental Disorders, Beijing Anding Hospital, Capital Medical University","correspondingAuthor":false,"prefix":"","firstName":"Sitong","middleName":"","lastName":"Feng","suffix":""},{"id":267331628,"identity":"0bd4396a-6850-465d-8c1f-0d2fc39ae61b","order_by":1,"name":"Ziyao Wu","email":"","orcid":"","institution":"Beijing Key Laboratory of Mental Disorders, National Clinical Research Center for Mental Disorders \u0026 National Center for Mental Disorders, Beijing Anding Hospital, Capital Medical University","correspondingAuthor":false,"prefix":"","firstName":"Ziyao","middleName":"","lastName":"Wu","suffix":""},{"id":267331629,"identity":"77ac6eb3-8cec-4851-9ae3-9c945931ef09","order_by":2,"name":"Sisi Zheng","email":"","orcid":"","institution":"Beijing Key Laboratory of Mental Disorders, National Clinical Research Center for Mental Disorders \u0026 National Center for Mental Disorders, Beijing Anding Hospital, Capital Medical University","correspondingAuthor":false,"prefix":"","firstName":"Sisi","middleName":"","lastName":"Zheng","suffix":""},{"id":267331630,"identity":"d79cccfa-7a1f-4f7d-a13f-f31cb2c96147","order_by":3,"name":"Linrui Dong","email":"","orcid":"","institution":"Beijing Key Laboratory of Mental Disorders, National Clinical Research Center for Mental Disorders \u0026 National Center for Mental Disorders, Beijing Anding Hospital, Capital Medical University","correspondingAuthor":false,"prefix":"","firstName":"Linrui","middleName":"","lastName":"Dong","suffix":""},{"id":267331631,"identity":"94f6ac3e-c410-493a-a583-14d66f202e26","order_by":4,"name":"Hongxiao Jia","email":"data:image/png;base64,iVBORw0KGgoAAAANSUhEUgAAAZAAAAAyAQMAAABI0h/eAAAABlBMVEX///8AAABVwtN+AAAACXBIWXMAAA7EAAAOxAGVKw4bAAAAx0lEQVRIiWNgGAWjYBACxhkMjAckKqA8HiK1MByQOEOKFgYJoBbGNlK0MM/uMThgOc9OXndGAuODt20M8uYEHTbnWMIByW3JhttuJDAbzm1jMNzZQEjLjOQDQC0HEsxuJLBJ87YxJBgcIKglseGA5BywFvbfRGoB2dIAsYWZSC1pCQckjgH9cuZhs+SccxKGGwhpMZyRY/hYosZO3ux48sEPb8ps5AnaYtgADGgJiIVAJoMEAfVAIA9S+4GwulEwCkbBKBjJAADTBkJLAap/hgAAAABJRU5ErkJggg==","orcid":"","institution":"Beijing Key Laboratory of Mental Disorders, National Clinical Research Center for Mental Disorders \u0026 National Center for Mental Disorders, Beijing Anding Hospital, Capital Medical University","correspondingAuthor":true,"prefix":"","firstName":"Hongxiao","middleName":"","lastName":"Jia","suffix":""},{"id":267331632,"identity":"7dfa3496-a732-4ec5-8188-c29afe0589d7","order_by":5,"name":"Yanzhe Ning","email":"","orcid":"","institution":"Beijing Key Laboratory of Mental Disorders, National Clinical Research Center for Mental Disorders \u0026 National Center for Mental Disorders, Beijing Anding Hospital, Capital Medical University","correspondingAuthor":false,"prefix":"","firstName":"Yanzhe","middleName":"","lastName":"Ning","suffix":""}],"badges":[],"createdAt":"2024-01-15 01:44:08","currentVersionCode":1,"declarations":"","doi":"10.21203/rs.3.rs-3865082/v1","doiUrl":"https://doi.org/10.21203/rs.3.rs-3865082/v1","draftVersion":[],"editorialEvents":[{"content":"https://doi.org/10.2147/NSS.S472323","type":"published","date":"2024-07-01T02:15:53+00:00"}],"editorialNote":"","failedWorkflow":false,"files":[{"id":49768917,"identity":"9df77b85-03f1-4ae4-8656-d570bdfb9f07","added_by":"auto","created_at":"2024-01-17 17:22:42","extension":"png","order_by":1,"title":"Figure 1","display":"","copyAsset":false,"role":"figure","size":57827,"visible":true,"origin":"","legend":"\u003cp\u003eA visual presentation of the attentional network test.\u003c/p\u003e","description":"","filename":"Fig.1.png","url":"https://assets-eu.researchsquare.com/files/rs-3865082/v1/f9015cdfa54e84d2bbe5af26.png"},{"id":49768918,"identity":"0af099a2-566a-4f4b-a7cc-176f4585eb80","added_by":"auto","created_at":"2024-01-17 17:22:43","extension":"png","order_by":2,"title":"Figure 2","display":"","copyAsset":false,"role":"figure","size":539217,"visible":true,"origin":"","legend":"\u003cp\u003eThe schematic diagram of the significantly changed functional connectivity between the thalamic subregions and cortical regions after SD. And the colors of functional connectivity between brain regions indicate the mean strength of functional connectivity referred to the color bar.\u003c/p\u003e","description":"","filename":"Fig.2.png","url":"https://assets-eu.researchsquare.com/files/rs-3865082/v1/7c27995012aed9b6d557ad6b.png"},{"id":49768919,"identity":"e24e82b7-9484-4d12-8a66-f5ea00210f06","added_by":"auto","created_at":"2024-01-17 17:22:43","extension":"png","order_by":3,"title":"Figure 3","display":"","copyAsset":false,"role":"figure","size":265948,"visible":true,"origin":"","legend":"\u003cp\u003eCorrelation between the changed orienting effect and the altered functional connectivity between the right middle temporal gyrus (posterior division) and ‘somatosensory’ thalamic seed. FC, functional connectivity.\u003c/p\u003e","description":"","filename":"Fig.3.png","url":"https://assets-eu.researchsquare.com/files/rs-3865082/v1/f3d7a3f634726b58a858c85e.png"},{"id":61271349,"identity":"fc2a4e35-ba09-41eb-9cb9-9d695b360577","added_by":"auto","created_at":"2024-07-29 02:16:02","extension":"pdf","order_by":0,"title":"","display":"","copyAsset":false,"role":"manuscript-pdf","size":1148148,"visible":true,"origin":"","legend":"","description":"","filename":"manuscript.pdf","url":"https://assets-eu.researchsquare.com/files/rs-3865082/v1/541e0e8e-9632-40e6-bd8d-580b118d4f00.pdf"}],"financialInterests":"No competing interests reported.","formattedTitle":"Altered functional connectivity of thalamus subregions after sleep deprivation associated with impaired attention","fulltext":[{"header":"Introduction","content":"\u003cp\u003eSleep deprivation (SD) is very common in society which is sleep duration less 4 hours in a typical 24-hour day (Hudson et al., \u003cspan citationid=\"CR16\" class=\"CitationRef\"\u003e2020\u003c/span\u003e; Tobaldini et al., \u003cspan citationid=\"CR34\" class=\"CitationRef\"\u003e2017\u003c/span\u003e). What\u0026rsquo;s more, SD is harmful to physical and mental health, including the increasing risk of cardiovascular disease, cancer, mood disorder, and cognitive impairments (Kecklund et al., 2016; Krause et al., \u003cspan citationid=\"CR21\" class=\"CitationRef\"\u003e2017\u003c/span\u003e). Attention is an essential part of cognitive processing and acts as a \u0026ldquo;bind\u0026rdquo; and \u0026ldquo;guide\u0026rdquo; (Wolfe, \u003cspan citationid=\"CR38\" class=\"CitationRef\"\u003e2021\u003c/span\u003e). Attention system can be divided into three subsystems: alerting, orienting and executive control, while different subsystems involve different brain regions (Petersen et al., 2012; Posner et al., 1990). Increasing evidence have indicated that SD diminishes not only attentional focus but also duration of sustained attention (Cai et al., \u003cspan citationid=\"CR5\" class=\"CitationRef\"\u003e2021\u003c/span\u003e; Goel et al., \u003cspan citationid=\"CR13\" class=\"CitationRef\"\u003e2009\u003c/span\u003e; Kong et al., \u003cspan citationid=\"CR20\" class=\"CitationRef\"\u003e2012\u003c/span\u003e; Krause et al., \u003cspan citationid=\"CR21\" class=\"CitationRef\"\u003e2017\u003c/span\u003e; Veksler et al., 2018). Functional magnetic resonance imaging (fMRI) is widely used to explore potential mechanism of attention impairment after acute SD. Functional connectivity (FC) can assess connections between different brain regions and reflect differences of network in different states (Duff et al., \u003cspan citationid=\"CR9\" class=\"CitationRef\"\u003e2018\u003c/span\u003e). Numerous of neuroimaging researches have exhibited that aberrant FC in networks after SD, such as the dorsal and ventral attention network, default mode network, salience network, hippocampal network and some abnormalities are connected with clinic syndrome including decreased vigilance and negative emotion (W. H. Chen et al., \u003cspan citationid=\"CR7\" class=\"CitationRef\"\u003e2018\u003c/span\u003e; Kaufmann et al., \u003cspan citationid=\"CR18\" class=\"CitationRef\"\u003e2016\u003c/span\u003e; Long et al., 2019; Zhang et al., \u003cspan citationid=\"CR40\" class=\"CitationRef\"\u003e2021\u003c/span\u003e; Zhang et al., \u003cspan citationid=\"CR41\" class=\"CitationRef\"\u003e2019\u003c/span\u003e).\u003c/p\u003e \u003cp\u003eThalamus is regarded as a pathway of transforming sensory information to the cortex, involving in cognitive function, such as attention, memory, awareness (Cassel et al., \u003cspan citationid=\"CR6\" class=\"CitationRef\"\u003e2021\u003c/span\u003e; Halassa et al., 2019; Perry et al., \u003cspan citationid=\"CR28\" class=\"CitationRef\"\u003e2021\u003c/span\u003e; Saalmann et al., 2009). When sleep is restricted, the normal restorative function of nonrapid eye movement sleep is influenced, which is recognized as thalamic function, leading to cognition impairment (Brown et al., \u003cspan citationid=\"CR4\" class=\"CitationRef\"\u003e2012\u003c/span\u003e; Jan et al., \u003cspan citationid=\"CR17\" class=\"CitationRef\"\u003e2009\u003c/span\u003e). Prior studies have investigated that significant changes in thalamus were affected by SD (Jan et al., \u003cspan citationid=\"CR17\" class=\"CitationRef\"\u003e2009\u003c/span\u003e; Liu et al., \u003cspan citationid=\"CR23\" class=\"CitationRef\"\u003e2014\u003c/span\u003e; Vanrobaeys et al., \u003cspan citationid=\"CR35\" class=\"CitationRef\"\u003e2023\u003c/span\u003e). Attention impairments after acute SD is correlated with decreased frontal-thalamus connectivity and increased frontal-visual connectivity and increased thalamus-parietal connectivity (Cai et al., \u003cspan citationid=\"CR5\" class=\"CitationRef\"\u003e2021\u003c/span\u003e; Y. Chen et al., \u003cspan citationid=\"CR8\" class=\"CitationRef\"\u003e2022\u003c/span\u003e). Limited by experimental paradigms or fMRI scans, the inner mechanism is still unclean. Therefore, all of these provide a possible opportunity to analyze interactions between thalamus and cerebrum and its relationship between attention function to investigate the neuroimaging mechanism of attention problems after SD.\u003c/p\u003e \u003cp\u003eIn this study, we hypothesized that the altered thalamocortical FC might be an underlying neurobiological feature of attention impairment after SD. To verify the hypothesis, thirty healthy subjects with regular sleep were enrolled to scan fMRI before and after 24 h SD. And the attention network task was applied to estimate attention function of the participants. Then, we probed the relationship between altered thalamocortical FC and reduced attention after acute SD.\u003c/p\u003e"},{"header":"Methods","content":"\u003cdiv id=\"Sec3\" class=\"Section2\"\u003e \u003ch2\u003eParticipants\u003c/h2\u003e \u003cp\u003eThirty healthy subjects (16 males and 14 females) from the college, aged between 20 and 30 years (25.20\u0026thinsp;\u0026plusmn;\u0026thinsp;2.20 years) and 18.10\u0026thinsp;\u0026plusmn;\u0026thinsp;2.45 years education duration, were enrolled from November 2020 to August 2021. The enrolled subjects must meet the criteria as follows: (i) Pittsburgh Sleep Quality Index (PSQI) score\u0026thinsp;\u0026lt;\u0026thinsp;5; (ii) regular sleep without excessive morning or evening types; (iii) right-handed; (ⅳ) no history of neurologic or psychiatric diseases; (ⅴ) no trauma stimuli; (ⅵ) no caffeine, smoking, alcohol or drug addictions; (ⅶ) no MRI contraindications. The Ethics Committee of Beijing Anding Hospital affiliated with Capital Medical University approved our study procedure (Number of clinical registration: ChiCTR2000039858). Before the study, the informed consent was signed by each enrolled individual.\u003c/p\u003e \u003c/div\u003e \u003cdiv id=\"Sec4\" class=\"Section2\"\u003e \u003ch2\u003eStudy procedure\u003c/h2\u003e \u003cp\u003eEach enrolled participant visits our laboratory twice. They had to sign the informed consent while receiving a concise overview of this study. At the second visit, the participants had to get up at 7:00 am and returned to the laboratory before 8:00 am for 24 h SD. During the study, all recruited subjects should stay awake, not taking in tea, alcohol or coffee. To make sure each participant was awake, the researchers took turns monitoring. Our researchers would wake them up if they showed any indication of falling sleep. Each subject had to complete two MRI scans before and after 24 h SD, respectively. We conducted the 250 s T1 and 490 s resting-state scans during the first MRI scan, and the 490-s resting-state scan at the second MRI scan around 7:00 am the following day. We would remind all subjects staying awake during scanning, and exclude the subject which falls asleep during fMRI scan. Overall, the 26 of 30 participants completed the entire trail.\u003c/p\u003e \u003c/div\u003e \u003cdiv id=\"Sec5\" class=\"Section2\"\u003e \u003ch2\u003eAttentional network test\u003c/h2\u003e \u003cp\u003eThe procedure of attentional network test (ANT) was used as described previously, which was programmed by E-prime software (Fan et al., \u003cspan citationid=\"CR10\" class=\"CitationRef\"\u003e2005\u003c/span\u003e). A total of 336 trails was conducted in this task, including 24 trails in practice and 312 trails for testing. The details of each trial were displayed in Fig.\u0026nbsp;\u003cspan refid=\"Fig1\" class=\"InternalRef\"\u003e1\u003c/span\u003e. The enrolled participants were required to identify the direction of an arrow (i.e. target) in the centre. Following the participants\u0026rsquo; response, the target disappeared and a fixation period lasts for an unpredictable duration (400\u0026ndash;1600 ms). There are three conditions when the target stimulus appears: congruent condition, neutral condition, and incongruent condition. Finally, we analyzed the variable of this task, containing alter effect, orienting effect, control conflict, reaction time, and accuracy.\u003c/p\u003e \u003cp\u003e \u003c/p\u003e \u003c/div\u003e \u003cdiv id=\"Sec6\" class=\"Section2\"\u003e \u003ch2\u003eMRI acquisition\u003c/h2\u003e \u003cp\u003eThe MRI scan was performed using a Siemens 3.0 Tesla Prisma at Beijing Anding Hospital in Beijing, China. During the MRI scan, subjects had to stay still, keep their eyes closed, and resist falling asleep. In addition, the participants needed to freeze their foam head supports to avoid head movement. A single-shot, gradient-recalled echo-planar imaging sequence was used for the resting-state fMRI data. The parameters were set in line with previously published studies (Feng et al., \u003cspan citationid=\"CR11\" class=\"CitationRef\"\u003e2022\u003c/span\u003e). A rapid gradient-echo sequence with T1-weighted multi-echo magnetization preparation was used to acquire high-resolution structural images.\u003c/p\u003e \u003c/div\u003e \u003cdiv id=\"Sec7\" class=\"Section2\"\u003e \u003ch2\u003eParcellation of thalamus and FC analysis\u003c/h2\u003e \u003cp\u003eImage processing was performed using DPABISurf developed by Yan et al (Li et al., \u003cspan citationid=\"CR22\" class=\"CitationRef\"\u003e2021\u003c/span\u003e). A surface-based image preprocessing pipeline was used, as previously described (Yan et al., \u003cspan citationid=\"CR39\" class=\"CitationRef\"\u003e2021\u003c/span\u003e). Similar to the procedure in previous studies (Behrens et al., \u003cspan citationid=\"CR3\" class=\"CitationRef\"\u003e2003\u003c/span\u003e), the cerebral cortex comprised six bilateral cortical subregions, including the motor, somatosensory, prefrontal, parietal, temporal, and occipital cortex. These cortical subregions were defined by Harvard-Oxford probabilistic cortical atlas. The following seed-based resting-state FC analysis used the six thalamic subregions as seeds (regions of interest) using the DPABISurf toolbox. Firstly, the BOLD time series of thalamic seed and the whole cortical cortex were extracted. Then, we calculated the Pearson\u0026rsquo;s correlation coefficients between the time series of each thalamic seed and the whole cortical cortex. To improve normality, correlation coefficients were transformed to Fisher\u0026rsquo;s z-scores. Seed-to-voxel second-level analyses were performed using the paired-sample t test, and age and gender as covariates.\u003c/p\u003e \u003c/div\u003e \u003cdiv id=\"Sec8\" class=\"Section2\"\u003e \u003ch2\u003eCorrelation analysis\u003c/h2\u003e \u003cp\u003eThe correlation between FC change and attentional performance was also calculated. Gender, age, and head motion were included as covariates in the statistical analysis. The false discovery rate (FDR) was used to account for multiple comparisons (corrected to \u003cem\u003ep\u003c/em\u003e\u0026thinsp;\u0026lt;\u0026thinsp;0.05).\u003c/p\u003e \u003c/div\u003e"},{"header":"Results","content":"\u003cdiv id=\"Sec10\" class=\"Section2\"\u003e\n \u003ch2\u003eAttention assessments\u003c/h2\u003e\n \u003cp\u003eA total of 25 participants completed the entire trail and were included in the final analysis (shown in Table\u0026nbsp;\u003cspan class=\"InternalRef\"\u003e1\u003c/span\u003e). Compared to the RW state, the significant lower alerting effect (t\u0026thinsp;=\u0026thinsp;2.357, \u003cem\u003ep\u003c/em\u003e\u0026thinsp;=\u0026thinsp;0.023) and higher executive effect (t = -2.174, \u003cem\u003ep\u003c/em\u003e\u0026thinsp;=\u0026thinsp;0.035) were found in the SD state. And we found that subjects showed a lower accuracy (t\u0026thinsp;=\u0026thinsp;2.091, \u003cem\u003ep\u003c/em\u003e\u0026thinsp;=\u0026thinsp;0.042) after SD. There were no significant differences in orienting effect and reaction time between the RW and SD states.\u003c/p\u003e\n \u003cdiv class=\"gridtable\"\u003e\n \u003ctable id=\"Tab1\" border=\"1\"\u003e\n \u003ccaption\u003e\n \u003cdiv class=\"CaptionNumber\"\u003eTable 1\u003c/div\u003e\n \u003cdiv class=\"CaptionContent\"\u003e\n \u003cp\u003eResults of attentional network test (RW vs. SD)\u003c/p\u003e\n \u003c/div\u003e\n \u003c/caption\u003e\n \u003cthead\u003e\n \u003ctr\u003e\n \u003cth align=\"left\"\u003e\u0026nbsp;\u003c/th\u003e\n \u003cth align=\"left\"\u003e\n \u003cp\u003eRW\u003c/p\u003e\n \u003c/th\u003e\n \u003cth align=\"left\"\u003e\n \u003cp\u003eSD\u003c/p\u003e\n \u003c/th\u003e\n \u003cth align=\"left\"\u003e\n \u003cp\u003et value\u003c/p\u003e\n \u003c/th\u003e\n \u003cth align=\"left\"\u003e\n \u003cp\u003e\u003cem\u003ep\u003c/em\u003e value\u003c/p\u003e\n \u003c/th\u003e\n \u003c/tr\u003e\n \u003c/thead\u003e\n \u003ctbody\u003e\n \u003ctr\u003e\n \u003ctd align=\"left\"\u003e\n \u003cp\u003eAlert effect\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd align=\"char\"\u003e\n \u003cp\u003e51.75\u0026thinsp;\u0026plusmn;\u0026thinsp;21.5\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd align=\"char\"\u003e\n \u003cp\u003e36.54\u0026thinsp;\u0026plusmn;\u0026thinsp;23.1\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd align=\"char\"\u003e\n \u003cp\u003e2.357\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd align=\"char\"\u003e\n \u003cp\u003e0.023\u003c/p\u003e\n \u003c/td\u003e\n \u003c/tr\u003e\n \u003ctr\u003e\n \u003ctd align=\"left\"\u003e\n \u003cp\u003eOrienting effect\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd align=\"char\"\u003e\n \u003cp\u003e52.63\u0026thinsp;\u0026plusmn;\u0026thinsp;22.2\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd align=\"char\"\u003e\n \u003cp\u003e46.00\u0026thinsp;\u0026plusmn;\u0026thinsp;22.1\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd align=\"char\"\u003e\n \u003cp\u003e1.038\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd align=\"char\"\u003e\n \u003cp\u003e0.305\u003c/p\u003e\n \u003c/td\u003e\n \u003c/tr\u003e\n \u003ctr\u003e\n \u003ctd align=\"left\"\u003e\n \u003cp\u003eControl conflict\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd align=\"char\"\u003e\n \u003cp\u003e99.17\u0026thinsp;\u0026plusmn;\u0026thinsp;25.9\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd align=\"char\"\u003e\n \u003cp\u003e115.38\u0026thinsp;\u0026plusmn;\u0026thinsp;25.7\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd align=\"char\"\u003e\n \u003cp\u003e-2.174\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd align=\"char\"\u003e\n \u003cp\u003e0.035\u003c/p\u003e\n \u003c/td\u003e\n \u003c/tr\u003e\n \u003ctr\u003e\n \u003ctd align=\"left\"\u003e\n \u003cp\u003eReaction time (ms)\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd align=\"char\"\u003e\n \u003cp\u003e585.83\u0026thinsp;\u0026plusmn;\u0026thinsp;66.0\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd align=\"char\"\u003e\n \u003cp\u003e601.79\u0026thinsp;\u0026plusmn;\u0026thinsp;80.9\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd align=\"char\"\u003e\n \u003cp\u003e-0.749\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd align=\"char\"\u003e\n \u003cp\u003e0.458\u003c/p\u003e\n \u003c/td\u003e\n \u003c/tr\u003e\n \u003ctr\u003e\n \u003ctd align=\"left\"\u003e\n \u003cp\u003eAccuracy\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd align=\"char\"\u003e\n \u003cp\u003e97.63\u0026thinsp;\u0026plusmn;\u0026thinsp;1.5\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd align=\"char\"\u003e\n \u003cp\u003e93.92\u0026thinsp;\u0026plusmn;\u0026thinsp;8.6\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd align=\"char\"\u003e\n \u003cp\u003e2.091\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd align=\"char\"\u003e\n \u003cp\u003e0.042\u003c/p\u003e\n \u003c/td\u003e\n \u003c/tr\u003e\n \u003c/tbody\u003e\n \u003ctfoot\u003e\n \u003ctr\u003e\n \u003ctd colspan=\"5\"\u003eRW, rested wakefulness; SD, sleep deprivation.\u003c/td\u003e\n \u003c/tr\u003e\n \u003c/tfoot\u003e\n \u003c/table\u003e\n \u003c/div\u003e\n\u003c/div\u003e\n\u003cdiv id=\"Sec11\" class=\"Section2\"\u003e\n \u003ch2\u003eAltered FC results after SD\u003c/h2\u003e\n \u003cp\u003eCompared to the RW state, we found the decreased FCs between \u0026lsquo;somatosensory\u0026rsquo; thalamic seed and left frontal pole, right frontal pole, left middle temporal gyrus (posterior division), and right middle temporal gyrus (posterior division). The decreased FCs between \u0026lsquo;motor\u0026rsquo; thalamic seed and left supramarginal gyrus (anterior division), right supramarginal gyrus (anterior division) were also found after SD. In addition, we found the decreased FC between left precuneus and \u0026lsquo;occipital\u0026rsquo; thalamic seed after SD. The details were illustrated in Table\u0026nbsp;\u003cspan class=\"InternalRef\"\u003e2\u003c/span\u003e and Fig.\u0026nbsp;\u003cspan class=\"InternalRef\"\u003e2\u003c/span\u003e.\u003c/p\u003e\n \u003cdiv class=\"gridtable\"\u003e\n \u003ctable id=\"Tab2\" border=\"1\"\u003e\n \u003ccaption\u003e\n \u003cdiv class=\"CaptionNumber\"\u003eTable 2\u003c/div\u003e\n \u003cdiv class=\"CaptionContent\"\u003e\n \u003cp\u003eAltered FC between the cerebellum and cerebrum after SD\u003c/p\u003e\n \u003c/div\u003e\n \u003c/caption\u003e\n \u003cthead\u003e\n \u003ctr\u003e\n \u003cth align=\"left\"\u003e\u0026nbsp;\u003c/th\u003e\n \u003cth align=\"left\"\u003e\n \u003cp\u003eT value\u003c/p\u003e\n \u003c/th\u003e\n \u003cth align=\"left\"\u003e\n \u003cp\u003e\u003cem\u003ep\u003c/em\u003e value\u003c/p\u003e\n \u003c/th\u003e\n \u003c/tr\u003e\n \u003c/thead\u003e\n \u003ctbody\u003e\n \u003ctr\u003e\n \u003ctd align=\"left\"\u003e\n \u003cp\u003eLeft frontal pole and \u0026lsquo;somatosensory\u0026rsquo; thalamic seed\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd align=\"char\"\u003e\n \u003cp\u003e3.918\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd align=\"char\"\u003e\n \u003cp\u003e0.0005\u003c/p\u003e\n \u003c/td\u003e\n \u003c/tr\u003e\n \u003ctr\u003e\n \u003ctd align=\"left\"\u003e\n \u003cp\u003eRight frontal pole and \u0026lsquo;somatosensory\u0026rsquo; thalamic seed\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd align=\"char\"\u003e\n \u003cp\u003e3.910\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd align=\"char\"\u003e\n \u003cp\u003e0.0005\u003c/p\u003e\n \u003c/td\u003e\n \u003c/tr\u003e\n \u003ctr\u003e\n \u003ctd align=\"left\"\u003e\n \u003cp\u003eLeft middle temporal gyrus, posterior division and \u0026lsquo;somatosensory\u0026rsquo; thalamic seed\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd align=\"char\"\u003e\n \u003cp\u003e4.415\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd align=\"char\"\u003e\n \u003cp\u003e0.0001\u003c/p\u003e\n \u003c/td\u003e\n \u003c/tr\u003e\n \u003ctr\u003e\n \u003ctd align=\"left\"\u003e\n \u003cp\u003eRight middle temporal gyrus, posterior division and \u0026lsquo;somatosensory\u0026rsquo; thalamic seed\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd align=\"char\"\u003e\n \u003cp\u003e3.877\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd align=\"char\"\u003e\n \u003cp\u003e0.0006\u003c/p\u003e\n \u003c/td\u003e\n \u003c/tr\u003e\n \u003ctr\u003e\n \u003ctd align=\"left\"\u003e\n \u003cp\u003eLeft supramarginal gyrus, anterior division and \u0026lsquo;motor\u0026rsquo; thalamic seed\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd align=\"char\"\u003e\n \u003cp\u003e4.903\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd align=\"char\"\u003e\n \u003cp\u003e\u0026lt;\u0026thinsp;0.0001\u003c/p\u003e\n \u003c/td\u003e\n \u003c/tr\u003e\n \u003ctr\u003e\n \u003ctd align=\"left\"\u003e\n \u003cp\u003eRight supramarginal gyrus, anterior division and \u0026lsquo;motor\u0026rsquo; thalamic seed\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd align=\"char\"\u003e\n \u003cp\u003e4.098\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd align=\"char\"\u003e\n \u003cp\u003e0.0003\u003c/p\u003e\n \u003c/td\u003e\n \u003c/tr\u003e\n \u003ctr\u003e\n \u003ctd align=\"left\"\u003e\n \u003cp\u003eLeft precuneous cortex and \u0026lsquo;occipital\u0026rsquo; thalamic seed\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd align=\"char\"\u003e\n \u003cp\u003e4.100\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd align=\"char\"\u003e\n \u003cp\u003e0.0003\u003c/p\u003e\n \u003c/td\u003e\n \u003c/tr\u003e\n \u003c/tbody\u003e\n \u003ctfoot\u003e\n \u003ctr\u003e\n \u003ctd colspan=\"3\"\u003eFC, functional connectivity; SD, sleep deprivation.\u003c/td\u003e\n \u003c/tr\u003e\n \u003c/tfoot\u003e\n \u003c/table\u003e\n \u003c/div\u003e\n\u003c/div\u003e\n\u003cdiv id=\"Sec12\" class=\"Section2\"\u003e\n \u003ch2\u003eCorrelation analysis\u003c/h2\u003e\n \u003cp\u003eWe performed the correlation analysis between changes in ANT task and altered FC. We found that the change in orienting effect of ANT task was negatively correlated with the altered FC between the right middle temporal gyrus (posterior division) and \u0026lsquo;somatosensory\u0026rsquo; thalamic seed (r = -0.406, \u003cem\u003ep\u003c/em\u003e\u0026thinsp;=\u0026thinsp;0.049, Fig. \u003cspan class=\"InternalRef\"\u003e3\u003c/span\u003e).\u003c/p\u003e\n\u003c/div\u003e"},{"header":"Discussion","content":"\u003cp\u003eTo our knowledge, this is first study to explore the altered FC of thalamus subregions underlying impaired attention after SD. The decreased FCs between thalamus subregions and cerebral cortices were detected after acute SD. Importantly, we found the significant correlation between the change in attention performance and the altered FC, which indicated the neural mechanism underlying impaired attention after SD.\u003c/p\u003e\n\u003cp\u003eThe ANT is applied to evaluate the orientating, alerting and executive components of attention performance. In this study, we found the significant lower alerting effect and higher executive effect after SD, which indicated declines in alerting and executive functions. It had been confirmed that the attention performance was impaired after acute SD (Ning et al., \u003cspan class=\"CitationRef\"\u003e2022\u003c/span\u003e). In line with our study, our previous study on shift work disorder, a form of chronic SD, also showed lower alerting effect and higher executive effect compared with healthy controls (Ning et al., \u003cspan class=\"CitationRef\"\u003e2021\u003c/span\u003e). Several studies on SD revealed the same results with us (Heaton et al., \u003cspan class=\"CitationRef\"\u003e2014\u003c/span\u003e; Riontino et al., 2022). Nevertheless, in contrast to our result, one previous study on 47 participants also revealed decreased orientating effect after SD (Whitney et al., \u003cspan class=\"CitationRef\"\u003e2017\u003c/span\u003e). The inconsistent result could be due to the high inter-subject variability after SD (Banks et al., 2007). The relatively small sample size might be also the cause of no significant decrease on orienting effect after SD in our study. Moreover, our study also showed the lower accuracy after SD, which furtherly demonstrated attention declines after SD.\u003c/p\u003e\n\u003cp\u003eThe role of the thalamus in attention decline after acute SD has been well documented. One recent resting-state fMRI study revealed increased ALFF in the thalamus after 24h SD (Cai et al., \u003cspan class=\"CitationRef\"\u003e2021\u003c/span\u003e). Another study on acute SD indicated the increased effective connectivity from the thalamus to the nodes in the frontal\u0026ndash;parietal attention network, which was significantly correlated with decreased lapses (Y. Chen et al., \u003cspan class=\"CitationRef\"\u003e2022\u003c/span\u003e).These findings demonstrate the important role of the thalamus in attentional maintenance after SD. Numerous studies had confirmed that the thalamus played a vital role in the sleep\u0026ndash;wake pathway and involved in cognitive functions, such as attention, working memory(Gent et al., \u003cspan class=\"CitationRef\"\u003e2018\u003c/span\u003e; Krause et al., \u003cspan class=\"CitationRef\"\u003e2017\u003c/span\u003e). Our findings showed the altered FC in thalamus subregions involving \u0026lsquo;somatosensory\u0026rsquo; thalamic seed, \u0026lsquo;motor\u0026rsquo; thalamic seed and \u0026lsquo;occipital\u0026rsquo; thalamic seed. The \u0026lsquo;somatosensory\u0026rsquo; thalamic seed and motor\u0026rsquo; thalamic seed selectively control the flow of sensory-motor information to the cerebral cortex during different states of the sleep-wake cycle and arousal, which are controlled through the actions of neurotransmitter systems in the cerebral cortex (McCormick et al., 1994). The \u0026lsquo;occipital\u0026rsquo; thalamic seed locate in the medial and posterior group of thalamic nuclei, which is connected with the visual cortex and critical for attentional processes (Arend et al., \u003cspan class=\"CitationRef\"\u003e2015\u003c/span\u003e). In hence, we speculated that the \u0026lsquo;somatosensory\u0026rsquo; thalamic seed, \u0026lsquo;motor\u0026rsquo; thalamic seed and \u0026lsquo;occipital\u0026rsquo; thalamic seed involved in attention deficits after SD.\u003c/p\u003e\n\u003cp\u003eOur findings showed the altered FC between thalamus subregions and left frontal pole, right frontal pole, left middle temporal gyrus (posterior division), right middle temporal gyrus (posterior division), left supramarginal gyrus (anterior division), right supramarginal gyrus (anterior division), and left precuneus. It had been demonstrated that the alerting component involved the thalamic, frontal and parietal areas, the executive attention component involving anterior cingulate cortex and the lateral prefrontal cortex, and the orientating component involving the superior parietal lobe, temporo\u0026ndash;parietal junctions and superior frontal cortex (Fan et al., \u003cspan class=\"CitationRef\"\u003e2005\u003c/span\u003e). Our results revealed the dysfunctional cerebral cortices underlying three components of attention performance declines after SD. In line with our results, one previous study revealed the decreased FC between the thalamus and right middle temporal gyrus, right superior frontal gyrus, the right medial frontal gyrus, bilateral middle temporal gyri and left superior frontal gyrus (Shao et al., \u003cspan class=\"CitationRef\"\u003e2013\u003c/span\u003e), which suggested that the thalamus had strong reciprocal connections with the cerebral cortex. Moreover, the altered FC between the right middle temporal gyrus and \u0026lsquo;somatosensory\u0026rsquo; thalamic seed was negatively correlated with the change in orienting effect, which suggested the association between the thalamocortical FC and attention performance after SD. Overall, our findings revealed that the altered FC between thalamus subregions and cerebral cortices after SD was associated with impaired attention.\u003c/p\u003e\n\u003cp\u003eHowever, there were several limitations to be noted. Firstly, only participants aged between 20 and 30 years were recruited in this study. our results could not be extrapolated to individuals in other age groups. Participants from a broader age range should be recruited in future. Secondly, the sample size was relatively small in our study, which might be the cause of no significant differences on orienting effect and reaction time after SD. Further studies with a larger sample size are needed in future.\u003c/p\u003e\n\u003cp\u003eConclusively, we found decreased FC between thalamus subregions and cerebral cortices after SD. Moreover, the altered FC between the right middle temporal gyrus and \u0026lsquo;somatosensory\u0026rsquo; thalamic seed was negatively correlated with the change in orienting effect. These findings suggest disruptive changes of the thalamocortical FC after SD, which may lead to the decline of attention.\u003c/p\u003e"},{"header":"Declarations","content":"\u003ch2\u003eEthical approval\u003c/h2\u003e\n\u003cp\u003eAll procedures followed were in accordance with the standards of the Ethics Committee of Beijing Anding Hospital affiliated with Capital Medical University. Informed consent was obtained from all participants for being included in this study.\u003c/p\u003e\n\u003ch2\u003eFunding\u003c/h2\u003e\n\u003cp\u003eThis study was supported by Beijing Hospitals Authority Youth Program (Grant No. QML20201901), National Natural Science Foundation (Grant No. 81904120), Beijing Hospitals Authority\u0026rsquo;s Ascent Plan (Grant No. DFL20191901), and Beijing Hospitals Authority Clinical Medicine Development of Special Funding (Grant No. ZYLX202129).\u003c/p\u003e\n\u003ch2\u003eConflict of interest\u003c/h2\u003e\n\u003cp\u003eAll authors have no conflicts of interest in this study.\u003c/p\u003e\n\u003ch2\u003eAvailability of data and materials\u003c/h2\u003e\n\u003cp\u003eData are available upon reasonable request.\u003c/p\u003e\n\u003ch2\u003eAuthor Contribution\u003c/h2\u003e\n\u003cp\u003eY.Z.N. and H.X.J. designed the experiment and acquired the fundings. S.T.F., Z.Y.W., S.S.Z., and L.R.D. programmed the experiment. L.R.D. and S.S.Z. acquired the data. Z.Y.W. and S.T.F. analyzed the data. S.T.F. and Z.Y.W. drafted the manuscript. All authors contributed to manuscript revision, read and approved the submitted version.\u003c/p\u003e"},{"header":"References","content":"\u003col\u003e\n\u003cli\u003eArend, I., Henik, A., \u0026amp; Okon-Singer, H. (2015). Dissociating emotion and attention functions in the pulvinar nucleus of the thalamus. \u003cem\u003eNeuropsychology, 29\u003c/em\u003e(2), 191-196. https://doi.org/10.1037/neu0000139\u003c/li\u003e\n\u003cli\u003eBanks, S., \u0026amp; Dinges, D. F. (2007). Behavioral and physiological consequences of sleep restriction. \u003cem\u003eJ Clin Sleep Med, 3\u003c/em\u003e(5), 519-528. \u003c/li\u003e\n\u003cli\u003eBehrens, T. E., Johansen-Berg, H., Woolrich, M. W., Smith, S. M., Wheeler-Kingshott, C. A., Boulby, P. A., . . . Matthews, P. M. (2003). 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Alterations in Cerebellar Functional Connectivity Are Correlated With Decreased Psychomotor Vigilance Following Total Sleep Deprivation. \u003cem\u003eFront Neurosci, 13\u003c/em\u003e, 134. https://doi.org/10.3389/fnins.2019.00134\u003c/li\u003e\n\u003c/ol\u003e"}],"fulltextSource":"","fullText":"","funders":[],"hasAdminPriorityOnWorkflow":false,"hasManuscriptDocX":true,"hasOptedInToPreprint":true,"hasPassedJournalQc":"","hasAnyPriority":false,"hideJournal":false,"highlight":"","institution":"","isAcceptedByJournal":true,"isAuthorSuppliedPdf":false,"isDeskRejected":"","isHiddenFromSearch":false,"isInQc":false,"isInWorkflow":false,"isPdf":false,"isPdfUpToDate":true,"isWithdrawnOrRetracted":false,"journal":{"display":true,"email":"[email protected]","identity":"researchsquare","isNatureJournal":false,"hasQc":true,"allowDirectSubmit":true,"externalIdentity":"","sideBox":"","snPcode":"","submissionUrl":"/submission","title":"Research Square","twitterHandle":"researchsquare","acdcEnabled":true,"dfaEnabled":false,"editorialSystem":"","reportingPortfolio":"","inReviewEnabled":false,"inReviewRevisionsEnabled":true},"keywords":"Sleep deprivation, Attention, Thalamus, Functional connectivity, Imaging","lastPublishedDoi":"10.21203/rs.3.rs-3865082/v1","lastPublishedDoiUrl":"https://doi.org/10.21203/rs.3.rs-3865082/v1","license":{"name":"CC BY 4.0","url":"https://creativecommons.org/licenses/by/4.0/"},"manuscriptAbstract":"\u003cp\u003eAttentional function is significantly damaged by acute sleep deprivation (SD), which manifests with thalamic dysfunction and the abnormal functional connectivity (FC) of extensive brain networks. However, the FC between the thalamus subregions and cerebrum underlying attentional impairment after acute SD remains elusive. Here, we aimed to probe the relationship between the attentional function and the altered thalamocortical FC after acute SD. In this study, 25 healthy participants with regular sleep conducted attentional network test and received resting-state fMRI scan before and after 24 h of SD. Then, we analyzed the FC between the thalamus and cerebrum and relationships with attentional function in the enrolled subjects. Our results displayed that the participants showed the significantly lower alerting effect, higher executive effect, and a lower accuracy after acute SD. Compared to the RW state, we observed the decreased FCs between \u0026lsquo;somatosensory\u0026rsquo; thalamic seed and left frontal pole, right frontal pole, left middle temporal gyrus (posterior division), and right middle temporal gyrus (posterior division). Furthermore, the reduced FC between the right middle temporal gyrus and \u0026lsquo;somatosensory\u0026rsquo; thalamic seed was negatively associated with the change in orienting effect of the participants. Our findings reveal that the damaged thalamocortical FC after SD may contribute to the declined attention.\u003c/p\u003e","manuscriptTitle":"Altered functional connectivity of thalamus subregions after sleep deprivation associated with impaired attention","msid":"","msnumber":"","nonDraftVersions":[{"code":1,"date":"2024-01-17 17:22:38","doi":"10.21203/rs.3.rs-3865082/v1","editorialEvents":[{"type":"communityComments","content":0}],"status":"published","journal":{"display":true,"email":"[email protected]","identity":"researchsquare","isNatureJournal":false,"hasQc":true,"allowDirectSubmit":true,"externalIdentity":"","sideBox":"","snPcode":"","submissionUrl":"/submission","title":"Research Square","twitterHandle":"researchsquare","acdcEnabled":true,"dfaEnabled":false,"editorialSystem":"","reportingPortfolio":"","inReviewEnabled":false,"inReviewRevisionsEnabled":true}}],"origin":"","ownerIdentity":"8289d4d4-bcad-4f49-9984-5e75b032adf9","owner":[],"postedDate":"January 17th, 2024","published":true,"recentEditorialEvents":[],"rejectedJournal":[],"revision":"","amendment":"","status":"published-in-journal","subjectAreas":[],"tags":[],"updatedAt":"2024-07-29T02:15:53+00:00","versionOfRecord":{"articleIdentity":"rs-3865082","link":"https://doi.org/10.2147/NSS.S472323","journal":{"identity":"nature-and-science-of-sleep","isVorOnly":true,"title":"Nature and Science of Sleep"},"publishedOn":"2024-07-01 02:15:53","publishedOnDateReadable":"July 1st, 2024"},"versionCreatedAt":"2024-01-17 17:22:38","video":"","vorDoi":"10.2147/NSS.S472323","vorDoiUrl":"https://doi.org/10.2147/NSS.S472323","workflowStages":[]},"version":"v1","identity":"rs-3865082","journalConfig":"researchsquare"},"__N_SSP":true},"page":"/article/[identity]/[[...version]]","query":{"redirect":"/article/rs-3865082","identity":"rs-3865082","version":["v1"]},"buildId":"qtupq5eGEP_6zYnWcrvyt","isFallback":false,"isExperimentalCompile":false,"dynamicIds":[84888],"gssp":true,"scriptLoader":[]}