Dysfunction of large-scale brain networks underlying cognitive impairments in shift work disorder
Yan Zhao
Beijing Key Laboratory of Mental Disorders, National Clinical Research Center for Mental Disorders & National Center for Mental Disorders, Beijing Anding Hospitaldiscu, Capital Medical University, Beijing, China
Advanced Innovation Center for Human Brain Protection, Capital Medical University, Beijing, China
Contribution: Writing - original draft, Investigation, Formal analysis, Methodology
Search for more papers by this authorSitong Feng
Beijing Key Laboratory of Mental Disorders, National Clinical Research Center for Mental Disorders & National Center for Mental Disorders, Beijing Anding Hospitaldiscu, Capital Medical University, Beijing, China
Advanced Innovation Center for Human Brain Protection, Capital Medical University, Beijing, China
Contribution: Writing - original draft, Investigation, Formal analysis, Methodology
Search for more papers by this authorLinrui Dong
Beijing Key Laboratory of Mental Disorders, National Clinical Research Center for Mental Disorders & National Center for Mental Disorders, Beijing Anding Hospitaldiscu, Capital Medical University, Beijing, China
Advanced Innovation Center for Human Brain Protection, Capital Medical University, Beijing, China
Contribution: Investigation, Data curation
Search for more papers by this authorZiyao Wu
Beijing Key Laboratory of Mental Disorders, National Clinical Research Center for Mental Disorders & National Center for Mental Disorders, Beijing Anding Hospitaldiscu, Capital Medical University, Beijing, China
Advanced Innovation Center for Human Brain Protection, Capital Medical University, Beijing, China
Contribution: Investigation, Data curation
Search for more papers by this authorCorresponding Author
Yanzhe Ning
Beijing Key Laboratory of Mental Disorders, National Clinical Research Center for Mental Disorders & National Center for Mental Disorders, Beijing Anding Hospitaldiscu, Capital Medical University, Beijing, China
Advanced Innovation Center for Human Brain Protection, Capital Medical University, Beijing, China
Correspondence
Yanzhe Ning, Beijing Key Laboratory of Mental Disorders, National Clinical Research Center for Mental Disorders & National Center for Mental Disorders, Beijing Anding Hospital, Capital Medical University, Beijing, China.
Email: [email protected]
Contribution: Conceptualization, Methodology, Investigation, Funding acquisition, Writing - review & editing
Search for more papers by this authorYan Zhao
Beijing Key Laboratory of Mental Disorders, National Clinical Research Center for Mental Disorders & National Center for Mental Disorders, Beijing Anding Hospitaldiscu, Capital Medical University, Beijing, China
Advanced Innovation Center for Human Brain Protection, Capital Medical University, Beijing, China
Contribution: Writing - original draft, Investigation, Formal analysis, Methodology
Search for more papers by this authorSitong Feng
Beijing Key Laboratory of Mental Disorders, National Clinical Research Center for Mental Disorders & National Center for Mental Disorders, Beijing Anding Hospitaldiscu, Capital Medical University, Beijing, China
Advanced Innovation Center for Human Brain Protection, Capital Medical University, Beijing, China
Contribution: Writing - original draft, Investigation, Formal analysis, Methodology
Search for more papers by this authorLinrui Dong
Beijing Key Laboratory of Mental Disorders, National Clinical Research Center for Mental Disorders & National Center for Mental Disorders, Beijing Anding Hospitaldiscu, Capital Medical University, Beijing, China
Advanced Innovation Center for Human Brain Protection, Capital Medical University, Beijing, China
Contribution: Investigation, Data curation
Search for more papers by this authorZiyao Wu
Beijing Key Laboratory of Mental Disorders, National Clinical Research Center for Mental Disorders & National Center for Mental Disorders, Beijing Anding Hospitaldiscu, Capital Medical University, Beijing, China
Advanced Innovation Center for Human Brain Protection, Capital Medical University, Beijing, China
Contribution: Investigation, Data curation
Search for more papers by this authorCorresponding Author
Yanzhe Ning
Beijing Key Laboratory of Mental Disorders, National Clinical Research Center for Mental Disorders & National Center for Mental Disorders, Beijing Anding Hospitaldiscu, Capital Medical University, Beijing, China
Advanced Innovation Center for Human Brain Protection, Capital Medical University, Beijing, China
Correspondence
Yanzhe Ning, Beijing Key Laboratory of Mental Disorders, National Clinical Research Center for Mental Disorders & National Center for Mental Disorders, Beijing Anding Hospital, Capital Medical University, Beijing, China.
Email: [email protected]
Contribution: Conceptualization, Methodology, Investigation, Funding acquisition, Writing - review & editing
Search for more papers by this authorYan Zhao and Sitong Feng contributed equally to this work.
Summary
It has been demonstrated that shift work can affect cognitive functions. Several neuroimaging studies have revealed altered brain function and structure for patients with shift work disorder (SWD). However, knowledge on the dysfunction of large-scale brain networks underlying cognitive impairments in shift work disorder is limited. This study aims to identify altered functional networks associated with cognitive declines in shift work disorder, and to assess their potential diagnostic value. Thirty-four patients with shift work disorder and 36 healthy controls (HCs) were recruited to perform the Repeatable Battery for the Assessment of Neuropsychological Status (RBANS) and resting-state functional scans. After surface-based preprocessing, we calculated within- and between-network functional connectivity (FC) using the Dosenbach atlas. Moreover, correlation analysis was done between altered functional connectivity of large-scale brain networks and scores of cognitive assessments in patients with shift work disorder. Finally, we established a classification model to provide features for patients with shift work disorder concerning the disrupted large-scale networks. Compared with healthy controls, increased functional connectivity within-networks across the seven brain networks, and between-networks involving ventral attention network (VAN)-subcortical network (SCN), SCN-frontoparietal network (FPN), and somatosensory network (SMN)-SCN were observed in shift work disorder. Decreased functional connectivity between brain networks was found in shift work disorder compared with healthy controls, including visual network (VN)-FPN, VN-default mode network (DMN), SMN-DMN, dorsal attention network (DAN)-DMN, VAN-DMN, and FPN-DMN. Furthermore, the altered functional connectivity of large-scale brain networks was significantly correlated with scores of immediate memory, visuospatial, and delayed memory in patients with shift work disorder, respectively. Abnormal functional connectivity of large-scale brain networks may play critical roles in cognitive dysfunction in shift work disorder. Our findings provide new evidence to interpret the underlying neural mechanisms of cognitive impairments in shift work disorder.
CONFLICT OF INTEREST STATEMENT
The authors declare that there was no conflict of interest.
Open Research
DATA AVAILABILITY STATEMENT
The data that support the findings of this study are available on request from the corresponding author. The data are not publicly available due to privacy or ethical restrictions.
REFERENCES
- Alhola, P., & Polo-Kantola, P. (2007). Sleep deprivation: Impact on cognitive performance. Neuropsychiatric Disease and Treatment, 3, 553–567.
- Andrews-Hanna, J. R., Reidler, J. S., Huang, C., & Buckner, R. L. (2010). Evidence for the default network's role in spontaneous cognition. Journal of Neurophysiology, 104, 322–335.
- Booker, L. A., Barnes, M., Alvaro, P., Collins, A., Chai-Coetzer, C. L., McMahon, M., & Sletten, T. L. (2020). The role of sleep hygiene in the risk of shift work disorder in nurses. Sleep, 43, zsz228.
- Booker, L. A., Sletten, T. L., Alvaro, P. K., Barnes, M., Collins, A., Chai-Coetzer, C. L., & Howard, M. E. (2020). Exploring the associations between shift work disorder, depression, anxiety and sick leave taken amongst nurses. Journal of Sleep Research, 29, e12872.
- Booker, L. A., Sletten, T. L., Barnes, M., Alvaro, P., Collins, A., Chai-Coetzer, C. L., & Howard, M. E. (2022). The effectiveness of an individualized sleep and shift work education and coaching program to manage shift work disorder in nurses: A randomized controlled trial. Journal of Clinical Sleep Medicine, 18, 1035–1045.
- Bourdouxhe, M., & Toulouse, G. (2001). Health and safety among film technicians working extended shifts. Journal of Human Ergology (Tokyo), 30, 113–118.
- Bressler, S. L., & Menon, V. (2010). Large-scale brain networks in cognition: Emerging methods and principles. Trends in Cognitive Sciences, 14, 277–290.
- Chellappa, S. L., Morris, C. J., & Scheer, F. (2019). Effects of circadian misalignment on cognition in chronic shift workers. Science Reports, 9, 699.
- Cheng, Y., Wu, W., Wang, J., Feng, W., Wu, X., & Li, C. (2011). Reliability and validity of the repeatable battery for the assessment of neuropsychological status in community-dwelling elderly. Archives of Medical Science, 7, 850–857.
- da Silva, R. A. (2015). Sleep disturbances and mild cognitive impairment: A review. Sleep Science, 8, 36–41.
- Dai, C., Zhang, Y., Cai, X., Peng, Z., Zhang, L., Shao, Y., & Wang, C. (2020). Effects of sleep deprivation on working memory: Change in functional connectivity between the dorsal attention, default mode, and fronto-parietal networks. Frontiers in Human Neuroscience, 14, 360.
- de Cordova, P. B., Bradford, M. A., & Stone, P. W. (2016). Increased errors and decreased performance at night: A systematic review of the evidence concerning shift work and quality. Work, 53, 825–834.
- Dosenbach, N. U., Nardos, B., Cohen, A. L., Fair, D. A., Power, J. D., Church, J. A., & Schlaggar, B. L. (2010). Prediction of individual brain maturity using fMRI. Science, 329, 1358–1361.
- Elovainio, M., Ferrie, J. E., Singh-Manoux, A., Gimeno, D., De Vogli, R., Shipley, M. J., & Kivimäki, M. (2009). Cumulative exposure to high-strain and active jobs as predictors of cognitive function: The Whitehall II study. Occupational and Environmental Medicine, 66, 32–37.
- Esmaily, A., Jambarsang, S., Mohammadian, F., & Mehrparvar, A. H. (2022). Effect of shift work on working memory, attention and response time in nurses. International Journal of Occupational Safety and Ergonomics, 28, 1085–1090.
- Ester, E. F., Sprague, T. C., & Serences, J. T. (2015). Parietal and frontal cortex encode stimulus-specific mnemonic representations during visual working memory. Neuron, 87, 893–905.
- Etkin, A. (2019). A reckoning and research agenda for neuroimaging in psychiatry. The American Journal of Psychiatry, 176, 507–511.
- Feng, S., Zheng, S., Zou, H., Dong, L., Zhu, H., Liu, S., & Jia, H. (2022). Altered functional connectivity of cerebellar networks in first-episode schizophrenia. Frontiers in Cellular Neuroscience, 16, 1024192.
- Finney, G. R., Minagar, A., & Heilman, K. M. (2016). Assessment of mental status. Neurologic Clinics, 34, 1–16.
- Fogassi, L., & Luppino, G. (2005). Motor functions of the parietal lobe. Current Opinion in Neurobiology, 15, 626–631.
- Gazzaley, A., & Nobre, A. C. (2012). Top-down modulation: Bridging selective attention and working memory. Trends in Cognitive Sciences, 16, 129–135.
- Giesbrecht, B., Woldorff, M. G., Song, A. W., & Mangun, G. R. (2003). Neural mechanisms of top-down control during spatial and feature attention. NeuroImage, 19, 496–512.
- Godwin, C. A., Hunter, M. A., Bezdek, M. A., Lieberman, G., Elkin-Frankston, S., Romero, V. L., & Schumacher, E. H. (2017). Functional connectivity within and between intrinsic brain networks correlates with trait mind wandering. Neuropsychologia, 103, 140–153.
- Golchert, J., Smallwood, J., Jefferies, E., Seli, P., Huntenburg, J. M., Liem, F., & Margulies, D. S. (2017). Individual variation in intentionality in the mind-wandering state is reflected in the integration of the default-mode, fronto-parietal, and limbic networks. NeuroImage, 146, 226–235.
- Greicius, M. D., Krasnow, B., Reiss, A. L., & Menon, V. (2003). Functional connectivity in the resting brain: A network analysis of the default mode hypothesis. Proceedings of the National Academy of Sciences of the United States of America, 100, 253–258.
- Haidarimoghadam, R., Kazemi, R., Motamedzadeh, M., Golmohamadi, R., Soltanian, A., & Zoghipaydar, M. R. (2017). The effects of consecutive night shifts and shift length on cognitive performance and sleepiness: A field study. International Journal of Occupational Safety and Ergonomics, 23, 251–258.
- He, Y., Shen, J., Wang, X., Wu, Q., Liu, J., & Ji, Y. (2022). Preliminary study on brain resting-state networks and cognitive impairments of patients with obstructive sleep apnea-hypopnea syndrome. BMC Neurology, 22, 456.
- Hutton, J. S., Dudley, J., Horowitz-Kraus, T., DeWitt, T., & Holland, S. K. (2019). Functional connectivity of attention, visual, and language networks during audio, illustrated, and animated stories in preschool-age children. Brain Connectivity, 9, 580–592.
- Jehan, S., Zizi, F., Pandi-Perumal, S. R., Myers, A. K., Auguste, E., Jean-Louis, G., & McFarlane, S. I. (2017). Shift work and sleep: Medical implications and management. Sleep Medicine and Disorders, 1, 00008.
- Kaliyaperumal, D., Elango, Y., Alagesan, M., & Santhanakrishanan, I. (2017). Effects of sleep deprivation on the cognitive performance of nurses working in shift. Journal of Clinical and Diagnostic Research, 11, CC01–CC03.
- Kecklund, G., & Axelsson, J. (2016). Health consequences of shift work and insufficient sleep. BMJ, 355, i5210.
- Kim, H. (2014). Involvement of the dorsal and ventral attention networks in oddball stimulus processing: A meta-analysis. Human Brain Mapping, 35, 2265–2284.
- Kim, S. Y., Lee, K. H., Lee, H., Jeon, J. E., Kim, S., Lee, M. H., & Lee, Y. J. (2022). Neural activation underlying emotional interference of cognitive control in rotating shift workers: Moderating effects of the prefrontal cortex response on the association between sleep disturbance and depressive symptoms. Sleep, 45, zsac219.
- Leso, V., Fontana, L., Caturano, A., Vetrani, I., Fedele, M., & Iavicoli, I. (2021). Impact of shift work and long working hours on worker cognitive functions: Current evidence and future research needs. International Journal of Environmental Research and Public Health, 18, 6540.
10.3390/ijerph18126540 Google Scholar
- Moreno, C. R. C., Marqueze, E. C., Sargent, C., Wright, K. P., Jr., Ferguson, S. A., & Tucker, P. (2019). Working time society consensus statements: Evidence-based effects of shift work on physical and mental health. Industrial Health, 57, 139–157.
- Ning, Y., Li, K., Zhang, Y., Chen, P., Yin, D., Zhu, H., & Jia, H. (2020). Assessing cognitive abilities of patients with shift work disorder: Insights from RBANS and granger causality connections among resting-state networks. Frontiers in Psychiatry, 11, 780.
- Ning, Y., Zheng, S., Feng, S., Li, K., & Jia, H. (2022). Altered functional connectivity and topological organization of brain networks correlate to cognitive impairments after sleep deprivation. Journal of Nature and Science of Sleep, 14, 1285–1297.
- Nunez-Iglesias, J., Kennedy, R., Plaza, S. M., Chakraborty, A., & Katz, W. T. (2014). Graph-based active learning of agglomeration (GALA): A python library to segment 2D and 3D neuroimages. Frontiers in Neuroinformatics, 8, 34.
- Park, C. H., Bang, M., Ahn, K. J., Kim, W. J., & Shin, N. Y. (2020). Sleep disturbance-related depressive symptom and brain volume reduction in shift-working nurses. Scientific Reports, 10, 9100.
- Power, J. D., Cohen, A. L., Nelson, S. M., Wig, G. S., Barnes, K. A., Church, J. A., & Petersen, S. E. (2011). Functional network organization of the human brain. Neuron, 72, 665–678.
- Raichle, M. E. (2015). The brain's default mode network. Annual Review of Neuroscience, 38, 433–447.
- Sachdev, P. S., Blacker, D., Blazer, D. G., Ganguli, M., Jeste, D. V., Paulsen, J. S., & Petersen, R. C. (2014). Classifying neurocognitive disorders: The DSM-5 approach. Nature Reviews. Neurology, 10, 634–642.
- Seidler, R., Erdeniz, B., Koppelmans, V., Hirsiger, S., Mérillat, S., & Jäncke, L. (2015). Associations between age, motor function, and resting state sensorimotor network connectivity in healthy older adults. NeuroImage, 108, 47–59.
- Serences, J. T., & Yantis, S. (2006). Selective visual attention and perceptual coherence. Trends in Cognitive Sciences, 10, 38–45.
- Shwetha, B. L., & Sudhakar, H. H. (2014). Learning, memory & executive function in female BPO employees exposed to regular shifts. National Journal of Physiology, Pharmacy and Pharmacology, 4, 20–24.
10.5455/njppp.njppp.2014.4.140620133 Google Scholar
- Slagter, H. A., Giesbrecht, B., Kok, A., Weissman, D. H., Kenemans, J. L., Woldorff, M. G., & Mangun, G. R. (2007). fMRI evidence for both generalized and specialized components of attentional control. Brain Research, 1177, 90–102.
- Smith, D. V., Davis, B., Niu, K., Healy, E. W., Bonilha, L., Fridriksson, J., & Rorden, C. (2010). Spatial attention evokes similar activation patterns for visual and auditory stimuli. Journal of Cognitive Neuroscience, 22, 347–361.
- Sprague, T. C., & Serences, J. T. (2013). Attention modulates spatial priority maps in the human occipital, parietal and frontal cortices. Nature Neuroscience, 16, 1879–1887.
- Tian, Y., Xie, C., & Lei, X. (2022). Isolation of subjectively reported sleepiness and objectively measured vigilance during sleep deprivation: A resting-state fMRI study. Cognitive Neurodynamics, 16, 1151–1162.
- Waage, S., Moen, B. E., Pallesen, S., Eriksen, H. R., Ursin, H., Akerstedt, T., & Bjorvatn, B. (2009). Shift work disorder among oil rig workers in the North Sea. Sleep, 32, 558–565.
- Wu, P., Zhang, A., Sun, N., Lei, L., Liu, P., Wang, Y., & Zhang, K. (2021). Cortical thickness predicts response following 2 weeks of SSRI regimen in first-episode, drug-naive major depressive disorder: An MRI study. Frontiers in Psychiatry, 12, 751756.
- Wu, X., Bai, F., Wang, Y., Zhang, L., Liu, L., Chen, Y., & Zhang, T. (2021). Circadian rhythm disorders and corresponding functional brain abnormalities in young female nurses: A preliminary study. Frontiers in Neurology, 12, 664610.
- Yan, C. G., Wang, X. D., & Lu, B. (2021). DPABISurf: Data processing & analysis for brain imaging on surface. Scientific Bulletin, 66, 2453–2455.
- Yeo, B. T., Krienen, F. M., Sepulcre, J., Sabuncu, M. R., Lashkari, D., Hollinshead, M., & Buckner, R. L. (2011). The organization of the human cerebral cortex estimated by intrinsic functional connectivity. Journal of Neurophysiology, 106, 1125–1165.
- Zhou, X., Wu, T., Yu, J., & Lei, X. (2017). Sleep deprivation makes the young brain resemble the elderly brain: A large-scale brain networks study. Brain Connectivity, 7, 58–68.
- Zhu, W., Chen, Q., Xia, L., Beaty, R. E., Yang, W., Tian, F., & Qiu, J. (2017). Common and distinct brain networks underlying verbal and visual creativity. Human Brain Mapping, 38, 2094–2111.
Citing Literature
