Advertisement

Brain Imaging and Behavior

, Volume 12, Issue 6, pp 1650–1657 | Cite as

Abnormal functional connectivity density in sleep-deprived subjects

  • Liu Yang
  • Yu Lei
  • Lubin Wang
  • Pinhong Chen
  • Shan Cheng
  • Shanshan Chen
  • Jicheng Sun
  • Yanyan Li
  • Yihan Wang
  • Wendong HuEmail author
  • Zheng YangEmail author
ORIGINAL RESEARCH
  • 206 Downloads

Abstract

Sleep deprivation (SD) can alter the intrinsic brain functional organization. However, its effects on intrinsic low-frequency connectivity in the whole brain have not been well characterized. In this study, we used voxel-based functional connectivity density (FCD) analysis to investigate the effects of SD on the spontaneous functional organization of the brain. Thirty-seven healthy participants underwent this within-subject crossover functional magnetic resonance imaging (fMRI) study during rested wakefulness (RW) and after 36 h of total sleep deprivation (TSD). Decreased long-/short-range FCDs were observed in the posterior cingulate cortex, precuneus, inferior parietal lobule, dorsolateral prefrontal cortex, dorsomedial prefrontal cortex, and ventromedial prefrontal cortex. Increased long-/short-range FCDs were found in the sensory integration and arousal regulating areas, including the postcentral gyrus, thalamus, superior temporal gyrus, and occipital-temporal cortex. Moreover, a significant negative correlation was found between the short-range FCD of the PCC and the reaction time of Psychomotor Vigilance Task. In the present study, spontaneous functional organization with significant group-wise differences between RW and TSD sessions was identified. Our findings extend our understanding of the neural mechanism of how brain activity is altered in sleep-deprived individuals.

Keywords

fMRI Functional connectivity density Resting state Sleep deprivation 

Notes

Funding

This work was supported by the National Military Science Foundation of China, Nos. AWS12J003-2 (ZY), 2012ZX09031 (ZY); the National Key Technology R&D Program, No. 2013BAH02B00 (ZY).

Compliance with ethical standards

Conflict of interest

None.

Ethical approval

All procedures performed in studies involving human participants were in accordance with the ethical standards of the institutional and/or national research committee and with the 1964 Helsinki declaration and its later amendments or comparable ethical standards.

Informed consent

Informed consent was obtained from all individual participants included in the study.

References

  1. Addis, D. R., McIntosh, A. R., Moscovitch, M., Crawley, A. P., & McAndrews, M. P. (2004). Characterizing spatial and temporal features of autobiographical memory retrieval networks: a partial least squares approach. Neuroimage, 23(4), 1460–1471.CrossRefGoogle Scholar
  2. Bembich, S., Clarici, A., Vecchiet, C., Baldassi, G., Cont, G., & Demarini, S. (2014). Differences in time course activation of dorsolateral prefrontal cortex associated with low or high risk choices in a gambling task. Frontiers in Human Neuroscience, 8, 464.CrossRefGoogle Scholar
  3. Ben Simon, E., Maron-Katz, A., Lahav, N., Shamir, R., & Hendler, T. (2017). Tired and misconnected: a breakdown of brain modularity following sleep deprivation. Human Brain Mapping, 38(6), 3300–3314.CrossRefGoogle Scholar
  4. Charroud, C., Steffener, J., Le Bars, E., Deverdun, J., Bonafe, A., Abdennour, M., et al. (2015). Working memory activation of neural networks in the elderly as a function of information processing phase and task complexity. Neurobiology of Learning and Memory, 125, 211–223.CrossRefGoogle Scholar
  5. Chee, M. W. L., Tan, J. C., Parimal, S., & Zagorodnov, V. (2010). Sleep deprivation and its effects on object-selective attention. NeuroImage, 49(2), 1903–1910.  https://doi.org/10.1016/j.neuroimage.2009.08.067.CrossRefPubMedGoogle Scholar
  6. Chuah, Y. M. L., Venkatraman, V., Dinges, D. F., & Chee, M. W. L. (2006). The neural basis of interindividual variability in inhibitory efficiency after sleep deprivation. The Journal of Neuroscience: The Official Journal of the Society for Neuroscience, 26(27), 7156–7162.  https://doi.org/10.1523/JNEUROSCI.0906-06.2006.CrossRefGoogle Scholar
  7. De Havas, J. A., Parimal, S., Soon, C. S., & Chee, M. W. L. (2012). Sleep deprivation reduces default mode network connectivity and anti-correlation during rest and task performance. NeuroImage, 59(2), 1745–1751.  https://doi.org/10.1016/j.neuroimage.2011.08.026.CrossRefPubMedGoogle Scholar
  8. Drummond, S. P. A., Bischoff-Grethe, A., Dinges, D. F., Ayalon, L., Mednick, S. C., & Meloy, M. J. (2005). The neural basis of the psychomotor vigilance task. Sleep-New York Then Westchester-, 28(9), 1059.Google Scholar
  9. Du Boisgueheneuc, F., Levy, R., Volle, E., Seassau, M., Duffau, H., Kinkingnehun, S., et al. (2006). Functions of the left superior frontal gyrus in humans: a lesion study. Brain, 129(12), 3315–3328.CrossRefGoogle Scholar
  10. Fransson, P., & Marrelec, G. (2008). The precuneus/posterior cingulate cortex plays a pivotal role in the default mode network: evidence from a partial correlation network analysis. Neuroimage, 42(3), 1178–1184.CrossRefGoogle Scholar
  11. Japee, S., Holiday, K., Satyshur, M. D., Mukai, I., & Ungerleider, L. G. (2015). A role of right middle frontal gyrus in reorienting of attention: a case study. Frontiers in Systems Neuroscience, 9, 23.CrossRefGoogle Scholar
  12. Kong, D., Asplund, C. L., & Chee, M. W. L. (2014). Sleep deprivation reduces the rate of rapid picture processing. Neuroimage, 91, 169–176.CrossRefGoogle Scholar
  13. Lei, Y., Shao, Y., Wang, L., Zhai, T., Zou, F., Ye, E., et al. (2015). Large-scale brain network coupling predicts total sleep deprivation effects on cognitive capacity. PLOS ONE, 10(7), e0133959.  https://doi.org/10.1371/journal.pone.0133959.CrossRefPubMedPubMedCentralGoogle Scholar
  14. Lei, Y., Wang, L., Chen, P., Li, Y., Han, W., Ge, M., et al. (2016). Neural correlates of increased risk-taking propensity in sleep-deprived people along with a changing risk level. Brain Imaging and Behavior.  https://doi.org/10.1007/s11682-016-9658-7.CrossRefGoogle Scholar
  15. Liu, H., Li, H., Wang, Y., & Lei, X. (2014). Enhanced brain small-worldness after sleep deprivation: a compensatory effect. Journal of Sleep Research, 23(5), 554–563.  https://doi.org/10.1111/jsr.12147.CrossRefPubMedGoogle Scholar
  16. Lundstrom, B. N., Ingvar, M., & Petersson, K. M. (2005). The role of precuneus and left inferior frontal cortex during source memory episodic retrieval. Neuroimage, 27(4), 824–834.CrossRefGoogle Scholar
  17. Menz, M. M., Buchel, C., & Peters, J. (2012). Sleep deprivation is associated with attenuated parametric valuation and control signals in the midbrain during value-based decision making. Journal of Neuroscience.  https://doi.org/10.1523/JNEUROSCI.3553-11.2012.CrossRefPubMedGoogle Scholar
  18. Mu, Q., Mishory, A., Johnson, K. A., Nahas, Z., Kozel, F. A., Yamanaka, K., et al. (2005a). Decreased brain activation during a working memory task at rested baseline is associated with vulnerability to sleep deprivation. Sleep, 28(4), 433–446.CrossRefGoogle Scholar
  19. Mu, Q., Nahas, Z., Johnson, K. A., Yamanaka, K., Mishory, A., Koola, J., et al. (2005b). Decreased cortical response to verbal working memory following sleep deprivation. Sleep, 28, 55–67.CrossRefGoogle Scholar
  20. Murphy, K., & Fox, M. D. (2017). Towards a consensus regarding global signal regression for resting state functional connectivity MRI. NeuroImage, 154(2016), 169–173.  https://doi.org/10.1016/j.neuroimage.2016.11.052.CrossRefPubMedPubMedCentralGoogle Scholar
  21. Namni Goel, Rao, H., Durmer, J. S., Dinges, D. F. (2009). Neurocognitive consequences of sleep deprivation. 29(4), 320–339.  https://doi.org/10.1055/s-0029-1237117.Neurocognitive.
  22. Power, J. D., Barnes, K. A., Snyder, A. Z., Schlaggar, B. L., & Petersen, S. E. (2012). Spurious but systematic correlations in functional connectivity MRI networks arise from subject motion. NeuroImage, 59(3), 2142–2154.  https://doi.org/10.1016/j.neuroimage.2011.10.018.CrossRefPubMedGoogle Scholar
  23. Qin, W., Xuan, Y., Liu, Y., Jiang, T., & Yu, C. (2015). Functional connectivity density in congenitally and late blind subjects. Cerebral Cortex, 25(9), 2507–2516.  https://doi.org/10.1093/cercor/bhu051.CrossRefPubMedGoogle Scholar
  24. Raichle, M. E. (2015). The restless brain: how intrinsic activity organizes brain function. Philosophical Transactions of the Royal Society of London B: Biological Sciences, 370(1668), 20140172.  https://doi.org/10.1098/rstb.2014.0172.CrossRefPubMedGoogle Scholar
  25. Raichle, M. E., MacLeod, A. M., Snyder, A. Z., Powers, W. J., Gusnard, D. A., & Shulman, G. L. (2001). A default mode of brain function. Proceedings of the National Academy of Sciences, 98(2), 676–682.CrossRefGoogle Scholar
  26. Sämann, P. G., Tully, C., Spoormaker, V. I., Wetter, T. C., Holsboer, F., Wehrle, R., & Czisch, M. (2010). Increased sleep pressure reduces resting state functional connectivity. Magma (New York, N.Y.), 23(5–6), 375–389.  https://doi.org/10.1007/s10334-010-0213-z.CrossRefGoogle Scholar
  27. Schilling, C., Kühn, S., Paus, T., Romanowski, A., Banaschewski, T., Barbot, A., et al. (2013). Cortical thickness of superior frontal cortex predicts impulsiveness and perceptual reasoning in adolescence. Molecular Psychiatry, 18(5), 624–630.CrossRefGoogle Scholar
  28. Schmidt, M. H. (2014). The energy allocation function of sleep: a unifying theory of sleep, torpor, and continuous wakefulness. Neuroscience and Biobehavioral Reviews, 47C, 122–153.  https://doi.org/10.1016/j.neubiorev.2014.08.001.CrossRefGoogle Scholar
  29. Simon, E. B., Oren, N., Sharon, H., Kirschner, A., Goldway, N., Okon-Singer, H., et al. (2015). Losing neutrality: the neural basis of impaired emotional control without sleep. Journal of Neuroscience, 35(38), 13194–13205.  https://doi.org/10.1523/JNEUROSCI.1314-15.2015.CrossRefPubMedGoogle Scholar
  30. Thomas, M., Sing, H., Belenky, G., Holcomb, H., Mayberg, H., Dannals, R., et al. (2000). Neural basis of alertness and cognitive performance impairments during sleepiness. Journal of Sleep Research, 9(4), 335–352.CrossRefGoogle Scholar
  31. Thomas, M. L., Sing, H. C., Belenky, G., Holcomb, H. H., Mayberg, H. S., Dannals, R. F., et al. (2003). Neural basis of alertness and cognitive performance impairments during sleepiness. I. Effects of 24 h of sleep deprivation on waking human regional brain activity. Journal of Sleep Research, 9(4), 335–352.CrossRefGoogle Scholar
  32. Tomasi, D., & Volkow, N. D. (2010). Functional connectivity density mapping. Proceedings of the National Academy of Sciences of the United States of America, 107(21), 9885–9890.  https://doi.org/10.1073/pnas.1001414107.CrossRefPubMedPubMedCentralGoogle Scholar
  33. Tomasi, D., & Volkow, N. D. (2011a). Functional connectivity hubs in the human brain. NeuroImage, 57(3), 908–917.  https://doi.org/10.1016/j.neuroimage.2011.05.024.CrossRefPubMedPubMedCentralGoogle Scholar
  34. Tomasi, D., & Volkow, N. D. (2011b). Association between functional connectivity hubs and brain networks. Cerebral Cortex, 21(9), 2003–2013.  https://doi.org/10.1093/cercor/bhq268.CrossRefPubMedGoogle Scholar
  35. Tomasi, D., & Volkow, N. D. (2012a). Abnormal functional connectivity in children with attention-deficit/hyperactivity disorder. Biological Psychiatry, 71(5), 443–450.  https://doi.org/10.1016/j.biopsych.2011.11.003.CrossRefPubMedGoogle Scholar
  36. Tomasi, D., & Volkow, N. D. (2012b). Gender differences in brain functional connectivity density. Human Brain Mapping, 33(4), 849–860.  https://doi.org/10.1002/hbm.21252.CrossRefPubMedGoogle Scholar
  37. Tomasi, D., & Volkow, N. D. (2012c). Laterality patterns of brain functional connectivity: gender effects. Cerebral Cortex (New York, N.Y.: 1991), 22(6), 1455–1462.  https://doi.org/10.1093/cercor/bhr230.CrossRefGoogle Scholar
  38. Tomasi, D., Wang, R. L., Telang, F., Boronikolas, V., Jayne, M. C., Wang, G.-J., et al. (2009). Impairment of attentional networks after 1 night of sleep deprivation. Cerebral Cortex (New York, N.Y.: 1991), 19(1), 233–240.  https://doi.org/10.1093/cercor/bhn073.CrossRefGoogle Scholar
  39. Tomasi, D., Shokri-Kojori, E., & Volkow, N. D. (2015). High-resolution functional connectivity density: hub locations, sensitivity, specificity,reproducibility, and reliability. Cerebral Cortex, 200, bhv171.  https://doi.org/10.1093/cercor/bhv171.CrossRefGoogle Scholar
  40. Utevsky, A. V., Smith, D. V., & Huettel, S. A. (2014). Precuneus is a functional core of the default-mode network. The Journal of Neuroscience, 34(3), 932–940.CrossRefGoogle Scholar
  41. Wang, Y., Liu, H., Hitchman, G., & Lei, X. (2015). Module number of default mode network: inter-subject variability and effects of sleep deprivation. Brain Research, 1596, 69–78.CrossRefGoogle Scholar
  42. Wu, J. C., Gillin, J. C., Buchsbaum, M. S., & Hershey, T. (1991). The effect of sleep deprivation on cerebral glucose metabolic rate in normal humans assessed with positron emission tomography. Sleep: Journal of Sleep Research & Sleep Medicine.Google Scholar
  43. Yeo, B. T. T., Tandi, J., & Chee, M. W. L. (2015). Functional connectivity during rested wakefulness predicts vulnerability to sleep deprivation. NeuroImage, 111, 147–158.  https://doi.org/10.1016/j.neuroimage.2015.02.018.CrossRefPubMedGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC, part of Springer Nature 2018

Authors and Affiliations

  • Liu Yang
    • 1
    • 2
  • Yu Lei
    • 1
    • 2
    • 3
  • Lubin Wang
    • 1
    • 2
  • Pinhong Chen
    • 1
    • 2
  • Shan Cheng
    • 4
  • Shanshan Chen
    • 1
    • 2
  • Jicheng Sun
    • 4
  • Yanyan Li
    • 1
    • 2
  • Yihan Wang
    • 4
  • Wendong Hu
    • 4
    Email author
  • Zheng Yang
    • 1
    • 2
    Email author
  1. 1.Beijing Institute of Basic Medical SciencesBeijingPeople’s Republic of China
  2. 2.Cognitive and Mental Health Research CenterBeijingPeople’s Republic of China
  3. 3.Brain Science CenterInstitute of Basic Medical SciencesBeijingPeople’s Republic of China
  4. 4.School of Aerospace MedicineFourth Military Medical UniversityXi’anPeople’s Republic of China

Personalised recommendations