Skip to main content
SpringerLink
Log in

Abnormal functional connectivity density in sleep-deprived subjects

  • ORIGINAL RESEARCH
  • Published:
Brain Imaging and Behavior Aims and scope Submit manuscript

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.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

References

  • 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.

    Article  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  PubMed  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • 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.

    Article  PubMed  Google Scholar 

  • 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 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  Google Scholar 

  • Kong, D., Asplund, C. L., & Chee, M. W. L. (2014). Sleep deprivation reduces the rate of rapid picture processing. Neuroimage, 91, 169–176.

    Article  Google Scholar 

  • 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.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  PubMed  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  PubMed  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  PubMed  PubMed Central  Google Scholar 

  • 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.

  • 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.

    Article  PubMed  Google Scholar 

  • 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.

    Article  PubMed  Google Scholar 

  • 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.

    Article  PubMed  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  CAS  PubMed  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  PubMed  PubMed Central  Google Scholar 

  • 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.

    Article  PubMed  PubMed Central  Google Scholar 

  • 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.

    Article  PubMed  Google Scholar 

  • 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.

    Article  PubMed  Google Scholar 

  • 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.

    Article  PubMed  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • 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.

  • 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.

    Article  PubMed  Google Scholar 

Download references

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).

Author information

Authors and Affiliations

  1. Beijing Institute of Basic Medical Sciences, Beijing, People’s Republic of China

    Liu Yang, Yu Lei, Lubin Wang, Pinhong Chen, Shanshan Chen, Yanyan Li & Zheng Yang

  2. Cognitive and Mental Health Research Center, Beijing, People’s Republic of China

    Liu Yang, Yu Lei, Lubin Wang, Pinhong Chen, Shanshan Chen, Yanyan Li & Zheng Yang

  3. Brain Science Center, Institute of Basic Medical Sciences, Beijing, People’s Republic of China

    Yu Lei

  4. School of Aerospace Medicine, Fourth Military Medical University, Xi’an, People’s Republic of China

    Shan Cheng, Jicheng Sun, Yihan Wang & Wendong Hu

Authors
  1. Liu Yang
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Yu Lei
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Lubin Wang
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Pinhong Chen
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Shan Cheng
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Shanshan Chen
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Jicheng Sun
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Yanyan Li
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Yihan Wang
    View author publications

    You can also search for this author in PubMed Google Scholar

  10. Wendong Hu
    View author publications

    You can also search for this author in PubMed Google Scholar

  11. Zheng Yang
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding authors

Correspondence to Wendong Hu or Zheng Yang.

Ethics declarations

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.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Yang, L., Lei, Y., Wang, L. et al. Abnormal functional connectivity density in sleep-deprived subjects. Brain Imaging and Behavior 12, 1650–1657 (2018). https://doi.org/10.1007/s11682-018-9829-9

Download citation

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11682-018-9829-9

Keywords

Search

Navigation