Skip to main content
SpringerLink
Log in

Aberrant regional homogeneity of resting-state executive control, default mode, and salience networks in adult patients with moyamoya disease

  • Original Research
  • Published:
Brain Imaging and Behavior Aims and scope Submit manuscript

Abstract

Aberrant local connectivity within cerebral intrinsic connectivity networks (ICNs) at rest has not been reported in adult moyamoya disease (MMD). Our aim was to examine the regional homogeneity (ReHo) of executive control (ECN), default mode (DMN), and salience networks (SN) in patients with executive dysfunction to explore the underlying mechanism. Twenty-six adult patients with MMD and 24 normal control (NC) subjects were recruited. Executive function was evaluated by Trail Making Test Part B (TMT-B) and executive subtests of Memory and Executive Screening (MES-EX). Compared with NC, the case group exhibited ReHo decrease mainly in the frontal and parietal gyrus, and increase only in the left middle temporal gyrus. Subsequent ICNs analysis indicated that compared with NC, patients with MMD exhibited significantly decreased ReHo in the dorsolateral prefrontal cortex (DLPFC) and inferior parietal gyrus (IPG) of left ECN; the IPG, superior frontal gyrus, and DLPFC of the right ECN; the right precuneus, left medial superior frontal gyrus, and right medial orbitofrontal gyrus of the DMN; as well as the left middle frontal gyrus and right supplemental motor area of SN. When referring to the Suzuki’s 6-stage classification, a trend of ReHo decrease with disease severity was observed in all of the ICNs examined, but only bilateral ECNs reached statistical significance. Finally, only bilateral ECNs exhibited a significant correlation of averaged ReHo values with executive performance. Our results provide new insight into the pathophysiology of adult MMD.

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
Fig. 4
Fig. 5

Similar content being viewed by others

References

  • Biswal, B., Yetkin, F. Z., Haughton, V. M., & Hyde, J. S. (1995). Functional connectivity in the motor cortex of resting human brain using echo-planar MRI. Magnetic Resonance in Medicine, 34(4), 537–541.

    Article  CAS  PubMed  Google Scholar 

  • Bressler, S. L., & Menon, V. (2010). Large-scale brain networks in cognition: emerging methods and principles. Trends in Cognitive Sciences, 14(6), 277–290.

    Article  PubMed  Google Scholar 

  • Buckner, R. L., Andrews-Hanna, J. R., & Schacter, D. L. (2008). The brain's default network: anatomy, function, and relevance to disease. Annals of the New York Academy of Sciences, 1124, 1–38.

    Article  PubMed  Google Scholar 

  • Calviere, L., Catalaa, I., Marlats, F., Viguier, A., Bonneville, F., Cognard, C., et al. (2010). Correlation between cognitive impairment and cerebral hemodynamic disturbances on perfusion magnetic resonance imaging in European adults with moyamoya disease. Clinical article. Journal of Neurosurgery, 133(4), 753–759.

    Article  Google Scholar 

  • Cocchi, L., Halford, G. S., Zalesky, A., Harding, I. H., Ramm, B. J., Cutmore, T., et al. (2014). Complexity in relational processing predicts changes in functional brain network dynamics. Cerebral Cortex, 24(9), 2283–2296.

    Article  PubMed  Google Scholar 

  • Cole, M. W., Reynolds, J. R., Power, J. D., Repovs, G., Anticevic, A., & Braver, T. S. (2013). Multi-task connectivity reveals flexible hubs for adaptive task control. Nature Neuroscience, 16(9), 1348–1355.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Festa, J. R., Schwarz, L. R., Pliskin, N., Cullum, C. M., Lacritz, L., Charbel, F. T., et al. (2010). Neurocognitive dysfunction in adult moyamoya disease. Journal of Neurology, 257(5), 806–815.

    Article  PubMed  Google Scholar 

  • Gorelick, P. B., Scuteri, A., Black, S. E., Decarli, C., Greenberg, S. M., Iadecola, C., et al. (2011). Vascular contributions to cognitive impairment and dementia: a statement for healthcare professionals from the American heart association/American stroke association. Stroke, 42(9), 2672–2713.

    Article  PubMed  PubMed Central  Google Scholar 

  • Guo, Q. H., Zhou, B., Zhao, Q. H., Wang, B., & Hong, Z. (2012). Memory and executive screening (MES): a brief cognitive test for detecting mild cognitive impairment. BMC Neurology, 12, 119.

    Article  PubMed  PubMed Central  Google Scholar 

  • Karzmark, P., Zeifert, P. D., Tan, S., Dorfman, L. J., Bell-Stephens, T. E., & Steinberg, G. K. (2008). Effect of moyamoya disease on neuropsychological functioning in adults. Neurosurgery, 62(5), 1048–1051 discussion 1051-1052.

    Article  PubMed  Google Scholar 

  • Karzmark, P., Zeifert, P. D., Bell-Stephens, T. E., Steinberg, G. K., & Dorfman, L. J. (2012). Neurocognitive impairment in adults with moyamoya disease without stroke. Neurosurgery, 70(3), 634–638.

    Article  PubMed  Google Scholar 

  • Katzman, R., Zhang, M. Y., Ouang-Ya-Qu, W. Z. Y., Liu, W. T., Yu, E., et al. (1998). A Chinese version of the mini-mental state examination; impact of illiteracy in a Shanghai dementia survey. Journal of Clinical Epidemiology, 41(10), 971–978.

    Article  Google Scholar 

  • Kazumata, K., Tha, K. K., Narita, H., Kusumi, I., Shichinohe, H., Ito, M., et al. (2015). Chronic ischemia alters brain microstructural integriy and cognitive performance in adult moyamoya disease. Stroke, 46(2), 354–360.

    Article  CAS  PubMed  Google Scholar 

  • Lei, Y., Li, Y. J., Ni, W., Jiang, H. Q., Yang, Z., Guo, Q. H., et al. (2014). Spontaneous brain activity in adult patients with moyamoya disease: a resting-state fMRI study. Brain Research, 1546, 27–33.

    Article  CAS  PubMed  Google Scholar 

  • Liang, X., Zou, Q. H., He, Y., & Yang, Y. H. (2015). Topologically reorganized connectivity architecture of default-mode, executive-control, and salience networks across working memory task loads. Cerebral Cortex. doi:10.1093/cercor/bhu316.

    Google Scholar 

  • Lu, L., & Bigler, E. D. (2002). Normative data on trail making test for neurologically normal, Chinese-speaking adults. Applied Neuropsychology, 9(4), 219–225.

    Article  PubMed  Google Scholar 

  • Schubert, G. A., Czabanka, M., Seiz, M., Horn, P., Vajkoczy, P., & Thomé, C. (2014). Perfusion characteristics of moyamoya disease: an anatomically and clinically oriented analysis and comparison. Stroke, 45(1), 101–106.

    Article  PubMed  Google Scholar 

  • Seeley, W. W., Menon, V., Schatzberg, A. F., Keller, J., Glover, G. H., Kenna, H., et al. (2007). Dissociable intrinsic connectivity networks for salience processing and executive control. The Journal of Neuroscience, 27(9), 2349–2356.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Shirer, W. R., Ryali, S., Rykhlevskaia, E., Menon, V., & Greicius, M. D. (2012). Decoding subject-driven cognitive states with whole-brain connectivity patterns. Cerebral Cortex, 22(1), 158–165.

    Article  CAS  PubMed  Google Scholar 

  • Sridharan, D., Levitin, D. J., & Menon, V. (2008). A critical role for the right fronto-insular cortex in switching between central-executive and default-mode networks. Proceedings of the National Academy of Sciences of the United States of America, 105(34), 12569–12574.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Suzuki, J., & Takaku, A. (1969). Cerebrovascular “moyamoya” disease. Disease showing abnormal net-like vessels in base of brain. Archives of Neurology, 20(3), 288–299.

    Article  CAS  PubMed  Google Scholar 

  • Vincent, J. L., Kahn, I., Snyder, A. Z., Raichle, M. E., & Bucker, R. L. (2008). Evidence for a frontoparietal control system revealed by intrinsic functional connectivity. Journal of Neurophysiology, 100(6), 3328–3342.

    Article  PubMed  PubMed Central  Google Scholar 

  • Weinberg, D. G., Rahme, R. J., Aoun, S. G., Batjer, H. H., & Bendok, B. R. (2011). Moyamoya disease: functional and neurocognitive outcomes in the pediatric and adult populations. Neurosurgical Focus, 30(6), E21.

    Article  PubMed  Google Scholar 

  • Wu, T., Long, X. Y., Zang, Y. F., Wang, L., Hallett, M., Li, K. C., et al. (2009). Regional homogeneity changes in patients with Parkinson’s disease. Human Brain Mapping, 30(5), 1502–1510.

    Article  PubMed  Google Scholar 

  • Xin, F., & Lei, X. (2015). Competition between frontoparietal control and default networks supports social working memory and empathy. Social Cognitive and Affective Neuroscience. doi:10.1093/scan/nsu160.

    PubMed Central  Google Scholar 

  • Zang, Y. F., Jiang, T. Z., Lu, Y. L., He, Y., & Tian, L. X. (2004). Regional homogeneity approach to fMRI data analysis. NeuroImage, 22(1), 394–400.

    Article  PubMed  Google Scholar 

Download references

Acknowledgments

This work is supported by grant 2014CB541604 from the National Key Basic Research Program of China (973 Program) and grant 81371307 from the National Natural Science Foundation of China.

Author information

Authors and Affiliations

  1. Department of Neurosurgery, Huashan Hospital of Fudan University, Wulumuqi Zhong Road 12, Shanghai, 200040, China

    Yu Lei, Jiabin Su, Hanqiang Jiang, Wei Ni, Heng Yang, Yuxiang Gu & Ying Mao

  2. Department of Neurology, Huashan Hospital of Fudan University, Shanghai, 200040, China

    Qihao Guo

Authors
  1. Yu Lei
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Jiabin Su
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Hanqiang Jiang
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Qihao Guo
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Wei Ni
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Heng Yang
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Yuxiang Gu
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Ying Mao
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Yuxiang Gu.

Ethics declarations

All research procedures were approved by the Institutional Ethics Committee of Huashan Hospital of Fudan University, and were conducted in accordance with the 1964 Helsinki declaration and its later amendments. All participants gave written informed consent after totally understanding the purposes of our study.

Conflicts of interest

Yu Lei, Jiabin Su, Hanqiang Jiang, Qihao Guo, Wei Ni, Heng Yang, Yuxiang Gu, and Ying Mao declare that they have no conflicts of interest.

Additional information

Yu Lei and Jiabin Su contributed equally to this work.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Lei, Y., Su, J., Jiang, H. et al. Aberrant regional homogeneity of resting-state executive control, default mode, and salience networks in adult patients with moyamoya disease. Brain Imaging and Behavior 11, 176–184 (2017). https://doi.org/10.1007/s11682-016-9518-5

Download citation

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11682-016-9518-5

Keywords

Search

Navigation