Skip to main content
Log in

Rich club characteristics of dynamic brain functional networks in resting state

  • Published:
Multimedia Tools and Applications Aims and scope Submit manuscript

Abstract

Conventional brain functional networks are constructed by extracting the entire time series from functional Magnetic Resonance Imaging (fMRI). Yet such a method is easy to ignore the dynamic interaction patterns of brain regions that essentially change across time. In this study, we analyze the functional connectivity characteristics of Rich Club in resting-state brain functional networks, and study the dynamic functional differences of core brain regions at different time periods. First, the time series is extracted from resting-state fMRI to construct a dynamic brain functional network. Then, Rich Clubs of different time periods are determined by the Rich Club coefficients. In particular, the efficiency of each Rich Club is calculated to examine the influences of the Rich Connections, Feeder Connections and Local Connections. Finally, the node degree, clustering coefficient and efficiency for Rich Club nodes are calculated to quantify the dynamic processes of Rich Clubs, and the functional connectivity of Rich Clubs are compared with those of the functional networks constructed by the entire fMRI time series. Experimental results demonstrate that the distribution of Rich Clubs in the dynamic brain functional network is consistent with that from the entire fMRI time series, while the composition and functional connectivity of Rich Club dynamically change across time. Moreover, Rich connection and Local connection in the brain functional networks show a significant correlation with the efficiency of Rich Club, and the local and the global efficiency of Rich Clubs are greater than that of the global network. These results further illustrate the viewpoint that Rich Clubs have significant influence on the functional characteristics of global brain functional networks.

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

Access this article

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

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8

Similar content being viewed by others

References

  1. Breakspear M (2017) Dynamic models of large-scale brain activity. Nat Neurosci 20(3):340–352

    Article  Google Scholar 

  2. Calhoun VD, Miller R, Pearlson G, Adal T (2014) The chronnectome: time-varying connectivity networks as the next frontier in fMRI data discovery. Neuron 84(2):262–274

    Article  Google Scholar 

  3. Chen XB, Zhang H, Gao YZ, Wee CY, Li G, Shen DG (2016) High-order resting-state functional connectivity network for MCI classification. Hum Brain Mapp 37(9):3282–3296

    Article  Google Scholar 

  4. Chen XB, Zhang H, Lee SW, Shen DG (2017) Hierarchical high-order functional connectivity networks and selective feature fusion for MCI classification. Neuroinformatics 15(3):1–14

    Article  Google Scholar 

  5. Colizza V, Flammini A, Serrano MA, Vespignani A (2006) Detecting rich-club ordering in complex networks. Nat Phys 2(2):110–115

    Article  Google Scholar 

  6. Daianu M, Jahanshad N, Nir TM, Jack CR Jr, Weiner MW, Bernstein MA, Thompson PM (2015) Rich club analysis in the Alzheimer's disease connectome reveals a relatively undisturbed structural core network. Hum Brain Mapp 36(8):3087–3103

    Article  Google Scholar 

  7. Damaraju E, Allen EA, Belger A, Ford JM, McEwen S, Mathalon DH, Mueller BA, Pearlson GD, Potkin SG, Preda A, Turner JA, Vaidya JG, van Erp TG, Calhoun VD (2014) Dynamic functional connectivity analysis reveals transient states of dysconnectivity in schizophrenia. NeuroImage: Clin 5(C):298–308

    Article  Google Scholar 

  8. Echávarri C, Aalten P, Uylings H, Jacobs H, Visser P, Gronenschild E, Verhey F, Burgmans S (2011) Atrophy in the parahippocampal gyrus as an early biomarker of Alzheimer’s disease. Brain Struct Funct 215(3–4):265–271

    Article  Google Scholar 

  9. Geng YY, Liang RZ, Li WZ, Wang JB, Liang GY, Xu CH, Wang JY (2016) Learning convolutional neural network to maximize pos@ top performance measure. ESANN 2017 proceedings, European symposium on artificial neural networks, Computational intelligence and machine learning: 589–594

  10. Geng YY, Zhang GH, Li WZ, Gu Y, Liang RZ, Liang GY, Wang JB, Wu YB, Patil N, Wang JY (2017) A novel image tag completion method based on convolutional neural transformation. Lect Notes Comput Sci 10614:539–546

  11. Griffa A, Baumann PS, Thiran JP, Hagmann P (2013) Structural connectomics in brain diseases. Neuroimage 80(20):515–526

    Article  Google Scholar 

  12. Guusje C, Kahn RS, De RMA, Wiepke C, van den Heuvel M (2014) Impaired Rich Club connectivity in unaffected siblings of schizophrenia patients. Schizophr Bull 40(2):438–448

    Article  Google Scholar 

  13. Harrington DL, Rubinov M, Durgerian S, Mourany L, Reece C, Koenig K, Long JD, Paulsen JS (2015) Network topology and functional connectivity disturbances precede the onset of Huntington’s disease. Brain 138(8):2332–2346

    Article  Google Scholar 

  14. Jiao ZQ, Zou L, Cao Y, Qian N, Ma ZH (2014) Effective connectivity analysis of fMRI data based on network motifs. J Supercomput 67(3):809–819

    Article  Google Scholar 

  15. Jiao ZQ, Wang H, Ma K (2016) The connectivity measurement in complex directed networks by motif structure. Int J Sensor Netw 21(3):197–204

    Article  Google Scholar 

  16. Jiao ZQ, Ma K, Rong YL, Wang H, Zou L (2017) Adaptive synchronization in small-world networks with Lorenz chaotic oscillators. Int J Sensor Netw 24(2):90–97

    Article  Google Scholar 

  17. Jiao ZQ, Ma K, Wang H, Zou L, Zhang YD (2017) Research on node properties of resting-state brain functional networks by using node activity and ALFF. Multimedia Tools Appl. https://doi.org/10.1007/s11042-017-5163-2

  18. Jiao ZQ, Wang H, Ma K, Zou L, Xiang JB (2017) Directed connectivity of brain default networks using GCA and motif. Front Biosci 22(10):1634–1643

    Article  Google Scholar 

  19. Jiao ZQ, Ma K, Wang H, Zou L, Xiang JB (2017) Functional connectivity analysis of brain default mode networks using Hamiltonian path. CNS Neurol Disord Drug Targets 16(1):44–50

    Article  Google Scholar 

  20. Jiao ZQ, Wang H, Ma K, Zou L, Xiang JB, Wang SH (2017) Effective connectivity in the default network using granger causal analysis. J Med Imaging Health Inform 7(2):407–415

    Article  Google Scholar 

  21. Latora V, Marchiori M (2001) Efficient behavior of small-world networks. Phys Rev Lett 87(19):198701

    Article  Google Scholar 

  22. Li HJ, Li HY (2016) Scalably revealing the dynamics of soft community structure in complex networks. J Syst Sci Complex 29(4):1071–1088

    Article  MathSciNet  MATH  Google Scholar 

  23. Ma A, Mondragón RJ (2014) Rich-cores in networks. PLoS One 10(3):e0119678

    Article  Google Scholar 

  24. Markett S, de Reus MA, Reuter M, Montag C, Weber B, Schoene-Bake JC (2017) Serotonin and the brain's Rich Club-association between molecular genetic variation on the TPH2 gene and the structural connectome. Cereb Cortex 27(3):2166–2174

    Google Scholar 

  25. Marusak HA, Calhoun VD, Brown S, Crespo LM, Sala-Hamrick K, Gotlib IH, Thomason ME (2016) Dynamic functional connectivity of neurocognitive networks in children. Hum Brain Mapp 38(1):97–108

    Article  Google Scholar 

  26. Mccolgan P, Seunarine KK, Razi A, Cole JH, Gregory S, Durr A, Roos RAC, Stout JC, Landwehrmeyer B, Scahill RI, Clark CA, Rees G, Tabrizi SJ (2015) Selective vulnerability of Rich Club brain regions is an organizational principle of structural connectivity loss in Huntington’s disease. Brain 138(11):3327–3344

    Article  Google Scholar 

  27. Nguyen TT, Kovacevic S, Dev SI, Lu K, Liu TT, Eyler LT (2016) Dynamic functional connectivity in bipolar disorder is associated with executive function and processing speed: a preliminary study. Neuropsychology 31(1):73–83

    Article  Google Scholar 

  28. Pasquale F, Penna S, Sporns O, Romani G, Corbetta M (2016) A dynamic core network and global efficiency in the resting human brain. Cereb Cortex 26(10):878–896

    Article  Google Scholar 

  29. Poulin SP, Dautoff R, Morris JC, Barrett LF, Dickerson BC (2011) Alzheimer's disease neuroimaging initiative. Amygdala atrophy is prominent in early Alzheimer’s disease and relates to symptom severity. Psychiatry Res 194(1):7–13

    Article  Google Scholar 

  30. Power JD, Schlaggar BL, Lessov-Schlaggar CN, Petersen SE (2013) Evidence for hubs in human functional brain networks. Neuron 79(4):798–813

    Article  Google Scholar 

  31. Ray S, Miller M, Karalunas S, Robertson C, Grayson DS, Cary RP, Hawkey E, Painter JG, Fombonne E, Nigg JT, Fair DA (2015) Structural and functional connectivity of the human brain in autism spectrum disorders and attention-deficit/hyperactivity disorder: a rich club organization study. Hum Brain Mapp 35(12):6032–6048

    Article  Google Scholar 

  32. Rubinov M, Sporns O (2010) Complex network measures of brain connectivity: uses and interpretations. Neuroimage 52(3):1059–1069

    Article  Google Scholar 

  33. Sheline YI, Raichle ME (2013) Resting state functional connectivity in preclinical Alzheimer’s disease. Biol Psychiatry 74(5):340–347

    Article  Google Scholar 

  34. Sporns O, Honey C, Kötter R (2007) Identification and classification of hubs in brain networks. PLoS One 2(10):1049–1062

    Article  Google Scholar 

  35. Tobia MJ, Hayashi K, Ballard G, Gotlib IH, Waugh CE (2017) Dynamic functional connectivity and individual differences in emotions during social stress. Hum Brain Mapp 38(12):6185–6205

    Article  Google Scholar 

  36. Tzourio-Mazoyer N, Landeau B, Papathanassiou D, Crivello F, Etard O, Delcroix N, Mazoyer B, Joliot M (2002) Automated anatomical labeling of activations in SPM using a macroscopic anatomical parcellation of the MNI MRI single-subject brain. NeuroImage 15(1):273–289

    Article  Google Scholar 

  37. Van MDH, Sporns O (2011) Rich-club organization of the human connectome. J Neurosci 31(44):15775–15786

    Article  Google Scholar 

  38. Wang JH, Zuo X, He Y (2010) Graph-based network analysis of resting-state functional MRI. Front Syst Neurosci 4(16):16

    Google Scholar 

  39. Wang X, Ren YS, Zhang WS (2017) Multi-task fused lasso metllod for constructing dynamic functional brain network of resting-state fMRI. J Image Graph 22(7):0978–0987

    Google Scholar 

  40. Wang SH, Du SD, Atangana A, Liu AJ, Lu ZY (2018) Application of stationary wavelet entropy in pathological brain detection. Multimedia Tools Appl 77(3):3701–3714

    Article  Google Scholar 

  41. Wang SH, Phillips P, Sui Y, Liu B, Yang M, Cheng H (2018) Classification of Alzheimer's disease based on eight-layer convolutional neural network with leaky rectified linear unit and max pooling. J Med Syst 42(5):85

    Article  Google Scholar 

  42. Wee CY, Yang S, Yap PT, Shen D (2016) Sparse temporally dynamic resting-state functional connectivity networks for early MCI identification. Brain Imaging Behav 10(2):342–356

    Article  Google Scholar 

  43. Yang M, Zhang Y, Li JW, Zou L, Lu SY, Liu B, Yang JQ, Zhang YD (2016) Detection of left-sided and right-sided hearing loss via fractional Fourier transform. Entropy 18(5):194

    Article  Google Scholar 

  44. Yao ZQ, Shang KK, Xu XK (2012) Fundamental statistics of weighted networks. J Univ Shanghai Sci Technol 34(1):18–26

    Google Scholar 

  45. Zhang YD, Wang SH (2015) Detection of Alzheimer's disease by displacement field and machine learning. Peerj 3(s1):e1251

    Article  Google Scholar 

  46. Zhang YD, Dong ZC, Phillips P, Wang SH, Ji GL, Yang JQ, Yuan TF (2015) Detection of subjects and brain regions related to Alzheimer's disease using 3D MRI scans based on eigenbrain and machine learning. Front Comput Neurosci 9:66

    Google Scholar 

  47. Zhang YD, Wang SD, Phillips P, Dong ZC, Ji GL, Yang JQ (2015) Detection of Alzheimer's disease and mild cognitive impairment based on structural volumetric MR images using 3D-DWT and WTA-KSVM trained by PSOTVAC. Biomed Signal Process Control 21:58–73

    Article  Google Scholar 

  48. Zhang YD, Chen XQ, Zhan TM, Jiao ZQ, Sun Y, Chen ZM, Yao Y, Fang LT, Lv YD, Wang SH (2016) Fractal dimension estimation for developing pathological brain detection system based on Minkowski-Bouligand method. IEEE Access 4:5937–5947

    Article  Google Scholar 

  49. Zhang YD, Yang JQ, Yang JF, Liu AJ, Sun P (2016) A novel compressed sensing method for magnetic resonance imaging: exponential wavelet iterative shrinkage-thresholding algorithm with random shift. Int J Biomed Imaging 3:1–10

    Article  Google Scholar 

  50. Zhang YD, Wang SH, Phillips P, Yang JQ, Yuan TF (2016) Three-dimensional eigenbrain for the detection of subjects and brain regions related with Alzheimer’s disease. J Alzheimers Dis 50(4):1163–1179

    Article  Google Scholar 

  51. Zhang YD, Yang M, Wang SH (2017) Two-level iterative compressed sensing for cardiovascular magnetic resonance imaging. J Am Coll Cardiol 70(16):C167

    Article  Google Scholar 

  52. Zhang GH, Liang GY, Li WZ, Fang J, Wang JB, Geng YY, Wang JY (2017) Learning convolutional ranking-score function by query preference regularization. Lect Notes Comput Sci 10585:1–8

  53. Zhang Y, Zhang H, Chen XB, Lee SW, Shen DG (2017) Hybrid high-order functional connectivity networks using resting-state functional MRI for mild cognitive impairment diagnosis. Sci Rep 7(1):6530

    Article  Google Scholar 

  54. Zhou S, Mondragon RJ (2003) The rich-club phenomenon in the internet topology. IEEE Commun Lett 8(3):180–182

    Article  Google Scholar 

  55. Zhou XX, Zhang YD, Ji GL, Yang JQ, Dong ZC, Wang SH, Zhang GS, Phillips P (2016) Detection of abnormal MR brains based on wavelet entropy and feature selection. IEEJ Trans Electr Electron Eng 11(3):364–373

    Article  Google Scholar 

Download references

Acknowledgements

The authors would like to thank the reviewers and the editors for their valuable comments and suggestions on improving this paper. This work is supported by the National Natural Science Foundation of China (No. 51307010), the Natural Science Foundation of Jiangsu Province and the University Natural Science Research Program of Jiangsu Province (No. 17KJB510003).

Author information

Authors and Affiliations

Authors

Contributions

ZJ and HW conceived of the study and contributed to the manuscript. SW contributed to the resting-state functional networks analysis. YC and LZ contributed to the fMRI experimental design and analysis. All authors read and approved the final manuscript.

Corresponding authors

Correspondence to Ling Zou or Shuihua Wang.

Ethics declarations

Conflict of interest

We have no conflicts of interest to disclose with regard to the subject matter of this paper.

Additional information

Publisher’s note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Jiao, Z., Wang, H., Cai, M. et al. Rich club characteristics of dynamic brain functional networks in resting state. Multimed Tools Appl 79, 15075–15093 (2020). https://doi.org/10.1007/s11042-018-6424-4

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11042-018-6424-4

Keywords

Navigation