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Abnormal rich club organization and impaired correlation between structural and functional connectivity in migraine sufferers

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Abstract

Because of the unique position of the topologically central role of densely interconnected brain hubs, our study aimed to investigate whether these regions and their related connections would be particularly vulnerable to migraine. In our study, we explored the rich club structure and its role in global functional dynamics in 30 patients with migraine without aura and 30 healthy controls. DTI and resting fMRI were used to construct structural connectivity (SC) and functional connectivity (FC) networks. An independent replication data set of 26 patients and 26 controls was included to replicate and validate significant findings. As compared with the controls, the structural networks of patients exhibited altered rich club organization with higher level of feeder connection density, abnormal small-world organization with increased global efficiency and decreased strength of SC-FC coupling. As these abnormal topological properties and headache attack duration exhibited a significant association with increased density of feeder connections, our results indicated that migraine may be characterized by a selective alteration of the structural connectivity of the rich club regions, tending to have higher ‘bridgeness’ with non-rich club regions, which may increase the integration among pain-related brain circuits with more excitability but less inhibition for the modulation of migraine.

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References

  • Achard, S., & Bullmore, E. (2007). Efficiency and cost of economical brain functional networks. PLoS Computational Biology, 3(2), e17.

    Article  PubMed  PubMed Central  Google Scholar 

  • Achard, S., Salvador, R., Whitcher, B., Suckling, J., & Bullmore, E. (2006). A resilient, low-frequency, small-world human brain functional network with highly connected association cortical hubs. Journal of Neuroscience, 26(1), 63–72.

    Article  CAS  PubMed  Google Scholar 

  • Alexander-Bloch, A. F., Vértes, P. E., Stidd, R., Lalonde, F., Clasen, L., Rapoport, J., et al. (2012). The anatomical distance of functional connections predicts brain network topology in health and schizophrenia. Cerebral Cortex, 23, 127–138.

    Article  PubMed  PubMed Central  Google Scholar 

  • Antal, A., & Paulus, W. (2011). A case of refractory orofacial pain treated by transcranial direct current stimulation applied over hand motor area in combination with NMDA agonist drug intake. Brain Stimulation, 4(2), 117–121.

    Article  PubMed  Google Scholar 

  • Apkarian, A. V., Baliki, M. N., & Geha, P. Y. (2009). Towards a theory of chronic pain. Progress in Neurobiology, 87(2), 81–97.

    Article  PubMed  Google Scholar 

  • Apkarian, A. V., Hashmi, J. A., & Baliki, M. N. (2011). Pain and the brain: specificity and plasticity of the brain in clinical chronic pain. Pain, 152(3), S49–S64.

    Article  PubMed  Google Scholar 

  • Bai, F., Shu, N., Yuan, Y., Shi, Y., Yu, H., Wu, D., et al. (2012). Topologically convergent and divergent structural connectivity patterns between patients with remitted geriatric depression and amnestic mild cognitive impairment. Journal of Neuroscience, 32(12), 4307–4318.

    Article  CAS  PubMed  Google Scholar 

  • Bashir, A., Lipton, R. B., Ashina, S., & Ashina, M. (2013). Migraine and structural changes in the brain A systematic review and meta-analysis. Neurology, 81(14), 1260–1268.

    Article  PubMed  PubMed Central  Google Scholar 

  • Bingel, U., Schoell, E., Herken, W., Büchel, C., & May, A. (2007). Habituation to painful stimulation involves the antinociceptive system. Pain, 131(1), 21–30.

    Article  CAS  PubMed  Google Scholar 

  • Borsook, D., Upadhyay, J., Chudler, E. H., & Becerra, L. (2010). A key role of the basal ganglia in pain and analgesia-insights gained through human functional imaging. Molecular Pain, 6(1), 27.

    PubMed  PubMed Central  Google Scholar 

  • Borsook, D., Maleki, N., Becerra, L., & McEwen, B. (2012). Understanding migraine through the lens of maladaptive stress responses: a model disease of allostatic load. Neuron, 73(2), 219–234.

    Article  CAS  PubMed  Google Scholar 

  • Brummitt, C. D., D’Souza, R. M., & Leicht, E. (2012). Suppressing cascades of load in interdependent networks. Proceedings of the National Academy of Sciences of the United States of America, 109(12), E680–E689.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bullmore, E., & Sporns, O. (2012). The economy of brain network organization. Nature Reviews Neuroscience, 13(5), 336–349.

    CAS  PubMed  Google Scholar 

  • Bullmore, E. T., Suckling, J., Overmeyer, S., Rabe-Hesketh, S., Taylor, E., & Brammer, M. J. (1999). Global, voxel, and cluster tests, by theory and permutation, for a difference between two groups of structural MR images of the brain. IEEE T Medical Imaging, 18(1), 32–42.

    Article  CAS  Google Scholar 

  • Cavada, C., Tejedor, J., Cruz-Rizzolo, R. J., & Reinoso-Suárez, F. (2000). The anatomical connections of the macaque monkey orbitofrontal cortex. a review. Cerebral Cortex, 10(3), 220–242.

    Article  CAS  PubMed  Google Scholar 

  • Colizza, V., Flammini, A., Serrano, M. A., & Vespignani, A. (2006). Detecting rich-club ordering in complex networks. Nature Physics, 2(2), 110–115.

    Article  CAS  Google Scholar 

  • Collin, G., Sporns, O., Mandl, R. C., & van den Heuvel, M. P. (2014). Structural and functional aspects relating to cost and benefit of rich club organization in the human cerebral cortex. Cerebral Cortex, 24(9), 2258–2267.

    Article  PubMed  Google Scholar 

  • Crossley, N. A., Mechelli, A., Vértes, P. E., Winton-Brown, T. T., Patel, A. X., Ginestet, C. E., et al. (2013). Cognitive relevance of the community structure of the human brain functional coactivation network. Proceedings of the National Academy of Sciences of the United States of America, 110(28), 11583–11588.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Crossley, N. A., Mechelli, A., Scott, J., Carletti, F., Fox, P. T., McGuire, P., et al. (2014). The hubs of the human connectome are generally implicated in the anatomy of brain disorders. Brain, 137(8), 2382–2395.

    Article  PubMed  PubMed Central  Google Scholar 

  • DaSilva, A. F., Mendonca, M. E., Zaghi, S., Lopes, M., DosSantos, M. F., Spierings, E. L., et al. (2012). tDCS‐induced analgesia and electrical fields in pain‐related neural networks in chronic migraine. Headache, 52(8), 1283–1295.

    Article  PubMed  PubMed Central  Google Scholar 

  • Draganski, B., Kherif, F., Klöppel, S., Cook, P. A., Alexander, D. C., Parker, G. J., et al. (2008). Evidence for segregated and integrative connectivity patterns in the human basal ganglia. Journal of Neuroscience, 28(28), 7143–7152.

    Article  CAS  PubMed  Google Scholar 

  • Fair, D. A., Nigg, J. T., Iyer, S., Bathula, D., Mills, K. L., Dosenbach, N. U., et al. (2012). Distinct neural signatures detected for ADHD subtypes after controlling for micro-movements in resting state functional connectivity MRI data. Frontiers in Systems Neuroscience, 6, 80.

    PubMed  Google Scholar 

  • Gong, G., He, Y., Concha, L., Lebel, C., Gross, D. W., Evans, A. C., et al. (2009a). Mapping anatomical connectivity patterns of human cerebral cortex using in vivo diffusion tensor imaging tractography. Cerebral Cortex, 19(3), 524–536.

    Article  PubMed  Google Scholar 

  • Gong, G., Rosa-Neto, P., Carbonell, F., Chen, Z. J., He, Y., & Evans, A. C. (2009b). Age-and gender-related differences in the cortical anatomical network. Journal of Neuroscience, 29(50), 15684–15693.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hagmann, P., Cammoun, L., Gigandet, X., Meuli, R., Honey, C. J., Wedeen, V. J., et al. (2008). Mapping the structural core of human cerebral cortex. PLoS Biology, 6(7), e159.

    Article  PubMed  PubMed Central  Google Scholar 

  • Irfanoglu, M. O., Walker, L., Sarlls, J., Marenco, S., & Pierpaoli, C. (2012). Effects of image distortions originating from susceptibility variations and concomitant fields on diffusion MRI tractography results. NeuroImage, 61(1), 275–288.

    Article  PubMed  Google Scholar 

  • Kong, J., & Charlestown, M. (2015). Neuromodulation of conditioned placebo/nocebo in heat pain: anodal vs. cathodal transcranial direct current stimulation to the right dorsolateral prefrontal cortex. doi:10.1097/j.pain.0000000000000163.

  • Leemans, A., & Jones, D. K. (2009). The B‐matrix must be rotated when correcting for subject motion in DTI data. Magnetic Resonance in Medicine, 61(6), 1336–1349.

    Article  PubMed  Google Scholar 

  • Liu, J., Lan, L., Li, G., Yan, X., Nan, J., Xiong, S., et al. (2013a). Migraine-related gray matter and white matter changes at a 1-year follow-up evaluation. The Journal of Pain, 14(12), 1703–1708.

    Article  PubMed  Google Scholar 

  • Liu, J., Zhao, L., Nan, J., Li, G., Xiong, S., von Deneen, K. M., et al. (2013b). The trade-off between wiring cost and network topology in white matter structural networks in health and migraine. Experimental Neurology, 248, 196–204.

    Article  PubMed  Google Scholar 

  • Liu, J., Lan, L., Mu, J., Zhao, L., Yuan, K., Zhang, Y., et al. (2015a). Genetic contribution of catechol‐O‐methyltransferase in hippocampal structural and functional changes of female migraine sufferers. Human Brain Mapping, 36(5), 1782–1795.

    Article  PubMed  Google Scholar 

  • Liu, J., Zhao, L., Lei, F., Zhang, Y., Yuan, K., Gong, Q., et al. (2015b). Disrupted resting‐state functional connectivity and its changing trend in migraine suffers. Human Brain Mapping, 36(5), 1892–1907.

    Article  PubMed  Google Scholar 

  • Loher, T., Burgunder, J., Weber, S., Sommerhalder, R., & Krauss, J. (2002). Effect of chronic pallidal deep brain stimulation on off period dystonia and sensory symptoms in advanced Parkinson’s disease. Journal of Neurology, Neurosurgery & Psychiatry, 73(4), 395–399.

    Article  CAS  Google Scholar 

  • Maleki, N., Becerra, L., Nutile, L., Pendse, G., Brawn, J., Bigal, M., et al. (2011). Migraine attacks the basal ganglia. Molecular Pain, 7(71), 8069–8067.

    Google Scholar 

  • May, A. (2009). New insights into headache: an update on functional and structural imaging findings. Nature Reviews Neurology, 5(4), 199–209.

    Article  PubMed  Google Scholar 

  • Mori, S., & van Zijl, P. (2002). Fiber tracking: principles and strategies—a technical review. NMR in Biomedicine, 15(7–8), 468–480.

    Article  PubMed  Google Scholar 

  • Newman, M. E. (2006). Modularity and community structure in networks. Proceedings of the National Academy of Sciences of the United States of America, 103(23), 8577–8582.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Nitsche, M. A., Cohen, L. G., Wassermann, E. M., Priori, A., Lang, N., Antal, A., et al. (2008). Transcranial direct current stimulation: state of the art 2008. Brain Stimulation, 1(3), 206–223.

    Article  PubMed  Google Scholar 

  • 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.

    Article  PubMed  Google Scholar 

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

    Article  PubMed  Google Scholar 

  • Rule, R. R., Shimamura, A. P., & Knight, R. T. (2002). Orbitofrontal cortex and dynamic filtering of emotional stimuli. Cognitive, Affective, & Behavioral Neuroscience, 2(3), 264–270.

    Article  Google Scholar 

  • Schwedt, T. J., Chiang, C.-C., Chong, C. D., & Dodick, D. W. (2015). Functional MRI of migraine. The Lancet Neurology, 14(1), 81–91.

    Article  PubMed  Google Scholar 

  • Senden, M., Deco, G., de Reus, M. A., Goebel, R., & van den Heuvel, M. P. (2014). Rich club organization supports a diverse set of functional network configurations. NeuroImage, 96, 174–182.

    Article  PubMed  Google Scholar 

  • Shu, N., Liu, Y., Li, K., Duan, Y., Wang, J., Yu, C., et al. (2011). Diffusion tensor tractography reveals disrupted topological efficiency in white matter structural networks in multiple sclerosis. Cerebral Cortex, 21(11), 2565–2577.

    Article  PubMed  Google Scholar 

  • Sporns, O., Tononi, G., & Kötter, R. (2005). The human connectome: a structural description of the human brain. PLoS Computational Biology, 1(4), e42.

    Article  PubMed  PubMed Central  Google Scholar 

  • Supekar, K., Uddin, L. Q., Prater, K., Amin, H., Greicius, M. D., & Menon, V. (2010). Development of functional and structural connectivity within the default mode network in young children. NeuroImage, 52(1), 290–301.

    Article  PubMed  PubMed Central  Google Scholar 

  • Tomasi, D., Wang, G. J., & Volkow, N. D. (2013). Energetic cost of brain functional connectivity. Proceedings of the National Academy of Sciences of the United States of America, 110(33), 13642–13647.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tzourio-Mazoyer, N., Landeau, B., Papathanassiou, D., Crivello, F., Etard, O., Delcroix, N., et al. (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  CAS  PubMed  Google Scholar 

  • van den Heuvel, M. P., & Sporns, O. (2011). Rich-club organization of the human connectome. Journal of Neuroscience, 31(44), 15775–15786.

    Article  PubMed  Google Scholar 

  • van den Heuvel, M. P., & Sporns, O. (2013). An anatomical substrate for integration among functional networks in human cortex. Journal of Neuroscience, 33(36), 14489–14500.

    Article  PubMed  Google Scholar 

  • van den Heuvel, M. P., Kahn, R. S., Goñi, J., & Sporns, O. (2012). High-cost, high-capacity backbone for global brain communication. Proceedings of the National Academy of Sciences of the United States of America, 109(28), 11372–11377.

    Article  PubMed  PubMed Central  Google Scholar 

  • van den Heuvel, M. P., Sporns, O., Collin, G., Scheewe, T., Mandl, R. C., Cahn, W., et al. (2013). Abnormal rich club organization and functional brain dynamics in schizophrenia. JAMA Psychiatry, 70(8), 783–792.

    Article  PubMed  Google Scholar 

  • Watts, D. J., & Strogatz, S. H. (1998). Collective dynamics of ‘small-world’ networks. Nature, 393(6684), 440–442.

    Article  CAS  PubMed  Google Scholar 

  • Weiland, B. J., Boutros, N. N., Moran, J. M., Tepley, N., & Bowyer, S. M. (2008). Evidence for a frontal cortex role in both auditory and somatosensory habituation: a MEG study. NeuroImage, 42(2), 827–835.

    Article  PubMed  PubMed Central  Google Scholar 

  • Xia, M., Wang, J., & He, Y. (2013). BrainNet Viewer: a network visualization tool for human brain connectomics. PLoS One, 8(7), e68910.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yuan, K., Zhao, L., Cheng, P., Yu, D., Zhao, L., Dong, T., et al. (2013). Altered structure and resting-state functional connectivity of the basal ganglia in migraine patients without aura. The Journal of Pain, 14(8), 836–844.

    Article  PubMed  Google Scholar 

  • Zalesky, A., Fornito, A., & Bullmore, E. T. (2010). Network-based statistic: identifying differences in brain networks. NeuroImage, 53(4), 1197–1207.

    Article  PubMed  Google Scholar 

  • Zhang, Z., Liao, W., Chen, H., Mantini, D., Ding, J.-R., Xu, Q., et al. (2011). Altered functional–structural coupling of large-scale brain networks in idiopathic generalized epilepsy. Brain, 134(10), 2912–2928.

    Article  PubMed  Google Scholar 

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Acknowledgments

This work was supported by the National Natural Science Foundation of China under Grant Nos. 81471737, 81571640, and 81371530; and the Basic and Cutting-edge Research (plan) Project of Commission of Science and Technology, Chong Qing (cstc2014jcyjA10120); and the Medical Scientific Research (plan) Project of Health and Family Planning Commission of Chong Qing (2012-2-187) (20142089).

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Correspondence to Jixin Liu or Ming Zhang.

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Kang Li, Lijun Liu, Qin Yin, Wanghuan Dun, Xiaolin Xu, Jixin Liu, Ming Zhang declare that they have no conflict of interest.

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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.

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Li, K., Liu, L., Yin, Q. et al. Abnormal rich club organization and impaired correlation between structural and functional connectivity in migraine sufferers. Brain Imaging and Behavior 11, 526–540 (2017). https://doi.org/10.1007/s11682-016-9533-6

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