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Reduced hemispheric asymmetry of brain anatomical networks in attention deficit hyperactivity disorder

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Abstract

Despite many studies reporting a variety of alterations in brain networks in patients with attention deficit hyperactivity disorder (ADHD), alterations in hemispheric anatomical networks are still unclear. In this study, we investigated topology alterations in hemispheric white matter in patients with ADHD and the relationship between these alterations and clinical features of the illness. Weighted hemispheric brain anatomical networks were first constructed for each of 40 right-handed patients with ADHD and 53 matched normal controls. Then, graph theoretical approaches were utilized to compute hemispheric topological properties. The small-world property was preserved in the hemispheric network. Furthermore, a significant group-by-hemisphere interaction was revealed in global efficiency, local efficiency and characteristic path length, attributed to the significantly reduced hemispheric asymmetry of global and local integration in patients with ADHD compared with normal controls. Specifically, reduced asymmetric regional efficiency was found in three regions. Finally, we found that the abnormal asymmetry of hemispheric brain anatomical network topology and regional efficiency were both associated with clinical features (the Adult ADHD Self-Report Scale and Wechsler Adult Intelligence Scale) in patients. Our findings provide new insights into the lateralized nature of hemispheric dysconnectivity and highlight the potential for using brain network measures of hemispheric asymmetry as neural biomarkers for ADHD and its clinical features.

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References

  • Achard, S., & Bullmore, E. (2007). Efficiency and cost of economical brain functional networks. PLoS Computational Biology, 3(2), e17. https://doi.org/10.1371/journal.pcbi.0030017.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ahmadlou, M., Adeli, H., & Adeli, A. (2012). Graph theoretical analysis of organization of functional brain networks in ADHD. Clinical EEG and Neuroscience, 43(1), 5–13. https://doi.org/10.1177/1550059411428555.

    Article  PubMed  Google Scholar 

  • Amunts, K., Jäncke, L., Mohlberg, H., Steinmetz, H., & Zilles, K. (2000). Interhemispheric asymmetry of the human motor cortex related to handedness and gender. Neuropsychologia, 38(3), 304–312.

    Article  CAS  Google Scholar 

  • Angelica, D. L. F., Xia, S., Craig, B., & Li, X. (2013). A review of attention-deficit/hyperactivity disorder from the perspective of brain networks. Frontiers in Human Neuroscience, 7(4), 192.

    Google Scholar 

  • Arthur, W. T., & Paul, M. T. (2003). Mapping brain asymmetry. Nature Reviews. Neuroscience, 4(1), 37–48.

    Article  Google Scholar 

  • Ashtari, M., Kumra, S., Bhaskar, S. L., Clarke, T., Thaden, E., Cervellione, K. L., et al. (2005). Attention-deficit/hyperactivity disorder: a preliminary diffusion tensor imaging study. Biological Psychiatry, 57(5), 448–455. https://doi.org/10.1016/j.biopsych.2004.11.047.

    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  Google Scholar 

  • Barkley R. A. (1994). Impaired delayed responding: a unified theory of attention-deficit hyperactivity disorder. Disruptive behavior disorders in children: Essays in honor of Herbert Quay (pp. 11–57). New York: Plenum Press.

  • Barkley, R. A. (2003). Issues in the diagnosis of attention-deficit/hyperactivity disorder in children. Brain & Development, 25(2), 77–83.

    Article  Google Scholar 

  • Barrick, T. R., Mackay, C. E., Prima, S., Maes, F., Vandermeulen, D., Crow, T. J., et al. (2005). Automatic analysis of cerebral asymmetry: an exploratory study of the relationship between brain torque and planum temporale asymmetry. NeuroImage, 24(3), 678–691.

    Article  Google Scholar 

  • Barrick, T. R., Lawes, I. N., Mackay, C. E., & Clark, C. A. (2007). White matter pathway asymmetry underlies functional lateralization. Cerebral Cortex, 17(3), 591–598. https://doi.org/10.1093/cercor/bhk004.

    Article  PubMed  Google Scholar 

  • Beare, R., Adamson, C., Bellgrove, M. A., Vilgis, V., Vance, A., Seal, M. L., et al. (2017). Altered structural connectivity in ADHD: a network based analysis. Brain Imaging and Behavior, 11(3), 846–858. https://doi.org/10.1007/s11682-016-9559-9.

    Article  PubMed  Google Scholar 

  • Boccaletti, S., Latora, V., Moreno, Y., Chavez, M., & Hwang, D. (2006). Complex networks: Structure and dynamics. Physics Reports, 424(4–5), 175–308. https://doi.org/10.1016/j.physrep.2005.10.009.

    Article  Google Scholar 

  • Booth, J. R., Wood, L., Lu, D., Houk, J. C., & Bitan, T. (2007). The role of the basal ganglia and cerebellum in language processing. Brain Research, 1133(1), 136–144.

    Article  CAS  Google Scholar 

  • Buchel, C., Raedler, T., Sommer, M., Sach, M., Weiller, C., & Koch, M. A. (2004). White matter asymmetry in the human brain: a diffusion tensor MRI study. Cerebral Cortex, 14(9), 945–951. https://doi.org/10.1093/cercor/bhh055.

    Article  CAS  PubMed  Google Scholar 

  • Bullmore, E., & Sporns, O. (2009). Complex brain networks: graph theoretical analysis of structural and functional systems. Nature Reviews Neuroscience, 10(3), 186.

    Article  CAS  Google Scholar 

  • Cabeza, R. (2002). Hemispheric asymmetry reduction in older adults: the HAROLD model. Psychology and Aging, 17, 85–100.

    Article  Google Scholar 

  • Cao, Y., Whalen, S., Huang, J., Berger, K. L., & DeLano, M. C. (2003). Asymmetry of subinsular anisotropy by in vivo diffusion tensor imaging. Human Brain Mapping, 20(2), 82–90. https://doi.org/10.1002/hbm.10130.

    Article  PubMed  PubMed Central  Google Scholar 

  • Cao, X., Cao, Q., Long, X., Sun, L., Sui, M., Zhu, C., et al. (2009). Abnormal resting-state functional connectivity patterns of the putamen in medication-naive children with attention deficit hyperactivity disorder. Brain Research, 1303, 195–206. https://doi.org/10.1016/j.brainres.2009.08.029.

    Article  CAS  PubMed  Google Scholar 

  • Cao, Q., Shu, N., An, L., Wang, P., Sun, L., Xia, M. R., et al. (2013). Probabilistic diffusion tractography and graph theory analysis reveal abnormal white matter structural connectivity networks in drug-naive boys with attention deficit/hyperactivity disorder. The Journal of Neuroscience, 33(26), 10676–10687. https://doi.org/10.1523/JNEUROSCI.4793-12.2013.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Casey, B. J., Castellanos, F. X., Giedd, J. N., Marsh, W. L., Hamburger, S. D., Schubert, A. B., et al. (1997). Implication of right frontostriatal circuitry in response inhibition and attention-deficit/hyperactivity disorder. Journal of the American Academy of Child and Adolescent Psychiatry, 36(3), 374–383.

    Article  CAS  Google Scholar 

  • Casey, B. J., Epstein, J. N., Buhle, J., Liston, C., Davidson, M. C., Tonev, S. T., et al. (2007). Frontostriatal connectivity and its role in cognitive control in parent-child dyads with ADHD. American Journal of Psychiatry, 164(11), 1729–1736.

    Article  CAS  Google Scholar 

  • Castellanos, F. X., Giedd, J. N., Berquin, P. C., Walter, J. M., Sharp, W., Tran, T., et al. (1996). Quantitative brain magnetic resonance imaging in girls with attention-deficit/hyperactivity disorder. Archives of General Psychiatry, 53(7), 607.

    Article  CAS  Google Scholar 

  • Chandana, S. R., Behen, M. E., Juhász, C., Muzik, O., Rothermel, R. D., Mangner, T. J., et al. (2005). Significance of abnormalities in developmental trajectory and asymmetry of cortical serotonin synthesis in autism. International Journal of Developmental Neuroscience, 23(2–3), 171–182.

    Article  CAS  Google Scholar 

  • Chang, C., Crottaz-Herbette, S., & Menon, V. (2007). Temporal dynamics of basal ganglia response and connectivity during verbal working memory. NeuroImage, 34(3), 1253–1269.

    Article  Google Scholar 

  • Cherkasova, M. V., & Hechtman, L. (2009). Neuroimaging in attention-deficit hyperactivity disorder: beyond the frontostriatal circuitry. Canadian Journal of Psychiatry Revue Canadienne De Psychiatrie, 54(10), 651–664.

    Article  Google Scholar 

  • Conturo, T. E., Lori, N. F., Cull, T. S., Akbudak, E., Snyder, A. Z., Shimony, J. S., et al. (1999). Tracking neuronal fiber pathways in the living human brain. Proceedings of the National Academy of Sciences of the United States of America, 96(18), 10422–10427.

    Article  CAS  Google Scholar 

  • Cortese, S., Kelly, C., Chabernaud, C., Proal, E., Di Martino, A., Milham, M. P., et al. (2012). Toward systems neuroscience of ADHD: a meta-analysis of 55 fMRI studies. The American Journal of Psychiatry, 169(10), 1038–1055. https://doi.org/10.1176/appi.ajp.2012.11101521.

    Article  PubMed  Google Scholar 

  • Cui, Z., Zhong, S., Xu, P., He, Y., & Gong, G. (2013). PANDA: a pipeline toolbox for analyzing brain diffusion images. Frontiers in Human Neuroscience, 7, 42. https://doi.org/10.3389/fnhum.2013.00042.

    Article  PubMed  PubMed Central  Google Scholar 

  • Derflinger, S., Sorg, C., Gaser, C., Myers, N., Arsic, M., Kurz, A., et al. (2011). Grey-matter atrophy in Alzheimer's disease is asymmetric but not lateralized. Journal of Alzheimers Disease Jad, 25(2), 347.

    Article  CAS  Google Scholar 

  • Dolcosa, F., Ricea, H. J., & Cabeza, R. (2002). Hemispheric asymmetry and aging right hemisphere decline or asymmetry reduction. Neuroscience and Biobehavioral Reviews, 26, 819–825.

    Article  Google Scholar 

  • Filipek, P. A., Semrudclikeman, M., Steingard, R. J., Renshaw, P. F., Kennedy, D. N., & Biederman, J. (1997). Volumetric MRI analysis comparing subjects having attention-deficit hyperactivity disorder with normal controls. Neurology, 48(3), 589–601.

    Article  CAS  Google Scholar 

  • Galaburda, A. M., Sanides, F., & Geschwind, N. (1978). Human brain: Cytoarchitectonic left–right asymmetries in the temporal speech region. Archives of Neurology, 35(12), 812–817.

    Article  CAS  Google Scholar 

  • Giedd, J. N., Castellanos, F. X., Casey, B. J., Kozuch, P., King, A. C., Hamburger, S. D., et al. (1994). Quantitative morphology of the corpus callosum in attention deficit hyperactivity disorder. The American Journal of Psychiatry, 151(5), 665–669.

    Article  CAS  Google Scholar 

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

    Article  Google Scholar 

  • Good, C. D., Johnsrude, I., Ashburner, J., Henson, R. N., Friston, K. J., & Frackowiak, R. S. (2001). Cerebral asymmetry and the effects of sex and handedness on brain structure: a voxel-based morphometric analysis of 465 normal adult human brains. NeuroImage, 14(3), 685–700. https://doi.org/10.1006/nimg.2001.0857.

    Article  CAS  PubMed  Google Scholar 

  • Griffa, A., Baumann, P. S., Thiran, J. P., & Hagmann, P. (2013). Structural connectomics in brain diseases. NeuroImage, 80(20), 515–526.

    Article  Google Scholar 

  • Hale, T. S., McCracken, J. T., McGough, J. J., Smalley, S. L., Phillips, J. M., & Zaidel, E. (2005). Impaired linguistic processing and atypical brain laterality in adults with ADHD. Clinical Neuroscience Research, 5(5–6), 255–263. https://doi.org/10.1016/j.cnr.2005.09.006.

    Article  Google Scholar 

  • Hale, T. S., Smalley, S. L., Dang, J., Hanada, G., Macion, J., McCracken, J. T., et al. (2010). ADHD familial loading and abnormal EEG alpha asymmetry in children with ADHD. Journal of Psychiatric Research, 44(9), 605–615. https://doi.org/10.1016/j.jpsychires.2009.11.012.

    Article  PubMed  Google Scholar 

  • Hamilton, L. S., Narr, K. L., Luders, E., Szeszko, P. R., Thompson, P. M., Bilder, R. M., et al. (2007). Asymmetries of cortical thickness: effects of handedness, sex, and schizophrenia. Neuroreport, 18(14), 1427–1431.

    Article  Google Scholar 

  • Hart, H., Radua, J., Nakao, T., Mataix-Cols, D., & Rubia, K. (2013). Meta-analysis of functional magnetic resonance imaging studies of inhibition and attention in attention-deficit/hyperactivity disorder: exploring task-specific, stimulant medication, and age effects. JAMA Psychiatry, 70(2), 185.

    Article  Google Scholar 

  • He, Y., & Evans, A. (2010). Graph theoretical modeling of brain connectivity. Current Opinion in Neurology, 23(4), 341–350.

    PubMed  Google Scholar 

  • Hynd, G. W., Hern, K. L., Novey, E. S., Eliopulos, D., Marshall, R., Gonzalez, J. J., et al. (1993). Attention Deficit- Hyperactivity Disorder and Asymmetry of the Caudate Nucleus. Journal of Child Neurology, 8(4), 339.

    Article  CAS  Google Scholar 

  • Iturria-Medina, Y., Perez Fernandez, A., Morris, D. M., Canales-Rodriguez, E. J., Haroon, H. A., Garcia Penton, L., et al. (2011). Brain hemispheric structural efficiency and interconnectivity rightward asymmetry in human and nonhuman primates. Cerebral Cortex, 21(1), 56–67. https://doi.org/10.1093/cercor/bhq058.

    Article  PubMed  Google Scholar 

  • Jenkinson, M., Bannister, P., Brady, M., & Smith, S. (2002). Improved Optimization for the Robust and Accurate Linear Registration and Motion Correction of Brain Images. NeuroImage, 17(2), 825–841.

    Article  Google Scholar 

  • Jones, K. E., Craver-Lemley, C., & Barrett, A. M. (2008). Asymmetrical visual-spatial attention in college students diagnosed with ADD/ADHD. Cognitive and Behavioral Neurology, 21(3), 176–178. https://doi.org/10.1097/WNN.0b013e318185e6a9.

    Article  PubMed  PubMed Central  Google Scholar 

  • Joseph, R. M., Fricker, Z., Fenoglio, A., Lindgren, K. A., Knaus, T. A., & Tager-Flusberg, H. (2014). Structural asymmetries of language-related gray and white matter and their relationship to language function in young children with ASD. Brain Imaging and Behavior, 8(1), 60–72. https://doi.org/10.1007/s11682-013-9245-0.

    Article  PubMed  Google Scholar 

  • Konrad, K., & Eickhoff, S. B. (2010). Is the ADHD brain wired differently? A review on structural and functional connectivity in attention deficit hyperactivity disorder. Human Brain Mapping, 31(6), 904–916. https://doi.org/10.1002/hbm.21058.

    Article  PubMed  Google Scholar 

  • Konrad, A., Dielentheis, T. F., El Masri, D., Bayerl, M., Fehr, C., Gesierich, T., et al. (2010). Disturbed structural connectivity is related to inattention and impulsivity in adult attention deficit hyperactivity disorder. The European Journal of Neuroscience, 31(5), 912–919. https://doi.org/10.1111/j.1460-9568.2010.07110.x.

    Article  PubMed  Google Scholar 

  • Kubicki, M., Westin, C. F., Maier, S. E., Frumin, M., Nestor, P. G., Salisbury, D. F., et al. (2002). Uncinate Fasciculus Findings in Schizophrenia: A Magnetic Resonance Diffusion Tensor Imaging Study. American Journal of Psychiatry, 159(5), 813.

    Article  Google Scholar 

  • Kubicki, M., Westin, C. F., Nestor, P. G., Wible, C. G., Frumin, M., Maier, S. E., et al. (2003). Cingulate fasciculus integrity disruption in schizophrenia: a magnetic resonance diffusion tensor imaging study. Biological Psychiatry, 54(11), 1171–1180.

    Article  Google Scholar 

  • Kulynych, J. J., Vladar, K., Jones, D. W., & Weinberger, D. R. (1994). Gender differences in the normal lateralization of the supratemporal cortex: MRI surface-rendering morphometry of Heschl's gyrus and the planum temporale. Cerebral Cortex, 4(2), 107–118.

    Article  CAS  Google Scholar 

  • Lancaster, J. L., Kochunov, P. V., Thompson, P. M., Toga, A. W., & Fox, P. T. (2003). Asymmetry of the brain surface from deformation field analysis. Human Brain Mapping, 19(2), 79.

    Article  Google Scholar 

  • Langleben, D. D., Austin, G., Krikorian, G., Ridlehuber, H. W., Goris, M. L., & Strauss, H. W. (2001). Interhemispheric asymmetry of regional cerebral blood flow in prepubescent boys with attention deficit hyperactivity disorder. Nuclear Medicine Communications, 22(12), 1333.

    Article  CAS  Google Scholar 

  • Lawes, I. N. C., Barrick, T. R., Murugam, V., Spierings, N., Evans, D. R., Song, M., et al. (2008). Atlas-based segmentation of white matter tracts of the human brain using diffusion tensor tractography and comparison with classical dissection. NeuroImage, 39(1), 62–79.

    Article  Google Scholar 

  • Liu, T., Chen, Y., Lin, P., & Wang, J. (2015). Small-World Brain Functional Networks in Children With Attention-Deficit/Hyperactivity Disorder Revealed by EEG Synchrony. Clinical EEG and Neuroscience, 46(3), 183–191. https://doi.org/10.1177/1550059414523959.

    Article  PubMed  Google Scholar 

  • Lo, C. Y., Wang, P. N., Chou, K. H., Wang, J., He, Y., & Lin, C. P. (2010). Diffusion tensor tractography reveals abnormal topological organization in structural cortical networks in Alzheimer's disease. The Journal of Neuroscience, 30(50), 16876–16885. https://doi.org/10.1523/JNEUROSCI.4136-10.2010.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Makris, N., Buka, S. L., Biederman, J., Papadimitriou, G. M., Hodge, S. M., Valera, E. M., et al. (2008). Attention and executive systems abnormalities in adults with childhood ADHD: A DT-MRI study of connections. Cerebral Cortex, 18(5), 1210.

    Article  Google Scholar 

  • McAlonan, G. M., Cheung, V., Cheung, C., Chua, S. E., Murphy, D. G., Suckling, J., et al. (2007). Mapping brain structure in attention deficit-hyperactivity disorder: a voxel-based MRI study of regional grey and white matter volume. Psychiatry Research, 154(2), 171–180. https://doi.org/10.1016/j.pscychresns.2006.09.006.

    Article  PubMed  Google Scholar 

  • McGlone, & Jeannette. (1980). Sex differences in human brain asymmetry: a critical survey. Behavioral & Brain Sciences, 3(2), 215–227.

    Article  Google Scholar 

  • Mori, S., Crain, B. J., Chacko, V. P., & Vanzijl, P. C. (1999). Three-dimensional tracking of axonal projections in the brain by magnetic resonance imaging. Annals of Neurology, 45(2), 265.

    Article  CAS  Google Scholar 

  • Mori, S., Kaufmann, W. E., Davatzikos, C., Stieltjes, B., Amodei, L., Fredericksen, K., et al. (2002). Imaging cortical association tracts in the human brain using diffusion-tensor-based axonal tracking. Magnetic Resonance in Medicine, 47(2), 215–223.

    Article  Google Scholar 

  • Murphy, K. R., Barkley, R. A., & Bush, T. (2001). Executive functioning and olfactory identification in young adults with attention deficit-hyperactivity disorder. Neuropsychology, 15(2), 211–220. https://doi.org/10.1037/0894-4105.15.2.211.

    Article  CAS  PubMed  Google Scholar 

  • Olesen, P. J., Westerberg, H., & Klingberg, T. (2004). Increased prefrontal and parietal activity after training of working memory. Nature Neuroscience, 7(1), 75–79. https://doi.org/10.1038/nn1165.

    Article  CAS  PubMed  Google Scholar 

  • Overmeyer, S., Bullmore, E. T., Suckling, J., Simmons, A., Williams, S. C. R., Santosh, P. J., et al. (2001). Distributed grey and white matter deficits in hyperkinetic disorder: MRI evidence for anatomical abnormality in an attentional network. Psychological Medicine, 31(08). https://doi.org/10.1017/s0033291701004706.

  • Park, H. J., Westin, C. F., Kubicki, M., Maier, S. E., Niznikiewicz, M., Baer, A., et al. (2004). White matter hemisphere asymmetries in healthy subjects and in schizophrenia: a diffusion tensor MRI study. NeuroImage, 23(1), 213–223.

    Article  Google Scholar 

  • Parker, G. J., Luzzi, S., Alexander, D. C., Wheeler-Kingshott, C. A., Ciccarelli, O., & Lambon Ralph, M. A. (2005). Lateralization of ventral and dorsal auditory-language pathways in the human brain. NeuroImage, 24(3), 656–666.

    Article  Google Scholar 

  • Poldrack, R. A., & Gorgolewski, K. J. (2017). OpenfMRI: Open sharing of task fMRI data. Neuroimage, 144(Pt B), 259–261. https://doi.org/10.1016/j.neuroimage.2015.05.073.

    Article  PubMed  Google Scholar 

  • Poldrack, R. A., Barch, D. M., Mitchell, J. P., Wager, T. D., Wagner, A. D., Devlin, J. T., et al. (2013). Toward open sharing of task-based fMRI data: the OpenfMRI project. Frontiers in Neuroinformatics, 7, 12. https://doi.org/10.3389/fninf.2013.00012.

    Article  PubMed  PubMed Central  Google Scholar 

  • Puetz, V. B., Parker, D., Kohn, N., Dahmen, B., Verma, R., & Konrad, K. (2017). Altered brain network integrity after childhood maltreatment: A structural connectomic DTI-study. Human Brain Mapping, 38(2), 855–868. https://doi.org/10.1002/hbm.23423.

    Article  CAS  PubMed  Google Scholar 

  • Pujol, J., López-Sala, A., Deus, J., Cardoner, N., Sebastián-Gallés, N., Conesa, G., et al. (2002). The Lateral Asymmetry of the Human Brain Studied by Volumetric Magnetic Resonance Imaging. NeuroImage, 17(2), 670–679. https://doi.org/10.1006/nimg.2002.1203.

    Article  PubMed  Google Scholar 

  • Qiu, M. G., Ye, Z., Li, Q. Y., Liu, G. J., Xie, B., & Wang, J. (2011). Changes of brain structure and function in ADHD children. Brain Topography, 24(3–4), 243–252. https://doi.org/10.1007/s10548-010-0168-4.

    Article  PubMed  Google Scholar 

  • Ratnarajah, N., RifkinGraboi, A., Fortier, M. V., Chong, Y. S., Kwek, K., Saw, S., et al. (2013). Structural Connectivity Asymmetry in the Neonatal Brain. NeuroImage, 75(1), 187.

    Article  Google Scholar 

  • Rubia, K., Overmeyer, S., Taylor, E., Brammer, M., Williams, S. C. R., Simmons, A., et al. (1999). Hypofrontality in attention deficit hyperactivity disorder during higher-order motor control_ a study with functional MRI. The American Journal of Psychiatry, 156(6).

  • Rubia, K., Smith, A. B., Brammer, M. J., Toone, B., & Taylor, E. (2005). Abnormal brain activation during inhibition and error detection in medication-naive adolescents with ADHD. The American Journal of Psychiatry, 162(6), 1067–1075.

    Article  Google Scholar 

  • Rubinov, M., & Sporns, O. (2010). Complex network measures of brain connectivity: uses and interpretations. NeuroImage, 52(3), 1059–1069. https://doi.org/10.1016/j.neuroimage.2009.10.003.

    Article  PubMed  Google Scholar 

  • Rudie, J. D., Brown, J. A., Beck-Pancer, D., Hernandez, L. M., Dennis, E. L., Thompson, P. M., et al. (2012). Altered functional and structural brain network organization in autism. NeuroImage: Clinical, 2, 79–94. https://doi.org/10.1016/j.nicl.2012.11.006.

    Article  CAS  Google Scholar 

  • Sailer, M., Fischl, B., Salat, D., Tempelmann, C., Schönfeld, M. A., Busa, E., et al. (2003). Focal thinning of the cerebral cortex in multiple sclerosis. Brain: A Journal of Neurology, 126(8), 1734–1744.

    Article  Google Scholar 

  • Schneider, M. F., Krick, C. M., Retz, W., Hengesch, G., Retz-Junginger, P., Reith, W., et al. (2010). Impairment of fronto-striatal and parietal cerebral networks correlates with attention deficit hyperactivity disorder (ADHD) psychopathology in adults - a functional magnetic resonance imaging (fMRI) study. Psychiatry Research, 183(1), 75–84. https://doi.org/10.1016/j.pscychresns.2010.04.005.

    Article  PubMed  Google Scholar 

  • Schweitzer, J. B., Lee, D. O., Hanford, R. B., Zink, C. F., Ely, T. D., Tagamets, M. A., et al. (2004). Effect of methylphenidate on executive functioning in adults with attention-deficit/hyperactivity disorder: normalization of behavior but not related brain activity. Biological Psychiatry, 56(8), 597–606.

    Article  CAS  Google Scholar 

  • Shaw, P., Lalonde, F., Lepage, C., Rabin, C., Eckstrand, K., Sharp, W., et al. (2009). Development of cortical asymmetry in typically developing children and its disruption in attention-deficit/hyperactivity disorder. Archives of General Psychiatry, 66(8), 888.

    Article  Google Scholar 

  • Shaywitz, B. A., Shaywltz, S. E., Pugh, K. R., Constable, R. T., Skudlarski, P., Fulbright, R. K., et al. (1995). Sex differences in the functional organization of the brain for language. Nature, 373(6515), 607.

    Article  CAS  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. https://doi.org/10.1093/cercor/bhr039.

    Article  PubMed  Google Scholar 

  • Sidlauskaite, J., Caeyenberghs, K., Sonuga-Barke, E., Roeyers, H., & Wiersema, J. R. (2015). Whole-brain structural topology in adult attention-deficit/hyperactivity disorder: Preserved global - disturbed local network organization. NeuroImage: Clinical, 9, 506–512. https://doi.org/10.1016/j.nicl.2015.10.001.

    Article  Google Scholar 

  • Sigalovsky, I. S., Fischl, B., & Melcher, J. R. (2006). Mapping an intrinsic MR property of gray matter in auditory cortex of living humans: a possible marker for primary cortex and hemispheric differences. NeuroImage, 32(4), 1524–1537. https://doi.org/10.1016/j.neuroimage.2006.05.023.

    Article  PubMed  PubMed Central  Google Scholar 

  • Silk, T. J., Vilgis, V., Adamson, C., Chen, J., Smit, L., Vance, A., et al. (2016). Abnormal asymmetry in frontostriatal white matter in children with attention deficit hyperactivity disorder. Brain Imaging and Behavior, 10(4), 1080–1089. https://doi.org/10.1007/s11682-015-9470-9.

    Article  PubMed  Google Scholar 

  • Smith, A. B., Taylor, E., Brammer, M., Halari, R., & Rubia, K. (2008). Reduced activation in right lateral prefrontal cortex and anterior cingulate gyrus in medication-naïve adolescents with attention deficit hyperactivity disorder during time discrimination. Journal of Child Psychology & Psychiatry, 49(9), 977–985.

    Article  Google Scholar 

  • Song, J. W., P, M., Kolasinski, J., Ellen Grant, P., Galaburda, A. M., & Takahashi, E. (2014). Asymmetry of white matter pathways in developing human brains. Cerebral Cortex, 25(19), 2883–2893.

    PubMed  Google Scholar 

  • Sowell, E. R., Thompson, P. M., Welcome, S. E., Henkenius, A. L., Toga, A. W., & Peterson, B. S. (2003). Cortical abnormalities in children and adolescents with attention-deficit hyperactivity disorder. Lancet, 362(9397), 1699–1707.

    Article  Google Scholar 

  • Sporns, O. (2011). The human connectome: a complex network. Annals of the New York Academy of Sciences, 1224, 109–125. https://doi.org/10.1111/j.1749-6632.2010.05888.x.

    Article  PubMed  Google Scholar 

  • Sun, Y., Chen, Y., Collinson, S. L., Bezerianos, A., & Sim, K. (2017). Reduced hemispheric asymmetry of brain anatomical networks is linked to schizophrenia: A connectome study. Cerebral Cortex, 27(1), 602–615. https://doi.org/10.1093/cercor/bhv255.

    Article  PubMed  Google Scholar 

  • Suskauer, S. J., Simmonds, D. J., Caffo, B. S., et al. (2008). fMRI of intrasubject variability in ADHD: anomalous premotor activity with prefrontal compensation. Journal of the American Academy of Child & Adolescent Psychiatry, 47(10), 1141–1150.

  • Takao, H., Abe, O., Yamasue, H., Aoki, S., Sasaki, H., Kasai, K., et al. (2011). Gray and white matter asymmetries in healthy individuals aged 21–29 years: A voxel-based morphometry and diffusion tensor imaging study. Human Brain Mapping, 32(10), 1762–1773.

    Article  Google Scholar 

  • Tamm, L., Menon, V., & Reiss, A. L. (2006). Parietal attentional system aberrations during target detection in adolescents with attention deficit hyperactivity disorder: event-related fMRI evidence. The American Journal of Psychiatry, 163(6), 1033–1043.

    Article  Google Scholar 

  • Team. (2000). Functional frontalisation with age: mapping neurodevelopmental trajectories with fMRI. Neuroscience & Biobehavioral Reviews, 24(1), 13–19.

    Article  Google Scholar 

  • Thiebaut, d. S. M., Ffytche, D. H., Bizzi, A., Dell'Acqua, F., Allin, M., Walshe, M., et al. (2011). Atlasing location, asymmetry and inter-subject variability of white matter tracts in the human brain with MR diffusion tractography. NeuroImage, 54(1), 49–59. https://doi.org/10.1016/j.neuroimage.2010.07.055.

    Article  Google Scholar 

  • Thompson, P. M., Moussai, J., Zohoori, S., Goldkorn, A., Khan, A. A., Mega, M. S., et al. (1998). Cortical variability and asymmetry in normal aging and Alzheimer's disease. Cerebral Cortex (New York, N.Y. : 1991), 8(6), 492–509.

    Article  CAS  Google Scholar 

  • Tian, L., Wang, J., Yan, C., & He, Y. (2011). Hemisphere- and gender-related differences in small-world brain networks: a resting-state functional MRI study. NeuroImage, 54(1), 191–202. https://doi.org/10.1016/j.neuroimage.2010.07.066.

    Article  PubMed  Google Scholar 

  • Tzouriomazoyer, 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  Google Scholar 

  • Wang, L., Zhu, C., He, Y., Zang, Y., Cao, Q., Zhang, H., et al. (2009). Altered small-world brain functional networks in children with attention-deficit/hyperactivity disorder. Human Brain Mapping, 30(2), 638–649. https://doi.org/10.1002/hbm.20530.

    Article  CAS  PubMed  Google Scholar 

  • Watkins, K. E., Paus, T., Lerch, J. P., Zijdenbos, A., Collins, D. L., Neelin, P., et al. (2001). Structural asymmetries in the human brain: a voxel-based statistical analysis of 142 MRI scans. Cerebral Cortex, 11(9), 868–877.

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Wu, J., Yan, T., Zhen, Z., Jin, F., & Guo, Q. (2012). Retinotopic mapping of the peripheral visual field to human visual cortex by functional magnetic resonance imaging. Human Brain Mapping, 33(7), 1727–1740.

    Article  Google Scholar 

  • Xia, M., Wang, J., & Yong, H. (2013). BrainNet Viewer: A Network Visualization Tool for Human Brain Connectomics. PLoS One, 8(7), e68910.

    Article  CAS  Google Scholar 

  • Xia, S., Foxe, J. J., Sroubek, A. E., Branch, C., & Li, X. (2014). Topological organization of the “small-world” visual attention network in children with attention deficit/hyperactivity disorder (ADHD). Frontiers in Human Neuroscience, 8(8), 162.

    PubMed  PubMed Central  Google Scholar 

  • Yan, T., Jin, F., He, J., & Wu, J. (2011). Development of a wide-view visual presentation system for visual retinotopic mapping during functional MRI. Journal of Magnetic Resonance Imaging, 33(2), 441.

    Article  Google Scholar 

  • Yan, T., Geng, Y., Wu, J., & Li, C. (2015). Interactions between multisensory inputs with voluntary spatial attention: an fMRI study. Neuroreport, 26(11), 605–612.

    Article  Google Scholar 

  • Yan, T., Feng, Y., Liu, T., Wang, L., Mu, N., Dong, X., et al. (2017). Theta oscillations related to orientation recognition in unattended condition: A vMMN study. Frontiers in Behavioral Neuroscience, 11, 166.

    Article  Google Scholar 

  • Yan, T., Dong, X., Mu, N., Liu, T., Chen, D., Deng, L., et al. (2018). Positive Classification Advantage: Tracing the Time Course Based on Brain Oscillation. Frontiers in Human Neuroscience, 11, 659.

    Article  Google Scholar 

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Funding

This work was supported by the National Natural Science Foundation of China (61503272, 61503273, 61741212), the Natural Science Foundation of Shanxi (2015021090, 201601D202042) and the project funded by the China Postdoctoral Science Foundation (2016 M601287), the Shanxi Provincial Foundation for Returned Scholars, China (2016–037), the Scientific Research Foundation for Returned Overseas Chinese Scholars (20151098-2), the Key Research and Development Project in Shanxi (201603D111014), the Foundation for Youths of Taiyuan University of Technology (2015QN025).

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Correspondence to Bin Wang.

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The author(s) declared no potential conflicts of interest with respect to the research, authorship, and/or publication of this article.

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The study was carried out in strict accordance with the University of California, Los Angeles Institutional Review Board.

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After receiving a thorough explanation, all participants gave written informed consent according to the procedures approved by the University of California Los Angeles Institutional Review Board.

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Dandan Li and Ting Li are first co-author.

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Li, D., Li, T., Niu, Y. et al. Reduced hemispheric asymmetry of brain anatomical networks in attention deficit hyperactivity disorder. Brain Imaging and Behavior 13, 669–684 (2019). https://doi.org/10.1007/s11682-018-9881-5

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