Abstract
Despite convergent evidence suggesting that schizophrenia is a disorder of brain dysconnectivity, it remains unclear whether intra- or inter-hemispheric deficits or their combination underlie the dysconnection. This study examined the source of the functional dysconnection in schizophrenia. Resting-state fMRI was performed in 66 patients with schizophrenia and 73 matched healthy controls. Functional brain networks were constructed for each participant and further partitioned into intra- and inter-hemispheric connections. We examined how schizophrenia altered the intra-hemispheric topological properties and the inter-hemispheric nodal strength. Although several subcortical and cingulate regions exhibited hemispheric-independent aberrations of regional efficiency, the optimal small-world properties in the hemispheric networks and their lateralization were preserved in patients. A significant deficit in the inter-hemispheric connectivity was revealed in most of the hub regions, leading to an inter-hemispheric hypo-connectivity pattern in patients. These abnormal intra- and inter-hemispheric network organizations were associated with the clinical features of schizophrenia. The patients in the present study received different medications. These findings provide new insights into the nature of dysconnectivity in schizophrenia, highlighting the dissociable processes between the preserved intra-hemispheric network topology and altered inter-hemispheric functional connectivity.
Similar content being viewed by others
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.
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. The Journal of Neuroscience, 26(1), 63–72. https://doi.org/10.1523/JNEUROSCI.3874-05.2006.
Alexander-Bloch, A. F., Gogtay, N., Meunier, D., Birn, R., Clasen, L., Lalonde, F., Lenroot, R., Giedd, J., & Bullmore, E. T. (2010). Disrupted modularity and local connectivity of brain functional networks in childhood-onset schizophrenia. Frontiers in Systems Neuroscience, 4, 147. https://doi.org/10.3389/fnsys.2010.00147.
Alexander-Bloch, A. F., Vertes, P. E., Stidd, R., Lalonde, F., Clasen, L., Rapoport, J., et al. (2013). The anatomical distance of functional connections predicts brain network topology in health and schizophrenia. Cerebral Cortex, 23(1), 127–138. https://doi.org/10.1093/cercor/bhr388.
Ananth, H., Popescu, I., Critchley, H. D., Good, C. D., Frackowiak, R. S., & Dolan, R. J. (2002). Cortical and subcortical gray matter abnormalities in schizophrenia determined through structural magnetic resonance imaging with optimized volumetric voxel-based morphometry. The American Journal of Psychiatry, 159(9), 1497–1505. https://doi.org/10.1176/appi.ajp.159.9.1497.
Anderson, J. S., Druzgal, T. J., Lopez-Larson, M., Jeong, E. K., Desai, K., & Yurgelun-Todd, D. (2011). Network anticorrelations, global regression, and phase-shifted soft tissue correction. Human Brain Mapping, 32(6), 919–934. https://doi.org/10.1002/hbm.21079.
Arslan, S., Ktena, S. I., Makropoulos, A., Robinson, E. C., Rueckert, D., & Parisot, S. (2017). Human brain mapping: A systematic comparison of parcellation methods for the human cerebral cortex. Neuroimage, 170, 5–30. https://doi.org/10.1016/j.neuroimage.2017.04.014.
Artiges, E., Martinot, J. L., Verdys, M., Attar-Levy, D., Mazoyer, B., Tzourio, N., Giraud, M. J., & Paillere-Martinot, M. L. (2000). Altered hemispheric functional dominance during word generation in negative schizophrenia. Schizophrenia Bulletin, 26(3), 709–721.
Bai, F., Shu, N., Yuan, Y., Shi, Y., Yu, H., Wu, D., Wang, J., Xia, M., He, Y., & Zhang, Z. (2012). Topologically convergent and divergent structural connectivity patterns between patients with remitted geriatric depression and amnestic mild cognitive impairment. The Journal of Neuroscience, 32(12), 4307–4318. https://doi.org/10.1523/JNEUROSCI.5061-11.2012.
Bassett, D. S., Nelson, B. G., Mueller, B. A., Camchong, J., & Lim, K. O. (2012). Altered resting state complexity in schizophrenia. Neuroimage, 59(3), 2196–2207. https://doi.org/10.1016/j.neuroimage.2011.10.002.
Bleich-Cohen, M., Hendler, T., Kotler, M., & Strous, R. D. (2009). Reduced language lateralization in first-episode schizophrenia: An fMRI index of functional asymmetry. Psychiatry Research, 171(2), 82–93. https://doi.org/10.1016/j.pscychresns.2008.03.002.
Bullmore, E., & Sporns, O. (2009). Complex brain networks: Graph theoretical analysis of structural and functional systems. Nature Reviews. Neuroscience, 10(3), 186–198. https://doi.org/10.1038/nrn2575.
Butler, P. D., Silverstein, S. M., & Dakin, S. C. (2008). Visual perception and its impairment in schizophrenia. Biological Psychiatry, 64(1), 40–47. https://doi.org/10.1016/j.biopsych.2008.03.023.
Cocchi, L., Harding, I. H., Lord, A., Pantelis, C., Yucel, M., & Zalesky, A. (2014). Disruption of structure-function coupling in the schizophrenia connectome. Neuroimage Clinical, 4, 779–787. https://doi.org/10.1016/j.nicl.2014.05.004.
Collin, G., Kahn, R. S., de Reus, M. A., Cahn, W., & van den Heuvel, M. P. (2014). Impaired rich club connectivity in unaffected siblings of schizophrenia patients. Schizophrenia Bulletin, 40(2), 438–448. https://doi.org/10.1093/schbul/sbt162.
Collinson, S. L., Mackay, C. E., O, J., James, A. C., & Crow, T. J. (2009). Dichotic listening impairments in early onset schizophrenia are associated with reduced left temporal lobe volume. Schizophrenia Research, 112(1–3), 24–31. https://doi.org/10.1016/j.schres.2009.03.034.
Crespo-Facorro, B., Nopoulos, P. C., Chemerinski, E., Kim, J. J., Andreasen, N. C., & Magnotta, V. (2004). Temporal pole morphology and psychopathology in males with schizophrenia. Psychiatry Research, 132(2), 107–115. https://doi.org/10.1016/j.pscychresns.2004.09.002.
Damoiseaux, J. S., & Greicius, M. D. (2009). Greater than the sum of its parts: A review of studies combining structural connectivity and resting-state functional connectivity. Brain Structure & Function, 213(6), 525–533. https://doi.org/10.1007/s00429-009-0208-6.
David, A. S., Malmberg, A., Brandt, L., Allebeck, P., & Lewis, G. (1997). IQ and risk for schizophrenia: A population-based cohort study. Psychological Medicine, 27(6), 1311–1323.
Ellison-Wright, I., & Bullmore, E. (2009). Meta-analysis of diffusion tensor imaging studies in schizophrenia. Schizophrenia Research, 108(1–3), 3–10. https://doi.org/10.1016/j.schres.2008.11.021.
Fornito, A., Yoon, J., Zalesky, A., Bullmore, E. T., & Carter, C. S. (2011). General and specific functional connectivity disturbances in first-episode schizophrenia during cognitive control performance. Biological Psychiatry, 70(1), 64–72. https://doi.org/10.1016/j.biopsych.2011.02.019.
Fornito, A., Zalesky, A., Pantelis, C., & Bullmore, E. T. (2012). Schizophrenia, neuroimaging and connectomics. Neuroimage, 62(4), 2296–2314. https://doi.org/10.1016/j.neuroimage.2011.12.090.
Fox, M. D., & Raichle, M. E. (2007). Spontaneous fluctuations in brain activity observed with functional magnetic resonance imaging. Nature Reviews. Neuroscience, 8(9), 700–711. https://doi.org/10.1038/nrn2201.
Friston, K., Brown, H. R., Siemerkus, J., & Stephan, K. E. (2016). The dysconnection hypothesis (2016). Schizophrenia Research, 176(2–3), 83–94. https://doi.org/10.1016/j.schres.2016.07.014.
Gotts, S. J., Jo, H. J., Wallace, G. L., Saad, Z. S., Cox, R. W., & Martin, A. (2013). Two distinct forms of functional lateralization in the human brain. Proceedings of the National Academy of Sciences of the United States of America, 110(36), E3435–E3444. https://doi.org/10.1073/pnas.1302581110.
Guo, S., Kendrick, K. M., Zhang, J., Broome, M., Yu, R., Liu, Z., & Feng, J. (2013). Brain-wide functional inter-hemispheric disconnection is a potential biomarker for schizophrenia and distinguishes it from depression. Neuroimage Clinical, 2, 818–826. https://doi.org/10.1016/j.nicl.2013.06.008.
Guo, W., Xiao, C., Liu, G., Wooderson, S. C., Zhang, Z., Zhang, J., Yu, L., & Liu, J. (2014). Decreased resting-state interhemispheric coordination in first-episode, drug-naive paranoid schizophrenia. Progress in Neuro-Psychopharmacology & Biological Psychiatry, 48, 14–19. https://doi.org/10.1016/j.pnpbp.2013.09.012.
Gur, R. E., Turetsky, B. I., Cowell, P. E., Finkelman, C., Maany, V., Grossman, R. I., Arnold, S. E., Bilker, W. B., & Gur, R. C. (2000). Temporolimbic volume reductions in schizophrenia. Archives of General Psychiatry, 57(8), 769–775.
Hagmann, P., Cammoun, L., Gigandet, X., Meuli, R., Honey, C. J., Wedeen, V. J., & Sporns, O. (2008). Mapping the structural core of human cerebral cortex. PLoS Biology, 6(7), e159. https://doi.org/10.1371/journal.pbio.0060159.
He, Y., & Evans, A. (2010). Graph theoretical modeling of brain connectivity. Current Opinion in Neurology, 23(4), 341–350. https://doi.org/10.1097/WCO.0b013e32833aa567.
He, Y., Chen, Z., & Evans, A. (2008). Structural insights into aberrant topological patterns of large-scale cortical networks in Alzheimer's disease. The Journal of Neuroscience, 28(18), 4756–4766. https://doi.org/10.1523/JNEUROSCI.0141-08.2008.
He, Y., Wang, J., Wang, L., Chen, Z. J., Yan, C., Yang, H., Tang, H., Zhu, C., Gong, Q., Zang, Y., & Evans, A. C. (2009). Uncovering intrinsic modular organization of spontaneous brain activity in humans. PLoS One, 4(4), e5226. https://doi.org/10.1371/journal.pone.0005226.
Hoffman, R. E., Fernandez, T., Pittman, B., & Hampson, M. (2011). Elevated functional connectivity along a corticostriatal loop and the mechanism of auditory/verbal hallucinations in patients with schizophrenia. Biological Psychiatry, 69(5), 407–414. https://doi.org/10.1016/j.biopsych.2010.09.050.
Honey, C. J., Sporns, O., Cammoun, L., Gigandet, X., Thiran, J. P., Meuli, R., & Hagmann, P. (2009). Predicting human resting-state functional connectivity from structural connectivity. Proceedings of the National Academy of Sciences of the United States of America, 106(6), 2035–2040. https://doi.org/10.1073/pnas.0811168106.
Hoptman, M. J., Zuo, X. N., D'Angelo, D., Mauro, C. J., Butler, P. D., Milham, M. P., & Javitt, D. C. (2012). Decreased interhemispheric coordination in schizophrenia: A resting state fMRI study. Schizophrenia Research, 141(1), 1–7. https://doi.org/10.1016/j.schres.2012.07.027.
Howes, O. D., & Murray, R. M. (2014). Schizophrenia: an integrated sociodevelopmental-cognitive model. Lancet, 383(9929), 1677–1687. https://doi.org/10.1016/S0140-6736(13)62036-X.
Humphries, M. D., Gurney, K., & Prescott, T. J. (2006). The brainstem reticular formation is a small-world, not scale-free, network. Proceedings of the Biological Sciences, 273(1585), 503–511. https://doi.org/10.1098/rspb.2005.3354.
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.
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.
Kasai, K., Shenton, M. E., Salisbury, D. F., Onitsuka, T., Toner, S. K., Yurgelun-Todd, D., Kikinis, R., Jolesz, F. A., & McCarley, R. W. (2003). Differences and similarities in insular and temporal pole MRI gray matter volume abnormalities in first-episode schizophrenia and affective psychosis. Archives of General Psychiatry, 60(11), 1069–1077. https://doi.org/10.1001/archpsyc.60.11.1069.
Kay, S. R., Fiszbein, A., & Opler, L. A. (1987). The positive and negative syndrome scale (PANSS) for schizophrenia. Schizophrenia Bulletin, 13(2), 261–276.
Langer, N., Pedroni, A., Gianotti, L. R., Hänggi, J., Knoch, D., & Jäncke, L. (2012). Functional brain network efficiency predicts intelligence. Human Brain Mapping, 33(6), 1393–1406.
Latora, V., & Marchiori, M. (2001). Efficient behavior of small-world networks. Physical Review Letters, 87(19), 198701. https://doi.org/10.1103/PhysRevLett.87.198701.
Liu, H., Liu, Z., Liang, M., Hao, Y., Tan, L., Kuang, F., Yi, Y., Xu, L., & Jiang, T. (2006). Decreased regional homogeneity in schizophrenia: A resting state functional magnetic resonance imaging study. Neuroreport, 17(1), 19–22.
Liu, Y., Liang, M., Zhou, Y., He, Y., Hao, Y., Song, M., Yu, C., Liu, H., Liu, Z., & Jiang, T. (2008). Disrupted small-world networks in schizophrenia. Brain, 131(Pt 4), 945–961. https://doi.org/10.1093/brain/awn018.
Lynall, M. E., Bassett, D. S., Kerwin, R., McKenna, P. J., Kitzbichler, M., Muller, U., & Bullmore, E. (2010). Functional connectivity and brain networks in schizophrenia. The Journal of Neuroscience, 30(28), 9477–9487. https://doi.org/10.1523/JNEUROSCI.0333-10.2010.
Maslov, S., & Sneppen, K. (2002). Specificity and stability in topology of protein networks. Science, 296(5569), 910–913. https://doi.org/10.1126/science.1065103.
Mesholam-Gately, R. I., Giuliano, A. J., Goff, K. P., Faraone, S. V., & Seidman, L. J. (2009). Neurocognition in first-episode schizophrenia: A meta-analytic review. Neuropsychology, 23(3), 315–336. https://doi.org/10.1037/a0014708.
Mesulam, M. M. (1998). From sensation to cognition. Brain, 121(Pt 6), 1013–1052.
Navari, S., & Dazzan, P. (2009). Do antipsychotic drugs affect brain structure? A systematic and critical review of MRI findings. Psychological Medicine, 39(11), 1763–1777. https://doi.org/10.1017/S0033291709005315.
Olson, I. R., Plotzker, A., & Ezzyat, Y. (2007). The enigmatic temporal pole: A review of findings on social and emotional processing. Brain, 130(Pt 7), 1718–1731. https://doi.org/10.1093/brain/awm052.
Pettersson-Yeo, W., Allen, P., Benetti, S., McGuire, P., & Mechelli, A. (2011). Dysconnectivity in schizophrenia: Where are we now? Neuroscience and Biobehavioral Reviews, 35(5), 1110–1124. https://doi.org/10.1016/j.neubiorev.2010.11.004.
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.
Razafimandimby, A., Maiza, O., Herve, P. Y., Lecardeur, L., Delamillieure, P., Brazo, P., et al. (2007). Stability of functional language lateralization over time in schizophrenia patients. Schizophrenia Research, 94(1–3), 197–206. https://doi.org/10.1016/j.schres.2007.04.011.
Repovs, G., Csernansky, J. G., & Barch, D. M. (2011). Brain network connectivity in individuals with schizophrenia and their siblings. Biological Psychiatry, 69(10), 967–973. https://doi.org/10.1016/j.biopsych.2010.11.009.
Ribolsi, M., Koch, G., Magni, V., Di Lorenzo, G., Rubino, I. A., Siracusano, A., & Centonze, D. (2009). Abnormal brain lateralization and connectivity in schizophrenia. Reviews in the Neurosciences, 20(1), 61–70.
Rimol, L. M., Hartberg, C. B., Nesvag, R., Fennema-Notestine, C., Hagler Jr., D. J., Pung, C. J., et al. (2010). Cortical thickness and subcortical volumes in schizophrenia and bipolar disorder. Biological Psychiatry, 68(1), 41–50. https://doi.org/10.1016/j.biopsych.2010.03.036.
Rubinov, M., & Bullmore, E. (2013). Schizophrenia and abnormal brain network hubs. Dialogues in Clinical Neuroscience, 15(3), 339–349.
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.
Rubinov, M., Knock, S. A., Stam, C. J., Micheloyannis, S., Harris, A. W., Williams, L. M., & Breakspear, M. (2009). Small-world properties of nonlinear brain activity in schizophrenia. Human Brain Mapping, 30(2), 403–416. https://doi.org/10.1002/hbm.20517.
Salvador, R., Sarro, S., Gomar, J. J., Ortiz-Gil, J., Vila, F., Capdevila, A., et al. (2010). Overall brain connectivity maps show cortico-subcortical abnormalities in schizophrenia. Human Brain Mapping, 31(12), 2003–2014. https://doi.org/10.1002/hbm.20993.
Shapleske, J., Rossell, S. L., Chitnis, X. A., Suckling, J., Simmons, A., Bullmore, E. T., et al. (2002). A computational morphometric MRI study of schizophrenia: Effects of hallucinations. Cerebral Cortex, 12(12), 1331–1341.
Shenton, M. E., Dickey, C. C., Frumin, M., & McCarley, R. W. (2001). A review of MRI findings in schizophrenia. Schizophrenia Research, 49(1–2), 1–52.
Skudlarski, P., Jagannathan, K., Anderson, K., Stevens, M. C., Calhoun, V. D., Skudlarska, B. A., & Pearlson, G. (2010). Brain connectivity is not only lower but different in schizophrenia: A combined anatomical and functional approach. Biological Psychiatry, 68(1), 61–69. https://doi.org/10.1016/j.biopsych.2010.03.035.
Smith, S. M., Miller, K. L., Salimi-Khorshidi, G., Webster, M., Beckmann, C. F., Nichols, T. E., Ramsey, J. D., & Woolrich, M. W. (2011). Network modelling methods for FMRI. Neuroimage, 54(2), 875–891. https://doi.org/10.1016/j.neuroimage.2010.08.063.
Sommer, I., Ramsey, N., Kahn, R., Aleman, A., & Bouma, A. (2001). Handedness, language lateralisation and anatomical asymmetry in schizophrenia: Meta-analysis. The British Journal of Psychiatry, 178, 344–351.
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.
Sporns, O., & Zwi, J. D. (2004). The small world of the cerebral cortex. Neuroinformatics, 2(2), 145–162. https://doi.org/10.1385/NI:2:2:145.
Stephan, K. E., Friston, K. J., & Frith, C. D. (2009). Dysconnection in schizophrenia: From abnormal synaptic plasticity to failures of self-monitoring. Schizophrenia Bulletin, 35(3), 509–527. https://doi.org/10.1093/schbul/sbn176.
Sun, Y., Yin, Q., Fang, R., Yan, X., Wang, Y., Bezerianos, A., Tang, H., Miao, F., & Sun, J. (2014). Disrupted functional brain connectivity and its association to structural connectivity in amnestic mild cognitive impairment and Alzheimer's disease. PLoS One, 9(5), e96505. https://doi.org/10.1371/journal.pone.0096505.
Sun, Y., Chen, Y., Collinson, S. L., Bezerianos, A., & Sim, K. (2017a). 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.
Sun, Y., Dai, Z., Li, J., Collinson, S. L., & Sim, K. (2017b). Modular-level alterations of structure-function coupling in schizophrenia connectome. Human Brain Mapping, 38(4), 2008–2025. https://doi.org/10.1002/hbm.23501.
Sun, Y., Li, J., Suckling, J., & Feng, L. (2017c). Asymmetry of hemispheric network topology reveals dissociable processes between functional and structural brain connectome in community-living elders. Frontiers in Aging Neuroscience, 9, 361. https://doi.org/10.3389/fnagi.2017.00361.
Thompson, S. A., Patterson, K., & Hodges, J. R. (2003). Left/right asymmetry of atrophy in semantic dementia: Behavioral-cognitive implications. Neurology, 61(9), 1196–1203.
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.
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. https://doi.org/10.1006/nimg.2001.0978.
van den Heuvel, M. P., & Fornito, A. (2014). Brain networks in schizophrenia. Neuropsychology Review, 24(1), 32–48. https://doi.org/10.1007/s11065-014-9248-7.
van den Heuvel, M. P., Stam, C. J., Kahn, R. S., & Hulshoff Pol, H. E. (2009). Efficiency of functional brain networks and intellectual performance. The Journal of Neuroscience, 29(23), 7619–7624. https://doi.org/10.1523/JNEUROSCI.1443-09.2009.
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. https://doi.org/10.1001/jamapsychiatry.2013.1328.
Van Dijk, K. R., Sabuncu, M. R., & Buckner, R. L. (2012). The influence of head motion on intrinsic functional connectivity MRI. Neuroimage, 59(1), 431–438. https://doi.org/10.1016/j.neuroimage.2011.07.044.
van Erp, T. G., Hibar, D. P., Rasmussen, J. M., Glahn, D. C., Pearlson, G. D., Andreassen, O. A., et al. (2016). Subcortical brain volume abnormalities in 2028 individuals with schizophrenia and 2540 healthy controls via the ENIGMA consortium. Molecular Psychiatry, 21(4), 585. https://doi.org/10.1038/mp.2015.118.
Wang, L., Metzak, P. D., Honer, W. G., & Woodward, T. S. (2010). Impaired efficiency of functional networks underlying episodic memory-for-context in schizophrenia. The Journal of Neuroscience, 30(39), 13171–13179. https://doi.org/10.1523/JNEUROSCI.3514-10.2010.
Wang, Z., Dai, Z., Gong, G., Zhou, C., & He, Y. (2015). Understanding structural-functional relationships in the human brain: A large-scale network perspective. Neuroscientist, 21(3), 290–305. https://doi.org/10.1177/1073858414537560.
Wang, X., Zhang, Y., Long, Z., Zheng, J., Zhang, Y., Han, S., et al. (2017). Frequency-specific alteration of functional connectivity density in antipsychotic-naive adolescents with early-onset schizophrenia. Journal of Psychiatric Research, 95, 68–75.
Watts, D. J., & Strogatz, S. H. (1998). Collective dynamics of 'small-world' networks. Nature, 393(6684), 440–442. https://doi.org/10.1038/30918.
Wu, K., Taki, Y., Sato, K., Kinomura, S., Goto, R., Okada, K., Kawashima, R., He, Y., Evans, A. C., & Fukuda, H. (2012). Age-related changes in topological organization of structural brain networks in healthy individuals. Human Brain Mapping, 33(3), 552–568. https://doi.org/10.1002/hbm.21232.
Xia, M., Wang, J., & He, Y. (2013). BrainNet viewer: A network visualization tool for human brain connectomics. PLoS One, 8(7), e68910. https://doi.org/10.1371/journal.pone.0068910.
Yan, C. G., & Zang, Y. F. (2010). DPARSF: A MATLAB toolbox for "pipeline" data analysis of resting-state fMRI. Frontiers in Systems Neuroscience, 4, 13. https://doi.org/10.3389/fnsys.2010.00013.
Yan, C. G., Craddock, R. C., Zuo, X. N., Zang, Y. F., & Milham, M. P. (2013). Standardizing the intrinsic brain: Towards robust measurement of inter-individual variation in 1000 functional connectomes. Neuroimage, 80, 246–262. https://doi.org/10.1016/j.neuroimage.2013.04.081.
Yu, Q., Plis, S. M., Erhardt, E. B., Allen, E. A., Sui, J., Kiehl, K. A., Pearlson, G., & Calhoun, V. D. (2011). Modular organization of functional network connectivity in healthy controls and patients with schizophrenia during the resting state. Frontiers in Systems Neuroscience, 5, 103. https://doi.org/10.3389/fnsys.2011.00103.
Yu, Q., Sui, J., Liu, J., Plis, S. M., Kiehl, K. A., Pearlson, G., & Calhoun, V. D. (2013). Disrupted correlation between low frequency power and connectivity strength of resting state brain networks in schizophrenia. Schizophrenia Research, 143(1), 165–171. https://doi.org/10.1016/j.schres.2012.11.001.
Yu, R., Chien, Y. L., Wang, H. L. S., Liu, C. M., Liu, C. C., Hwang, T. J., Hsieh, M. H., Hwu, H. G., & Tseng, W. Y. I. (2014). Frequency-specific alternations in the amplitude of low-frequency fluctuations in schizophrenia. Human Brain Mapping, 35(2), 627–637.
Zalesky, A., Fornito, A., & Bullmore, E. (2012). On the use of correlation as a measure of network connectivity. Neuroimage, 60(4), 2096–2106. https://doi.org/10.1016/j.neuroimage.2012.02.001.
Author information
Authors and Affiliations
Corresponding authors
Ethics declarations
Conflict of interest
The authors have nothing to disclose.
Sources of support
This work was supported by Zhejiang University (“Hundred Talents Program” awarded to Y. S.), by the Fundamental Research Funds for the Central Universities (Grant no. 2018QNA5017 awarded to Y.S.), and by the Ministry of Education of Singapore (MOE2016-T2–1-015 awarded to R. Y.). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
Informed consent
All procedures followed were in accordance with the ethical standards of the responsible committee on human experimentation (institutional and national) and with the Helsinki Declaration of 1975, and the applicable revisions at the time of the investigation. Informed consent was obtained from all patients included in the study.
Rights and permissions
About this article
Cite this article
Zhang, Y., Dai, Z., Chen, Y. et al. Altered intra- and inter-hemispheric functional dysconnectivity in schizophrenia. Brain Imaging and Behavior 13, 1220–1235 (2019). https://doi.org/10.1007/s11682-018-9935-8
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11682-018-9935-8