Hostname: page-component-cd9895bd7-hc48f Total loading time: 0 Render date: 2024-12-27T12:27:53.443Z Has data issue: false hasContentIssue false
  • English
  • Français

Characteristics of disrupted topological organization in white matter functional connectome in schizophrenia

Published online by Cambridge University Press:  03 September 2020

Yuchao Jiang Open the ORCID record for Yuchao Jiang [Opens in a new window] ,
Dezhong Yao ,
Jingyu Zhou ,
Yue Tan ,
Huan Huang ,
MeiLin Wang ,
Xin Chang ,
Mingjun Duan  and
Cheng Luo
Yuchao Jiang
Affiliation:
The Clinical Hospital of Chengdu Brain Science Institute, MOE Key Lab for Neuroinformation, Center for Information in Medicine, University of Electronic Science and Technology of China, Chengdu, P. R. China High-Field Magnetic Resonance Brain Imaging Key Laboratory of Sichuan Province, School of life Science and technology, University of Electronic Science and Technology of China, Chengdu, P. R. China
Dezhong Yao
Affiliation:
The Clinical Hospital of Chengdu Brain Science Institute, MOE Key Lab for Neuroinformation, Center for Information in Medicine, University of Electronic Science and Technology of China, Chengdu, P. R. China Research Unit of NeuroInformation, Chinese Academy of Medical Sciences, 2019RU035, Chengdu, P. R. China School of Electrical Engineering, Zhengzhou University, Zhengzhou, P. R. China
Jingyu Zhou
Affiliation:
The Clinical Hospital of Chengdu Brain Science Institute, MOE Key Lab for Neuroinformation, Center for Information in Medicine, University of Electronic Science and Technology of China, Chengdu, P. R. China High-Field Magnetic Resonance Brain Imaging Key Laboratory of Sichuan Province, School of life Science and technology, University of Electronic Science and Technology of China, Chengdu, P. R. China
Yue Tan
Affiliation:
The Clinical Hospital of Chengdu Brain Science Institute, MOE Key Lab for Neuroinformation, Center for Information in Medicine, University of Electronic Science and Technology of China, Chengdu, P. R. China
Huan Huang
Affiliation:
The Clinical Hospital of Chengdu Brain Science Institute, MOE Key Lab for Neuroinformation, Center for Information in Medicine, University of Electronic Science and Technology of China, Chengdu, P. R. China
MeiLin Wang
Affiliation:
The Clinical Hospital of Chengdu Brain Science Institute, MOE Key Lab for Neuroinformation, Center for Information in Medicine, University of Electronic Science and Technology of China, Chengdu, P. R. China
Xin Chang
Affiliation:
The Clinical Hospital of Chengdu Brain Science Institute, MOE Key Lab for Neuroinformation, Center for Information in Medicine, University of Electronic Science and Technology of China, Chengdu, P. R. China High-Field Magnetic Resonance Brain Imaging Key Laboratory of Sichuan Province, School of life Science and technology, University of Electronic Science and Technology of China, Chengdu, P. R. China
Mingjun Duan
Affiliation:
The Clinical Hospital of Chengdu Brain Science Institute, MOE Key Lab for Neuroinformation, Center for Information in Medicine, University of Electronic Science and Technology of China, Chengdu, P. R. China Department of Psychiatry, Chengdu Mental Health Center, Chengdu, P. R. China
Cheng Luo*
Affiliation:
The Clinical Hospital of Chengdu Brain Science Institute, MOE Key Lab for Neuroinformation, Center for Information in Medicine, University of Electronic Science and Technology of China, Chengdu, P. R. China High-Field Magnetic Resonance Brain Imaging Key Laboratory of Sichuan Province, School of life Science and technology, University of Electronic Science and Technology of China, Chengdu, P. R. China Research Unit of NeuroInformation, Chinese Academy of Medical Sciences, 2019RU035, Chengdu, P. R. China
*
Author for correspondence: Cheng Luo, E-mail: [email protected]
Get access Rights & Permissions [Opens in a new window]

Abstract

Background

Neuroimaging characteristics have demonstrated disrupted functional organization in schizophrenia (SZ), involving large-scale networks within grey matter (GM). However, previous studies have ignored the role of white matter (WM) in supporting brain function.

Methods

Using resting-state functional MRI and graph theoretical approaches, we investigated global topological disruptions of large-scale WM and GM networks in 93 SZ patients and 122 controls. Six global properties [clustering coefficient (Cp), shortest path length (Lp), local efficiency (Eloc), small-worldness (σ), hierarchy (β) and synchronization (S) and three nodal metrics [nodal degree (Knodal), nodal efficiency (Enodal) and nodal betweenness (Bnodal)] were utilized to quantify the topological organization in both WM and GM networks.

Results

At the network level, both WM and GM networks exhibited reductions in Eloc, Cp and S in SZ. The SZ group showed reduced σ and β only for the WM network. Furthermore, the Cp, Eloc and S of the WM network were negatively correlated with negative symptoms in SZ. At the nodal level, the SZ showed nodal disturbances in the corpus callosum, optic radiation, posterior corona radiata and tempo-occipital WM tracts. For GM, the SZ manifested increased nodal centralities in frontoparietal regions and decreased nodal centralities in temporal regions.

Conclusions

These findings provide the first evidence for abnormal global topological properties in SZ from the perspective of a substantial whole brain, including GM and WM. Nodal centralities enhance GM areas, along with a reduction in adjacent WM, suggest that WM functional alterations may be compensated for adjacent GM impairments in SZ.

Keywords

ConnectomefMRIgraph theoryschizophreniawhite matter
Type
Original Article
Information
Psychological Medicine , Volume 52 , Issue 7 , May 2022 , pp. 1333 - 1343
Check for updates
Copyright
Copyright © The Author(s) 2020. Published by Cambridge University Press

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Agcaoglu, O., Miller, R., Damaraju, E., Rashid, B., Bustillo, J., Cetin, M. S., … Calhoun, V. D. (2018). Decreased hemispheric connectivity and decreased intra- and inter- hemisphere asymmetry of resting state functional network connectivity in schizophrenia. Brain Imaging and Behavior, 12(3), 615–630. doi: 10.1007/s11682-017-9718-7.CrossRefGoogle Scholar
Aydin, K., Ucok, A., & Guler, J. (2008). Altered metabolic integrity of corpus callosum among individuals at ultra high risk of schizophrenia and first-episode patients. Biological Psychiatry, 64(9), 750–757. doi: 10.1016/j.biopsych.2008.04.007.CrossRefGoogle ScholarPubMed
Barahona, M., & Pecora, L. M. (2002). Synchronization in small-world systems. Physical Review Letters, 89(5), 054101. doi: 10.1103/PhysRevLett.89.054101.CrossRefGoogle ScholarPubMed
Barbaresi, P., Fabri, M., & Mensa, E. (2014). Characterization of NO-producing neurons in the rat corpus callosum. Brain and Behavior, 4(3), 317–336. doi: 10.1002/brb3.218.CrossRefGoogle ScholarPubMed
Bassett, D. S., Bullmore, E., Verchinski, B. A., Mattay, V. S., Weinberger, D. R., & Meyer-Lindenberg, A. (2008). Hierarchical organization of human cortical networks in health and schizophrenia. Journal of Neuroscience, 28(37), 9239–9248. doi: 10.1523/JNEUROSCI.1929-08.2008.CrossRefGoogle Scholar
Beaulieu, C. (2002). The basis of anisotropic water diffusion in the nervous system – a technical review. Nmr in Biomedicine, 15(7–8), 435–455. doi: 10.1002/nbm.782.CrossRefGoogle ScholarPubMed
Bora, E., Fornito, A., Radua, J., Walterfang, M., Seal, M., Wood, S. J., … Pantelis, C. (2011). Neuroanatomical abnormalities in schizophrenia: A multimodal voxelwise meta-analysis and meta-regression analysis. Schizophrenia Research, 127(1–3), 46–57. doi: 10.1016/j.schres.2010.12.020.CrossRefGoogle ScholarPubMed
Bullmore, E., & Sporns, O. (2009). Complex brain networks: Graph theoretical analysis of structural and functional systems. Nature Reviews Neuroscience, 10(3), 186–198. doi: 10.1038/nrn2575.CrossRefGoogle ScholarPubMed
Chen, Z., Hu, X., Chen, Q., & Feng, T. (2019). Altered structural and functional brain network overall organization predict human intertemporal decision-making. Human Brain Mapping, 40(1), 306–328. doi: 10.1002/hbm.24374.CrossRefGoogle ScholarPubMed
Chen, X., Liu, C., He, H., Chang, X., Jiang, Y., Li, Y., … Yao, D. (2017a). Transdiagnostic differences in the resting-state functional connectivity of the prefrontal cortex in depression and schizophrenia. Journal of Affective Disorders, 217, 118–124. doi: 10.1016/j.jad.2017.04.001.CrossRefGoogle Scholar
Chen, X., Zhang, H., Zhang, L., Shen, C., Lee, S. W., & Shen, D. (2017b). Extraction of dynamic functional connectivity from brain grey matter and white matter for MCI classification. Human Brain Mapping, 38(10), 5019–5034. doi: 10.1002/hbm.23711.CrossRefGoogle Scholar
Courtemanche, M. J., Sparrey, C. J., Song, X., MacKay, A., & D'Arcy, R. C. N. (2018). Detecting white matter activity using conventional 3 Tesla fMRI: An evaluation of standard field strength and hemodynamic response function. Neuroimage, 169, 145–150. doi: 10.1016/j.neuroimage.2017.12.008.CrossRefGoogle ScholarPubMed
Desikan, R. S., Segonne, F., Fischl, B., Quinn, B. T., Dickerson, B. C., Blacker, D., … Killiany, R. J. (2006). An automated labeling system for subdividing the human cerebral cortex on MRI scans into gyral based regions of interest. Neuroimage, 31(3), 968–980. doi: 10.1016/j.neuroimage.2006.01.021.CrossRefGoogle ScholarPubMed
Dong, D., Luo, C., Guell, X., Wang, Y., He, H., Duan, M., … Yao, D. (2020). Compression of cerebellar functional gradients in schizophrenia. Schizophrenia Bulletin. doi: 10.1093/schbul/sbaa016.CrossRefGoogle Scholar
Dong, D., Wang, Y., Chang, X., Luo, C., & Yao, D. (2018). Dysfunction of large-scale brain networks in schizophrenia: A meta-analysis of resting-state functional connectivity. Schizophrenia Bulletin, 44(1), 168–181. doi: 10.1093/schbul/sbx034.CrossRefGoogle ScholarPubMed
Duan, M., Chen, X., He, H., Jiang, Y., Jiang, S., Xie, Q., … Yao, D. (2015). Altered basal ganglia network integration in schizophrenia. Frontiers in Human Neuroscience, 9, 561. doi: 10.3389/fnhum.2015.00561.CrossRefGoogle Scholar
Fan, Y. S., Li, Z., Duan, X., Xiao, J., Guo, X., Han, S., … Chen, H. (2020). Impaired interactions among white-matter functional networks in antipsychotic-naive first-episode schizophrenia. Human Brain Mapping, 41(1), 230–240. doi: 10.1002/hbm.24801.CrossRefGoogle ScholarPubMed
Ford, J. M., Krystal, J. H., & Mathalon, D. H. (2007). Neural synchrony in schizophrenia: From networks to new treatments. Schizophrenia Bulletin, 33(4), 848–852. doi: 10.1093/schbul/sbm062.CrossRefGoogle ScholarPubMed
Fornito, A., Zalesky, A., Pantelis, C., & Bullmore, E. T. (2012). Schizophrenia, neuroimaging and connectomics. Neuroimage, 62(4), 2296–2314. doi: 10.1016/j.neuroimage.2011.12.090.CrossRefGoogle ScholarPubMed
Fries, P. (2009). Neuronal gamma-band synchronization as a fundamental process in cortical computation. Annual Review of Neuroscience, 32, 209–224. doi: 10.1146/annurev.neuro.051508.135603.CrossRefGoogle ScholarPubMed
Gawryluk, J. R., Mazerolle, E. L., Beyea, S. D., & D'Arcy, R. C. (2014a). Functional MRI activation in white matter during the Symbol Digit Modalities Test. Frontiers in Human Neuroscience, 8, 589. doi: 10.3389/fnhum.2014.00589.CrossRefGoogle Scholar
Gawryluk, J. R., Mazerolle, E. L., & D'Arcy, R. C. (2014b). Does functional MRI detect activation in white matter? A review of emerging evidence, issues, and future directions. Frontiers in Neuroscience, 8, 239. doi: 10.3389/fnins.2014.00239.CrossRefGoogle Scholar
Gong, J., Luo, C., Li, X., Jiang, S., Khundrakpam, B. S., Duan, M., … Yao, D. (2019). Evaluation of functional connectivity in subdivisions of the thalamus in schizophrenia. British Journal of Psychiatry, 214(5), 288–296. doi: 10.1192/bjp.2018.299.CrossRefGoogle Scholar
Guo, W., Liu, F., Liu, J., Yu, L., Zhang, J., Zhang, Z., … Zhao, J. (2015). Abnormal causal connectivity by structural deficits in first-episode, drug-naive schizophrenia at rest. Schizophrenia Bulletin, 41(1), 57–65. doi: 10.1093/schbul/sbu126.CrossRefGoogle ScholarPubMed
Ho, N. F., Iglesias, J. E., Sum, M. Y., Kuswanto, C. N., Sitoh, Y. Y., De Souza, J., … Holt, D. J. (2017). Progression from selective to general involvement of hippocampal subfields in schizophrenia. Molecular Psychiatry, 22(1), 142–152. doi: 10.1038/mp.2016.4.CrossRefGoogle Scholar
Huang, Y., Bailey, S. K., Wang, P., Cutting, L. E., Gore, J. C., & Ding, Z. (2018). Voxel-wise detection of functional networks in white matter. Neuroimage, 183, 544–552. doi: 10.1016/j.neuroimage.2018.08.049.CrossRefGoogle ScholarPubMed
Ji, G. J., Liao, W., Chen, F. F., Zhang, L., & Wang, K. (2017). Low-frequency blood oxygen level-dependent fluctuations in the brain white matter: More than just noise. Science Bulletin, 62(9), 656–657. doi: 10.1016/j.scib.2017.03.021.CrossRefGoogle Scholar
Ji, G. J., Ren, C., Li, Y., Sun, J., Liu, T., Gao, Y., … Wang, K. (2019). Regional and network properties of white matter function in Parkinson's disease. Human Brain Mapping, 40(4), 1253–1263. doi: 10.1002/hbm.24444.CrossRefGoogle ScholarPubMed
Jiang, Y., Duan, M., Chen, X., Zhang, X., Gong, J., Dong, D., … Yao, D. (2019a). Aberrant prefrontal-thalamic-cerebellar circuit in schizophrenia and depression: Evidence from a possible causal connectivity. International Journal of Neural Systems, 29(5), 1850032. doi: 10.1142/S0129065718500326.CrossRefGoogle Scholar
Jiang, Y., Luo, C., Li, X., Duan, M., He, H., Chen, X., … Yao, D. (2018). Progressive reduction in gray matter in patients with schizophrenia assessed with MR imaging by using causal network analysis. Radiology, 287(2), 633–642. doi: 10.1148/radiol.2017171832.CrossRefGoogle ScholarPubMed
Jiang, Y., Luo, C., Li, X., Li, Y., Yang, H., Li, J., … Yao, D. (2019b). White-matter functional networks changes in patients with schizophrenia. Neuroimage, 190, 172–181. doi: 10.1016/j.neuroimage.2018.04.018.CrossRefGoogle Scholar
Jiang, Y., Song, L., Li, X., Zhang, Y., Chen, Y., Jiang, S., … Luo, C. (2019c). Dysfunctional white-matter networks in medicated and unmedicated benign epilepsy with centrotemporal spikes. Human Brain Mapping, 40(10), 3113–3124. doi: 10.1002/hbm.24584.Google Scholar
Kochunov, P., & Hong, L. E. (2014). Neurodevelopmental and neurodegenerative models of schizophrenia: White matter at the center stage. Schizophrenia Bulletin, 40(4), 721–728. doi: 10.1093/schbul/sbu070.CrossRefGoogle ScholarPubMed
Li, J., Biswal, B. B., Wang, P., Duan, X., Cui, Q., Chen, H., & Liao, W. (2019a). Exploring the functional connectome in white matter. Human Brain Mapping, 40(15), 4331–4344. doi: 10.1002/hbm.24705.CrossRefGoogle Scholar
Li, M., Newton, A. T., Anderson, A. W., Ding, Z., & Gore, J. C. (2019b). Characterization of the hemodynamic response function in white matter tracts for event-related fMRI. Nature Communications, 10(1), 1140. doi: 10.1038/s41467-019-09076-2.CrossRefGoogle Scholar
Liu, Y., Liang, M., Zhou, Y., He, Y., Hao, Y., Song, M., … Jiang, T. (2008). Disrupted small-world networks in schizophrenia. Brain, 131(Pt 4), 945–961. doi: 10.1093/brain/awn018.CrossRefGoogle Scholar
Lo, C. Y., Su, T. W., Huang, C. C., Hung, C. C., Chen, W. L., Lan, T. H., … Bullmore, E. T. (2015). Randomization and resilience of brain functional networks as systems-level endophenotypes of schizophrenia. Proceedings of the National Academy of Sciences of the United States of America, 112(29), 9123–9128. doi: 10.1073/pnas.1502052112.CrossRefGoogle ScholarPubMed
Luo, Y., He, H., Duan, M., Huang, H., Hu, Z., Wang, H., … Luo, C. (2019). Dynamic functional connectivity strength within different frequency-band in schizophrenia. Frontiers in Psychiatry, 10, 995. doi: 10.3389/fpsyt.2019.00995.CrossRefGoogle Scholar
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. Journal of Neuroscience, 30(28), 9477–9487. doi: 10.1523/JNEUROSCI.0333-10.2010.CrossRefGoogle Scholar
Makedonov, I., Chen, J. J., Masellis, M., & MacIntosh, B. J., & Alzheimer's Disease Neuroimaging, I. (2016). Physiological fluctuations in white matter are increased in Alzheimer's disease and correlate with neuroimaging and cognitive biomarkers. Neurobiology of Aging, 37, 12–18. doi: 10.1016/j.neurobiolaging.2015.09.010.CrossRefGoogle ScholarPubMed
Marussich, L., Lu, K. H., Wen, H., & Liu, Z. (2017). Mapping white-matter functional organization at rest and during naturalistic visual perception. Neuroimage, 146, 1128–1141. doi: 10.1016/j.neuroimage.2016.10.005.CrossRefGoogle ScholarPubMed
McCutcheon, R. A., Abi-Dargham, A., & Howes, O. D. (2019). Schizophrenia, dopamine and the striatum: From biology to symptoms. Trends in Neurosciences, 42(3), 205–220. doi: 10.1016/j.tins.2018.12.004.CrossRefGoogle ScholarPubMed
Menon, V. (2011). Large-scale brain networks and psychopathology: A unifying triple network model. Trends in Cognitive Sciences, 15(10), 483–506. doi: 10.1016/j.tics.2011.08.003mCrossRefGoogle ScholarPubMed
Moran, L. V., Tagamets, M. A., Sampath, H., O'Donnell, A., Stein, E. A., Kochunov, P., & Hong, L. E. (2013). Disruption of anterior insula modulation of large-scale brain networks in schizophrenia. Biological Psychiatry, 74(6), 467–474. doi: 10.1016/j.biopsych.2013.02.029.CrossRefGoogle Scholar
Peer, M., Nitzan, M., Bick, A. S., Levin, N., & Arzyt, S. (2017). Evidence for functional networks within the human brain's white matter. Journal of Neuroscience, 37(27), 6394–6407. doi: 10.1523/Jneurosci.3872-16.2017.CrossRefGoogle ScholarPubMed
Pergola, G., Selvaggi, P., Trizio, S., Bertolino, A., & Blasi, G. (2015). The role of the thalamus in schizophrenia from a neuroimaging perspective. Neuroscience and Biobehavioral Reviews, 54, 57–75. doi: 10.1016/j.neubiorev.2015.01.013.CrossRefGoogle ScholarPubMed
Petzold, G. C., & Murthy, V. N. (2011). Role of astrocytes in neurovascular coupling. Neuron, 71(5), 782–797. doi: 10.1016/j.neuron.2011.08.009.CrossRefGoogle ScholarPubMed
Rash, J. E. (2010). Molecular disruptions of the panglial syncytium block potassium siphoning and axonal saltatory conduction: Pertinence to neuromyelitis optica and other demyelinating diseases of the central nervous system. Neuroscience, 168(4), 982–1008. doi: 10.1016/j.neuroscience.2009.10.028.CrossRefGoogle ScholarPubMed
Ray, K. L., Lesh, T. A., Howell, A. M., Salo, T. P., Ragland, J. D., MacDonald, A. W., … Carter, C. S. (2017). Functional network changes and cognitive control in schizophrenia. NeuroImage-Clinical, 15, 161–170. doi: 10.1016/j.nicl.2017.05.001.CrossRefGoogle Scholar
Rosenberger, G., Nestor, P. G., Oh, J. S., Levitt, J. J., Kindleman, G., Bouix, S., … Kubicki, M. (2012). Anterior limb of the internal capsule in schizophrenia: A diffusion tensor tractography study. Brain Imaging and Behavior, 6(3), 417–425. doi: 10.1007/s11682-012-9152-9.CrossRefGoogle ScholarPubMed
Rubinov, M., & Sporns, O. (2010). Complex network measures of brain connectivity: Uses and interpretations. Neuroimage, 52(3), 1059–1069. doi: 10.1016/j.neuroimage.2009.10.003.CrossRefGoogle ScholarPubMed
Sellgren, C. M., Gracias, J., Watmuff, B., Biag, J. D., Thanos, J. M., Whittredge, P. B., … Perlis, R. H. (2019). Increased synapse elimination by microglia in schizophrenia patient-derived models of synaptic pruning. Nature Neuroscience, 22(3), 374. doi: 10.1038/s41593-018-0334-7.CrossRefGoogle ScholarPubMed
Shen, K., Misic, B., Cipollini, B. N., Bezgin, G., Buschkuehl, M., Hutchison, R. M., … Berman, M. G. (2015). Stable long-range interhemispheric coordination is supported by direct anatomical projections. Proceedings of the National Academy of Sciences of the United States of America, 112(20), 6473–6478. doi: 10.1073/pnas.1503436112.CrossRefGoogle ScholarPubMed
Smith, A. J., Blumenfeld, H., Behar, K. L., Rothman, D. L., Shulman, R. G., & Hyder, F. (2002). Cerebral energetics and spiking frequency: The neurophysiological basis of fMRI. Proceedings of the National Academy of Sciences of the United States of America, 99(16), 10765–10770. doi: 10.1073/pnas.132272199.CrossRefGoogle ScholarPubMed
Uhlhaas, P. J., Haenschel, C., Nikolic, D., & Singer, W. (2008). The role of oscillations and synchrony in cortical networks and their putative relevance for the pathophysiology of schizophrenia. Schizophrenia Bulletin, 34(5), 927–943. doi: 10.1093/schbul/sbn062.CrossRefGoogle ScholarPubMed
Uhlhaas, P. J., & Singer, W. (2010). Abnormal neural oscillations and synchrony in schizophrenia. Nature Reviews Neuroscience, 11(2), 100–113. doi: 10.1038/nrn2774.CrossRefGoogle Scholar
Wang, J., Jiang, Y., Tang, Y., Xia, M., Curtin, A., Li, J., … Wang, J. (2020). Altered functional connectivity of the thalamus induced by modified electroconvulsive therapy for schizophrenia. Schizophrenia Research. doi: 10.1016/j.schres.2019.12.044.CrossRefGoogle Scholar
Wang, Q., Zhang, J., Liu, Z., Crow, T. J., Zhang, K., Palaniyappan, L., … Li, T. (2019). “Brain connectivity deviates by Sex and hemisphere in the first episode of schizophrenia” – a route to the genetic basis of language and psychosis? Schizophrenia Bulletin, 45(2), 484–494. doi: 10.1093/schbul/sby061.CrossRefGoogle Scholar
Whitford, T. J., Kubicki, M., Schneiderman, J. S., O'Donnell, L. J., King, R., Alvarado, J. L., … Shenton, M. E. (2010). Corpus callosum abnormalities and their association with psychotic symptoms in patients with schizophrenia. Biological Psychiatry, 68(1), 70–77. doi: 10.1016/j.biopsych.2010.03.025.CrossRefGoogle ScholarPubMed
Wu, T. L., Wang, F., Li, M., Schilling, K. G., Gao, Y., Anderson, A. W., … Gore, J. C. (2019). Resting-state white matter-cortical connectivity in non-human primate brain. Neuroimage, 184, 45–55. doi: 10.1016/j.neuroimage.2018.09.021.CrossRefGoogle ScholarPubMed
Wu, X., Yang, Z., Bailey, S. K., Zhou, J., Cutting, L. E., Gore, J. C., & Ding, Z. (2017). Functional connectivity and activity of white matter in somatosensory pathways under tactile stimulations. Neuroimage, 152, 371–380. doi: 10.1016/j.neuroimage.2017.02.074.CrossRefGoogle ScholarPubMed
Yang, C., Zhang, W., Yao, L., Liu, N., Shah, C., Zeng, J., … Lui, S. (2019). Functional alterations of white matter in chronic never-treated and treated schizophrenia patients. Journal of Magnetic Resonance Imaging. doi: 10.1002/jmri.27028.Google ScholarPubMed
Yu, M., Dai, Z., Tang, X., Wang, X., Zhang, X., Sha, W., … Zhang, Z. (2017). Convergence and divergence of brain network dysfunction in deficit and non-deficit schizophrenia. Schizophrenia Bulletin, 43(6), 1315–1328. doi: 10.1093/schbul/sbx014.CrossRefGoogle ScholarPubMed
Supplementary material: File

Jiang et al. supplementary material

Jiang et al. supplementary material

Download Jiang et al. supplementary material(File)
File 56.5 KB