Skip to main content Accessibility help
×
Home
Hostname: page-component-559fc8cf4f-rz424 Total loading time: 0.324 Render date: 2021-02-24T21:13:55.964Z Has data issue: true Feature Flags: { "shouldUseShareProductTool": true, "shouldUseHypothesis": true, "isUnsiloEnabled": true, "metricsAbstractViews": false, "figures": false, "newCiteModal": false, "newCitedByModal": true }

Altered functional synchrony between gray and white matter as a novel indicator of brain system dysconnectivity in schizophrenia

Published online by Cambridge University Press:  13 January 2021

Naici Liu
Affiliation:
Huaxi MR Research Center (HMRRC), Department of Radiology, West China Hospital of Sichuan University, Chengdu, China
Rebekka Lencer
Affiliation:
Department of Psychiatry and Psychotherapy, Otto Creutzfeldt Center for Cognitive and Behavioral Neuroscience, University of Muenster, Muenster, Germany
Zhipeng Yang
Affiliation:
College of Electronic Engineering, Chengdu University of Information Technology, Chengdu, PR, China
Wenjing Zhang
Affiliation:
Huaxi MR Research Center (HMRRC), Department of Radiology, West China Hospital of Sichuan University, Chengdu, China
Chengmin Yang
Affiliation:
Huaxi MR Research Center (HMRRC), Department of Radiology, West China Hospital of Sichuan University, Chengdu, China
Jiaxin Zeng
Affiliation:
Huaxi MR Research Center (HMRRC), Department of Radiology, West China Hospital of Sichuan University, Chengdu, China
John A. Sweeney
Affiliation:
Huaxi MR Research Center (HMRRC), Department of Radiology, West China Hospital of Sichuan University, Chengdu, China Department of Psychiatry and Behavioral Neuroscience, University of Cincinnati, Cincinnati, OH, USA
Qiyong Gong
Affiliation:
Huaxi MR Research Center (HMRRC), Department of Radiology, West China Hospital of Sichuan University, Chengdu, China
Su Lui
Affiliation:
Huaxi MR Research Center (HMRRC), Department of Radiology, West China Hospital of Sichuan University, Chengdu, China
Corresponding

Abstract

Background

There is increasing evidence that blood oxygenation level-dependent signaling in white matter (WM) reflects WM functional activity. Whether this activity is altered in schizophrenia remains uncertain, as does whether it is related to established alterations of gray matter (GM) or the microstructure of WM tracts.

Methods

A total of 153 antipsychotic-naïve schizophrenia patients and 153 healthy comparison subjects were assessed by resting-state functional magnetic resonance imaging, diffusion tensor imaging, and high-resolution T1-weighted imaging. We tested for case–control differences in the functional activity of WM, and examined their relation to the functional activity of GM and WM microstructure. The relations between fractional anisotropy (FA) in WM and GM–WM functional synchrony were investigated as well. Then, we examined the associations of identified abnormalities to age, duration of untreated psychosis (DUP), and symptom severity.

Results

Schizophrenia patients displayed reductions of the amplitude of low-frequency fluctuations (ALFF), GM–WM functional synchrony, and FA in widespread regions. Specifically, the genu of corpus callosum not only had weakening in the synchrony of functional activity but also had reduced ALFF and FA. Positive associations were found between FA and functional synchrony in the genu of corpus callosum as well. No significant association was found between identified abnormalities and DUP, and symptom severity.

Conclusions

The widespread weakening in the synchrony of functional activity of GM and WM provided novel evidence for functional alterations in schizophrenia. Regarding the WM function as a component of brain systems and investigating its alternation represent a promising direction for future research.

Type
Original Article
Copyright
Copyright © West China Hospital of Sichuan University, 2021. Published by Cambridge University Press

Access options

Get access to the full version of this content by using one of the access options below.

Footnotes

*

Dr Liu, Dr Lencer, and Dr Yang contributed equally to the study.

References

Bartzokis, G., Lu, P. H., Nuechterlein, K. H., Gitlin, M., Doi, C., Edwards, N., … Mintz, J. (2008). Differential effects of typical and atypical antipsychotics on brain myelination in schizophrenia (vol 93, pg 13, 2007). Schizophrenia Research, 99(1–3), 379. doi: 10.1016/j.schres.2007.09.023CrossRefGoogle Scholar
Cetin-Karayumak, S., Di Biase, M. A., Chunga, N., Reid, B., Somes, N., Lyall, A. E., … Kubicki, M. (2019). White matter abnormalities across the lifespan of schizophrenia: A harmonized multi-site diffusion MRI study. Molecular Psychiatry, 25(12), 32083219. doi: 10.1038/s41380-019-0509-yCrossRefGoogle ScholarPubMed
Chechko, N., Cieslik, E. C., Muller, V. I., Nickl-Jockschat, T., Derntl, B., Kogler, L., … Eickhoff, S. B. (2018). Differential resting-state connectivity patterns of the right anterior and posterior dorsolateral prefrontal cortices (DLPFC) in schizophrenia. Frontiers in Psychiatry, 9, 211. doi: 10.3389/fpsyt.2018.00211CrossRefGoogle Scholar
Ding, Z. H., Huang, Y. L., Bailey, S. K., Gao, Y. R., Cutting, L. E., Rogers, B. P., … Gore, J. C. (2018). Detection of synchronous brain activity in white matter tracts at rest and under functional loading. Proceedings of the National Academy of Sciences of the USA, 115(3), 595600. doi: 10.1073/pnas.1711567115CrossRefGoogle ScholarPubMed
Flynn, S. W., Lang, D. J., Mackay, A. L., Goghari, V., Vavasour, I. M., Whittall, K. P., … Honer, W. G. (2003). Abnormalities of myelination in schizophrenia detected in vivo with MRI, and post-mortem with analysis of oligodendrocyte proteins. Molecular Psychiatry, 8(9), 811820. doi: 10.1038/sj.mp.4001337CrossRefGoogle ScholarPubMed
Friston, K. J., Williams, S., Howard, R., Frackowiak, R. S. J., & Turner, R. (1996). Movement-related effects in fMRI time-series. Magnetic Resonance in Medicine, 35(3), 346355. doi: DOI 10.1002/mrm.1910350312CrossRefGoogle ScholarPubMed
Gawryluk, J. R., Mazerolle, E. L., & D'Arcy, R. C. N. (2014). Does functional MRI detect activation in white matter? A review of emerging evidence, issues, and future directions. Frontiers in Neuroscience, 8. doi: ARTN 23910.3389/fnins.2014.00239CrossRefGoogle ScholarPubMed
Jiang, Y. C., Luo, C., Li, X., Li, Y. J., Yang, H., Li, J. F., … Yao, D. Z. (2019). White-matter functional networks changes in patients with schizophrenia. Neuroimage, 190, 172181. doi: 10.1016/j.neuroimage.2018.04.018CrossRefGoogle ScholarPubMed
Lencer, R., Yao, L., Reilly, J. L., Keedy, S. K., McDowell, J. E., Keshavan, M. S., … Sweeney, J. A. (2019). Alterations in intrinsic fronto-thalamo-parietal connectivity are associated with cognitive control deficits in psychotic disorders. Human Brain Mapping, 40(1), 163174. doi: 10.1002/hbm.24362CrossRefGoogle ScholarPubMed
Li, S. Y., Hu, N., Zhang, W. J., Tao, B., Dai, J., Gong, Y., … Lui, S. (2019). Dysconnectivity of multiple brain networks in schizophrenia: A meta-analysis of resting-state functional connectivity. Frontiers in Psychiatry, 10.CrossRefGoogle ScholarPubMed
Liu, J. K., Yao, L., Zhang, W. J., Deng, W., Xiao, Y., Li, F., … Lui, S. (2019). Dissociation of fractional anisotropy and resting-state functional connectivity alterations in antipsychotic-naive first-episode schizophrenia. Schizophrenia Research, 204, 230237. doi: 10.1016/j.schres.2018.08.005CrossRefGoogle ScholarPubMed
Lui, S., Yao, L., Xiao, Y., Keedy, S. K., Reilly, J. L., Keefe, R. S., … Sweeney, J. A. (2015). Resting-state brain function in schizophrenia and psychotic bipolar probands and their first-degree relatives. Psychological Medicine, 45(1), 97108. doi: 10.1017/S003329171400110xCrossRefGoogle ScholarPubMed
Maldjian, J. A., Laurienti, P. J., Kraft, R. A., & Burdette, J. H. (2003). An automated method for neuroanatomic and cytoarchitectonic atlas-based interrogation of fMRI data sets. Neuroimage, 19(3), 12331239. doi: 10.1016/S1053-8119(03)00169-1CrossRefGoogle ScholarPubMed
Mazerolle, E. L., Beyea, S. D., Gawryluk, J. R., Brewer, K. D., Bowen, C. V., & D'Arcy, R. C. N. (2010). Confirming white matter fMRI activation in the corpus callosum: Co-localization with DTI tractography. Neuroimage, 50(2), 616621. doi: 10.1016/j.neuroimage.2009.12.102CrossRefGoogle ScholarPubMed
Meng, L., Li, K., Li, W., Xiao, Y., Lui, S., Sweeney, J. A., & Gong, Q. (2019). Widespread white-matter microstructure integrity reduction in first-episode schizophrenia patients after acute antipsychotic treatment. Schizophrenia Research, 204, 238244. doi: 10.1016/j.schres.2018.08.021CrossRefGoogle ScholarPubMed
Mori, S., Oishi, K., Jiang, H. Y., Jiang, L., Li, X., Akhter, K., … Mazziotta, J. (2008). Stereotaxic white matter atlas based on diffusion tensor imaging in an ICBM template. Neuroimage, 40(2), 570582.CrossRefGoogle Scholar
Moskowitz, A., & Heim, G. (2011). Eugen Bleuler's Dementia praecox or the group of schizophrenias (1911): A centenary appreciation and reconsideration. Schizophrenia Bulletin, 37(3), 471479. doi: 10.1093/schbul/sbr016CrossRefGoogle ScholarPubMed
Norman, R. M. G., & Malla, A. K. (2001). Duration of untreated psychosis: A critical examination of the concept and its importance. Psychological Medicine, 31(3), 381400.CrossRefGoogle ScholarPubMed
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), 63946407. doi: 10.1523/Jneurosci.3872-16.2017CrossRefGoogle ScholarPubMed
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), 6169. doi: 10.1016/j.biopsych.2010.03.035CrossRefGoogle Scholar
Wu, T. L., Wang, F., Li, M. W., Schilling, K. G., Gao, Y. R., Anderson, A. W., … Gore, J. C. (2019). Resting-state white matter-cortical connectivity in non-human primate brain. Neuroimage, 184, 4555. doi: 10.1016/j.neuroimage.2018.09.021CrossRefGoogle ScholarPubMed
Xiao, Y., Sun, H. Q., Shi, S. L., Jiang, D., Tao, B., Zhao, Y. J., … Lui, S. (2018). White matter abnormalities in never-treated patients with long-term schizophrenia. American Journal of Psychiatry, 175(11), 11291136.CrossRefGoogle ScholarPubMed

Liu et al. supplementary material

Figures S1-S2 and Tables S1-S2

File 171 KB

Altmetric attention score

Full text views

Full text views reflects PDF downloads, PDFs sent to Google Drive, Dropbox and Kindle and HTML full text views.

Total number of HTML views: 47
Total number of PDF views: 37 *
View data table for this chart

* Views captured on Cambridge Core between 13th January 2021 - 24th February 2021. This data will be updated every 24 hours.

Send article to Kindle

To send this article to your Kindle, first ensure no-reply@cambridge.org is added to your Approved Personal Document E-mail List under your Personal Document Settings on the Manage Your Content and Devices page of your Amazon account. Then enter the ‘name’ part of your Kindle email address below. Find out more about sending to your Kindle. Find out more about sending to your Kindle.

Note you can select to send to either the @free.kindle.com or @kindle.com variations. ‘@free.kindle.com’ emails are free but can only be sent to your device when it is connected to wi-fi. ‘@kindle.com’ emails can be delivered even when you are not connected to wi-fi, but note that service fees apply.

Find out more about the Kindle Personal Document Service.

Altered functional synchrony between gray and white matter as a novel indicator of brain system dysconnectivity in schizophrenia
Available formats
×

Send article to Dropbox

To send this article to your Dropbox account, please select one or more formats and confirm that you agree to abide by our usage policies. If this is the first time you use this feature, you will be asked to authorise Cambridge Core to connect with your <service> account. Find out more about sending content to Dropbox.

Altered functional synchrony between gray and white matter as a novel indicator of brain system dysconnectivity in schizophrenia
Available formats
×

Send article to Google Drive

To send this article to your Google Drive account, please select one or more formats and confirm that you agree to abide by our usage policies. If this is the first time you use this feature, you will be asked to authorise Cambridge Core to connect with your <service> account. Find out more about sending content to Google Drive.

Altered functional synchrony between gray and white matter as a novel indicator of brain system dysconnectivity in schizophrenia
Available formats
×
×

Reply to: Submit a response


Your details


Conflicting interests

Do you have any conflicting interests? *