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Gray Matter Atrophy in the Cortico-Striatal-Thalamic Network and Sensorimotor Network in Relapsing–Remitting and Primary Progressive Multiple Sclerosis

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A Correction to this article was published on 08 April 2021

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Abstract

Gray matter atrophy in multiple sclerosis (MS) is thought to be associated with disability and cognitive impairment, but previous studies have sometimes had discordant results, and the atrophy patterns of relapsing–remitting multiple sclerosis (RRMS) and primary progressive multiple sclerosis (PPMS) remain to be clarified. We conducted a meta-analysis using anisotropic effect-size-based algorithms (AES-SDM) to identify consistent findings from whole-brain voxel-based morphometry (VBM) studies of gray matter volume (GMV) in 924 RRMS patients and 204 PPMS patients. This study is registered with PROSPERO (number CRD42019121319). Compared with healthy controls, RRMS and PPMS patients showed gray matter atrophy in the cortico-striatal-thalamic network, sensorimotor network, and bilateral insula. RRMS patients had a larger GMV in the left insula, cerebellum, right precentral gyrus, and bilateral putamen as well as a smaller GMV in the bilateral cingulate, caudate nucleus, right thalamus, superior temporal gyrus and left postcentral gyrus than PPMS patients. The disease duration, Expanded Disability Status Scale score, Paced Auditory Serial Addition Test z-score, and T2-weighted lesion load were associated with specific gray matter regions in RRMS or PPMS. Alterations in the cortico-striatal-thalamic networks, sensorimotor network, and insula may be involved in the common pathogenesis of RRMS and PPMS. The deficits in the cingulate gyrus and caudate nucleus are more apparent in RRMS than in PPMS. The more severe cerebellum atrophy in PPMS may be a brain feature associated with its neurological manifestations. These imaging biomarkers provide morphological evidence for the pathophysiology of MS and should be verified in future research.

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Funding

This study was supported by the National Natural Science Foundation of China (Grant Nos. 81771812 and 81971595 ), the Innovation Spark Project of Sichuan University (Grant No. 2019SCUH0003) and the 1·3·5 Project for Disciplines of Excellence–Clinical Research Incubation Project, West China Hospital, Sichuan University (Grant No. 2020HXFH005).

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Author notes

  1. Yuan Cao and Wei Diao contributed equally to this work.

Authors and Affiliations

  1. Department of Nuclear Medicine, West China Hospital of Sichuan University, Chengdu, 610041, China

    Yuan Cao, Wei Diao, Fangfang Tian, Xipeng Long & Zhiyun Jia

  2. Huaxi MR Research Center (HMRRC), Department of Radiology, West China Hospital of Sichuan University, Chengdu, 610041, China

    Yuan Cao, Wei Diao, Fangfang Tian, Feifei Zhang, Xipeng Long & Zhiyun Jia

  3. Department of Radiology, The First Affiliated Hospital of Nanchang University, Nanchang, 330001, China

    Laichang He & Fuqinq Zhou

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  1. Yuan Cao
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  2. Wei Diao
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  3. Fangfang Tian
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  4. Feifei Zhang
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Contributions

Y.C. wrote the first draft of the paper; F.Q.Z, F.F.T., W.D., L.C.H and Z.Y.J. edited the paper;,Y.C., W.D., F.Q.Z., L.C.H., and Z.Y.J. designed research; Y.C., W.D., F.F.T. X.P.L and F.F.Z. performed research; Y.C., W.D., F.F.T., X.P.L, and F.F.Z analyzed data.

Corresponding author

Correspondence to Zhiyun Jia.

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The original online version of this article was revised: Unfortunately, an Acknowledgement section was inadvertently included in the paper. The section was deleted.

Supplementary Information

Below is the link to the electronic supplementary material.

11065_2021_9479_MOESM1_ESM.tif

Supplementary file1 Supplementary Fig. 1. The funnel plots showing the publication bias for each altered brain region in RRMS compared with healthy controls. RRMS < healthy controls: Funnel plot of superior temporal gyri, Egger’s test p = 0.165; Funnel plot of left striatum, Egger’s test p = 0.145; Funnel plot of insula, Egger’s test p = 0.052; Funnel plot of cingulate gyrus, Egger’s test p = 0.055; Funnel plot of thalamus, Egger’s test p = 0.096; Funnel plot of striatum, Egger’s test p = 0.345; Funnel plot of postcentral gyrus, Egger’s test p = 0.036; Funnel plot of inferior frontal gyrus s, Egger’s test p = 0.08. (TIF 170 KB)

11065_2021_9479_MOESM2_ESM.tif

Supplementary file2 Supplementary Fig. 2. The funnel plots showing the publication bias for each altered brain region in PPMS compared with healthy controls. PPMS < healthy controls: Funnel plot of insula, Egger’s test p = 0.944; Funnel plot of striatum, Egger’s test p = 0.071; Funnel plot of left thalamus, Egger’s test p = 0.539; Funnel plot of postcentral gyrus, Egger’s test p = 0.007. (TIF 103 KB)

11065_2021_9479_MOESM3_ESM.tif

Supplementary file3 Supplementary Fig. 3. The funnel plots showing the publication bias for each altered brain region in RRMS compared with PPMS. RRMS > PPMS: Funnel plot of left insula, Egger’s test p = 0.179; Funnel plot of right precentral gyrus, Egger’s test p = 0.30; Funnel plot of lenticular nucleus, putamen, Egger’s test p = 0.284; Funnel plot of left cerebellum, crus II, Egger’s test p = 0.894. RRMS < PPMS: Funnel plot of cingulate gyrus, Egger’s test p = 0.056; Funnel plot of left postcentral gyrus, Egger’s test p = 0.004; Funnel plot of right caudate nucleus, Egger’s test p = 0.729. Funnel plot of the right thalamus, Egger’s test p = 0.894; funnel plot of the left caudate nucleus, Egger’s test p = 0.081. Funnel plot of the right superior temporal gyrus, Egger’s test p = 0.399. (TIF 267 KB)

Supplementary file4 (DOCX 40 KB)

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Cao, Y., Diao, W., Tian, F. et al. Gray Matter Atrophy in the Cortico-Striatal-Thalamic Network and Sensorimotor Network in Relapsing–Remitting and Primary Progressive Multiple Sclerosis. Neuropsychol Rev 31, 703–720 (2021). https://doi.org/10.1007/s11065-021-09479-3

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