Reduced Network Dynamics on Functional MRI Signals Cognitive Impairment in Multiple Sclerosis

Background Previous studies have demonstrated extensive functional network disturbances in patients with multiple sclerosis (MS), showing a less efficient brain network. Recent studies indicate that the dynamic properties of the brain network show a strong correlation with cognitive function. Purpos...

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Published in:Radiology Vol. 292; no. 2; p. 449
Main Authors: Eijlers, Anand J C, Wink, Alle Meije, Meijer, Kim A, Douw, Linda, Geurts, Jeroen J G, Schoonheim, Menno M
Format: Journal Article
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Published: United States 01.08.2019
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Abstract Background Previous studies have demonstrated extensive functional network disturbances in patients with multiple sclerosis (MS), showing a less efficient brain network. Recent studies indicate that the dynamic properties of the brain network show a strong correlation with cognitive function. Purpose To investigate network dynamics on functional MRI in cognitively impaired patients with MS. Materials and Methods In secondary analysis of prospectively acquired data, with imaging performed between 2008 and 2012, differences in regional functional network dynamics (ie, eigenvector centrality dynamics) between cognitively impaired and cognitively preserved participants with MS were investigated. Functional network dynamics were computed on images from functional MRI (3 T) by using a sliding-window approach. Cognitively impaired and preserved groups were compared by using a clusterwise permutation-based method. Results The study included 96 healthy control subjects and 332 participants with MS (including 226 women and 106 men; median age, 48.1 years ± 11.0). Among the 332 participants with MS, 87 were cognitively impaired and 180 had preserved cognitive function; mildly impaired patients ( = 65) were excluded. The cognitively impaired group included a higher proportion of men compared with the cognitively preserved group (35 of 87 [40%] vs 48 of 180 [27%], respectively; = .02) and had a higher mean age (51.1 years vs 46.3 years, respectively; < .01). The clusterwise permutation-based comparison at less than .05 showed reduced centrality dynamics in default-mode, frontoparietal, and visual network regions on functional MRI in cognitively impaired participants versus cognitively preserved participants. A subsequent correlation and hierarchical clustering analysis revealed that the default-mode and visual networks normally demonstrate negatively correlated fluctuations in functional importance ( = -0.23 in healthy control subjects), with an almost complete loss of this negative correlation in cognitively impaired participants compared with cognitively preserved participants ( = -0.04 vs = -0.14; corrected = .02 . Conclusion As shown on functional MRI, cognitively impaired patients with multiple sclerosis not only demonstrate reduced dynamics in default-mode, frontoparietal, and visual networks, but also show a loss of interplay between default-mode and visual networks. © RSNA, 2019 See also the article by Eijlers et al and the editorial by Zivadinov and Dwyer in this issue.
AbstractList Background Previous studies have demonstrated extensive functional network disturbances in patients with multiple sclerosis (MS), showing a less efficient brain network. Recent studies indicate that the dynamic properties of the brain network show a strong correlation with cognitive function. Purpose To investigate network dynamics on functional MRI in cognitively impaired patients with MS. Materials and Methods In secondary analysis of prospectively acquired data, with imaging performed between 2008 and 2012, differences in regional functional network dynamics (ie, eigenvector centrality dynamics) between cognitively impaired and cognitively preserved participants with MS were investigated. Functional network dynamics were computed on images from functional MRI (3 T) by using a sliding-window approach. Cognitively impaired and preserved groups were compared by using a clusterwise permutation-based method. Results The study included 96 healthy control subjects and 332 participants with MS (including 226 women and 106 men; median age, 48.1 years ± 11.0). Among the 332 participants with MS, 87 were cognitively impaired and 180 had preserved cognitive function; mildly impaired patients ( = 65) were excluded. The cognitively impaired group included a higher proportion of men compared with the cognitively preserved group (35 of 87 [40%] vs 48 of 180 [27%], respectively; = .02) and had a higher mean age (51.1 years vs 46.3 years, respectively; < .01). The clusterwise permutation-based comparison at less than .05 showed reduced centrality dynamics in default-mode, frontoparietal, and visual network regions on functional MRI in cognitively impaired participants versus cognitively preserved participants. A subsequent correlation and hierarchical clustering analysis revealed that the default-mode and visual networks normally demonstrate negatively correlated fluctuations in functional importance ( = -0.23 in healthy control subjects), with an almost complete loss of this negative correlation in cognitively impaired participants compared with cognitively preserved participants ( = -0.04 vs = -0.14; corrected = .02 . Conclusion As shown on functional MRI, cognitively impaired patients with multiple sclerosis not only demonstrate reduced dynamics in default-mode, frontoparietal, and visual networks, but also show a loss of interplay between default-mode and visual networks. © RSNA, 2019 See also the article by Eijlers et al and the editorial by Zivadinov and Dwyer in this issue.
Background Previous studies have demonstrated extensive functional network disturbances in patients with multiple sclerosis (MS), showing a less efficient brain network. Recent studies indicate that the dynamic properties of the brain network show a strong correlation with cognitive function. Purpose To investigate network dynamics on functional MRI in cognitively impaired patients with MS. Materials and Methods In secondary analysis of prospectively acquired data, with imaging performed between 2008 and 2012, differences in regional functional network dynamics (ie, eigenvector centrality dynamics) between cognitively impaired and cognitively preserved participants with MS were investigated. Functional network dynamics were computed on images from functional MRI (3 T) by using a sliding-window approach. Cognitively impaired and preserved groups were compared by using a clusterwise permutation-based method. Results The study included 96 healthy control subjects and 332 participants with MS (including 226 women and 106 men; median age, 48.1 years ± 11.0). Among the 332 participants with MS, 87 were cognitively impaired and 180 had preserved cognitive function; mildly impaired patients (n = 65) were excluded. The cognitively impaired group included a higher proportion of men compared with the cognitively preserved group (35 of 87 [40%] vs 48 of 180 [27%], respectively; P = .02) and had a higher mean age (51.1 years vs 46.3 years, respectively; P < .01). The clusterwise permutation-based comparison at P less than .05 showed reduced centrality dynamics in default-mode, frontoparietal, and visual network regions on functional MRI in cognitively impaired participants versus cognitively preserved participants. A subsequent correlation and hierarchical clustering analysis revealed that the default-mode and visual networks normally demonstrate negatively correlated fluctuations in functional importance (r = -0.23 in healthy control subjects), with an almost complete loss of this negative correlation in cognitively impaired participants compared with cognitively preserved participants (r = -0.04 vs r = -0.14; corrected P = .02). Conclusion As shown on functional MRI, cognitively impaired patients with multiple sclerosis not only demonstrate reduced dynamics in default-mode, frontoparietal, and visual networks, but also show a loss of interplay between default-mode and visual networks. © RSNA, 2019 Online supplemental material is available for this article. See also the article by Eijlers et al and the editorial by Zivadinov and Dwyer in this issue.Background Previous studies have demonstrated extensive functional network disturbances in patients with multiple sclerosis (MS), showing a less efficient brain network. Recent studies indicate that the dynamic properties of the brain network show a strong correlation with cognitive function. Purpose To investigate network dynamics on functional MRI in cognitively impaired patients with MS. Materials and Methods In secondary analysis of prospectively acquired data, with imaging performed between 2008 and 2012, differences in regional functional network dynamics (ie, eigenvector centrality dynamics) between cognitively impaired and cognitively preserved participants with MS were investigated. Functional network dynamics were computed on images from functional MRI (3 T) by using a sliding-window approach. Cognitively impaired and preserved groups were compared by using a clusterwise permutation-based method. Results The study included 96 healthy control subjects and 332 participants with MS (including 226 women and 106 men; median age, 48.1 years ± 11.0). Among the 332 participants with MS, 87 were cognitively impaired and 180 had preserved cognitive function; mildly impaired patients (n = 65) were excluded. The cognitively impaired group included a higher proportion of men compared with the cognitively preserved group (35 of 87 [40%] vs 48 of 180 [27%], respectively; P = .02) and had a higher mean age (51.1 years vs 46.3 years, respectively; P < .01). The clusterwise permutation-based comparison at P less than .05 showed reduced centrality dynamics in default-mode, frontoparietal, and visual network regions on functional MRI in cognitively impaired participants versus cognitively preserved participants. A subsequent correlation and hierarchical clustering analysis revealed that the default-mode and visual networks normally demonstrate negatively correlated fluctuations in functional importance (r = -0.23 in healthy control subjects), with an almost complete loss of this negative correlation in cognitively impaired participants compared with cognitively preserved participants (r = -0.04 vs r = -0.14; corrected P = .02). Conclusion As shown on functional MRI, cognitively impaired patients with multiple sclerosis not only demonstrate reduced dynamics in default-mode, frontoparietal, and visual networks, but also show a loss of interplay between default-mode and visual networks. © RSNA, 2019 Online supplemental material is available for this article. See also the article by Eijlers et al and the editorial by Zivadinov and Dwyer in this issue.
Author Schoonheim, Menno M
Douw, Linda
Wink, Alle Meije
Meijer, Kim A
Eijlers, Anand J C
Geurts, Jeroen J G
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  organization: From the Departments of Anatomy and Neurosciences (A.J.C.E., K.A.M., L.D., J.J.G.G., M.M.S.) and Radiology and Nuclear Medicine (A.M.W.), MS Center Amsterdam, Amsterdam UMC, Locatie VUmc, Amsterdam Neuroscience, De Boelelaan 1117, PO Box 7057, 1007 MB, Amsterdam, the Netherlands
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  organization: From the Departments of Anatomy and Neurosciences (A.J.C.E., K.A.M., L.D., J.J.G.G., M.M.S.) and Radiology and Nuclear Medicine (A.M.W.), MS Center Amsterdam, Amsterdam UMC, Locatie VUmc, Amsterdam Neuroscience, De Boelelaan 1117, PO Box 7057, 1007 MB, Amsterdam, the Netherlands
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  givenname: Jeroen J G
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  organization: From the Departments of Anatomy and Neurosciences (A.J.C.E., K.A.M., L.D., J.J.G.G., M.M.S.) and Radiology and Nuclear Medicine (A.M.W.), MS Center Amsterdam, Amsterdam UMC, Locatie VUmc, Amsterdam Neuroscience, De Boelelaan 1117, PO Box 7057, 1007 MB, Amsterdam, the Netherlands
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  givenname: Menno M
  orcidid: 0000-0002-2504-6959
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  organization: From the Departments of Anatomy and Neurosciences (A.J.C.E., K.A.M., L.D., J.J.G.G., M.M.S.) and Radiology and Nuclear Medicine (A.M.W.), MS Center Amsterdam, Amsterdam UMC, Locatie VUmc, Amsterdam Neuroscience, De Boelelaan 1117, PO Box 7057, 1007 MB, Amsterdam, the Netherlands
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Snippet Background Previous studies have demonstrated extensive functional network disturbances in patients with multiple sclerosis (MS), showing a less efficient...
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SubjectTerms Brain - diagnostic imaging
Brain - physiopathology
Brain Mapping - methods
Cognitive Dysfunction - complications
Cognitive Dysfunction - physiopathology
Female
Humans
Magnetic Resonance Imaging - methods
Male
Middle Aged
Multiple Sclerosis - complications
Multiple Sclerosis - physiopathology
Prospective Studies
Title Reduced Network Dynamics on Functional MRI Signals Cognitive Impairment in Multiple Sclerosis
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