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Brain Imaging and Behavior

, Volume 10, Issue 4, pp 1117–1126 | Cite as

Changes in brain functional connectivity patterns are driven by an individual lesion in MS: a resting-state fMRI study

  • Amgad Droby
  • Kenneth S. L. Yuen
  • Muthuraman Muthuraman
  • Sarah-Christina Reitz
  • Vinzenz Fleischer
  • Johannes Klein
  • René-Maxime Gracien
  • Ulf Ziemann
  • Ralf Deichmann
  • Frauke Zipp
  • Sergiu Groppa
Original Research

Abstract

Diffuse inflammation in multiple sclerosis (MS) extends beyond focal lesion sites, affecting interconnected regions; however, little is known about the impact of an individual lesion affecting major white matter (WM) pathways on brain functional connectivity (FC). Here, we longitudinally assessed the effects of acute and chronic lesions on FC in relapsing-remitting MS (RRMS) patients using resting-state fMRI. 45 MRI data sets from 9 RRMS patients were recorded using 3T MR scanner over 5 time points at 8 week intervals. Patients were divided into two groups based on the presence (n = 5; MS+) and absence (n = 4; MS-) of a lesion at a predilection site for MS. While FC levels were found not to fluctuate significantly in the overall patient group, the MS+ patient group showed increased FC in the contralateral cuneus and precuneus and in the ipsilateral precuneus (p < 0.01, corrected). This can be interpreted as the recruitment of intact cortical regions to compensate for tissue damage. During the study, one patient developed an acute WM lesion in the left posterior periventricular space. A marked increase in FC in the right pre-, post-central gyrus, right superior frontal gyrus, the left cuneus, the vermis and the posterior and anterior lobes of the cerebellum was noted following the clinical relapse, which gradually decreased in subsequent follow-ups, suggesting short-term functional reorganization during the acute phase. This strongly suggests that the lesion-related network changes observed in patients with chronic lesions occur as a result of reorganization processes following the initial appearance of an acute lesion.

Keywords

Compensation Functional connectivity Neuroplasticity rs-fMRI 

Notes

Compliance with ethical standards

This study was performed in accordance with the ethical standards of the institutional and/or national research committee and with the 1964 Helsinki declaration and its later amendments or comparable ethical standards. Informed consent was obtained from all individual participants included in the study.

Funding

This work has been supported by grants from the German Research Foundation (DFG; CRC-TR 128/B5 to Drs. Deichmann and Zipp).

Conflict of interest

None of the authors declare any relevant conflicts of interest.

Supplementary material

11682_2015_9476_MOESM1_ESM.docx (15 kb)
Supplementary Table 1 (DOCX 15 kb)
11682_2015_9476_Fig5_ESM.gif (50 kb)
Supplementary Fig. 1

T1-weighted MPRAGE images time series demonstrating the newly detected WM lesion in the reported single-case patient. The new lesion was detected on the first MRI-follow-up session (red circle) and was still visible throughout the follow-up period. (GIF 50 kb)

11682_2015_9476_MOESM2_ESM.tif (6.4 mb)
High resolution image (TIF 6526 kb)

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Copyright information

© Springer Science+Business Media New York 2015

Authors and Affiliations

  • Amgad Droby
    • 1
    • 2
  • Kenneth S. L. Yuen
    • 2
  • Muthuraman Muthuraman
    • 1
    • 2
  • Sarah-Christina Reitz
    • 3
    • 4
  • Vinzenz Fleischer
    • 1
  • Johannes Klein
    • 3
    • 4
  • René-Maxime Gracien
    • 3
    • 4
  • Ulf Ziemann
    • 5
  • Ralf Deichmann
    • 4
  • Frauke Zipp
    • 1
    • 2
  • Sergiu Groppa
    • 1
    • 2
  1. 1.Department of NeurologyUniversity Medical Centre of the Johannes Gutenberg University MainzMainzGermany
  2. 2.Neuroimaging Center (NIC) of the Focus Program Translational Neuroscience (FTN)Johannes Gutenberg University MainzMainzGermany
  3. 3.Department of NeurologyUniversity Hospital FrankfurtFrankfurt am MainGermany
  4. 4.Brain Imaging Center (BIC)Goethe UniversityFrankfurt am MainGermany
  5. 5.Department of Neurology and Stroke, Hertie Institute for Clinical Brain ResearchEberhard-Karls-UniversityTübingenGermany

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