Cited by 19Advanced Neuroimaging Techniques and ApplicationsFunctional Brain Connectivity StudiesComplex Network Analysis Techniques

Diffusion MRI tractography filtering techniques change the topology of structural connectomes

Open access
Frigo, Matteo, Deslauriers-Gauthier, Samuel, Parker, Drew, Aziz Ould Ismail, Abdol, John Kim, Junghoon, Verma, Ragini, Deriche, Rachid·2020·Journal of Neural Engineering

Abstract

Abstract Objective. The use of non-invasive techniques for the estimation of structural brain networks (i.e. connectomes) opened the door to large-scale investigations on the functioning and the architecture of the brain, unveiling the link between neurological disorders and topological changes of the brain network. This study aims at assessing if and how the topology of structural connectomes estimated non-invasively with diffusion MRI is affected by the employment of tractography filtering techniques in structural connectomic pipelines. Additionally, this work investigates the robustness of topological descriptors of filtered connectomes to the common practice of density-based thresholding. Approach. We investigate the changes in global efficiency, characteristic path length, modularity and clustering coefficient on filtered connectomes obtained with the spherical deconvolution informed filtering of tractograms and using the convex optimization modelling for microstructure informed tractography. The analysis is performed on both healthy subjects and patients affected by traumatic brain injury and with an assessment of the robustness of the computed graph-theoretical measures with respect to density-based thresholding of the connectome. Main results. Our results demonstrate that tractography filtering techniques change the topology of brain networks, and thus alter network metrics both in the pathological and the healthy cases. Moreover, the measures are shown to be robust to density-based thresholding. Significance. The present work highlights how the inclusion of tractography filtering techniques in connectomic pipelines requires extra caution as they systematically change the network topology both in healthy subjects and patients affected by traumatic brain injury. Finally, the practice of low-to-moderate density-based thresholding of the connectomes is confirmed to have negligible effects on the topological analysis.

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

A few free checks a day · papers already verified open instantly · results are public

Integrity signals

Registry

Crossref · 10.1088/1741-2552/abc29b

Cites

4 of 4 references verified0 citation errors · 0 not checkable

Statistics

Claims the paper makes

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

A few free checks a day · papers already verified open instantly · results are public

Claims other papers make about this one

Each is checked against this paper’s own text: does it say what the citing paper says it does?

  • Selection of tractography filtering strategies is important and has been shown to affect the analysis of the topology of brain networks and affect sensitivity and specificity when analyzing connectomes.

    “Selection of tractography filtering strategies is important and has been shown to affect the analysis of the topology of brain networks (Civier et al., 2019; Frigo et al., 2020; Yeh et al., 2016a) and affect sensitivity and specificity when analyzing the connectomes (Zalesky et al., 2016a).”

Self-check

Percentages, sums and reported differences re-computed from the paper’s own numbers.

The self-check needs the paper’s full text.

Cites

Flagged first, then by citations

Research works printed but not linked: 50

  1. [1]Deriche Rachid. “ Computational brain connectivity mapping: A core health and scientific challenge”. In: Medical Image Analysis 33 (2016), pp. 122– 126. 27338172
  2. [2]Sporns Olaf, Tononi Giulio, and Kötter Rolf. “ The human connectome: a structural description of the human brain”. In: PLoS computational biology 1.4 (2005), e42. 16201007 PMC1239902
  3. [4]Bassett Danielle S and Bullmore Edward T. “ Small-world brain networks revisited”. In: The Neuroscientist 23.5 (2017), pp. 499– 516. 27655008 PMC5603984
  4. [5]Verma Ragini “ Neuroimaging Findings in US Government Personnel With Possible Exposure to Directional Phenomena in Havana, Cuba”. In: Jama 322.4 (2019), pp. 336– 347. PMC6652163 31334794
  5. [6]Yeh Chun-Hung “ Connectomes from streamlines tractography: Assigning streamlines to brain parcellations is not trivial but highly consequential”. In: NeuroImage 199 (2019), pp. 160– 171. issn: 1053-8119. doi: 10.1016/j.neuroimage.2019.05.005. 31082471 · DOI
  6. [7]Marco Catani and Michel Thiebaut de Schotten. Atlas of human brain connections. Oxford University Press, 2012.
  7. [9]Smith Robert E “ The effects of SIFT on the reproducibility and biological accuracy of the structural connectome”. In: Neuroimage 104 (2015), pp. 253– 265. 25312774
  8. [10]Rheault Francois “ Common misconceptions, hidden biases and modern challenges of dMRI tractography”. In: Journal of Neural Engineering (2020). 31931484
  9. [11]Maier-Hein Klaus H “ The challenge of mapping the human connectome based on diffusion tractography”. In: Nature communications 8.1 (2017), p. 1349. PMC5677006 29116093
  10. [12]Civier Oren “ Is removal of weak connections necessary for graph-theoretical analysis of dense weighted structural connectomes from diffusion MRI?” In: NeuroImage 194 (2019), pp. 68– 81. 30844506
  11. [13]Smith Robert E “ SIFT2: Enabling dense quantitative assessment of brain white matter connectivity using streamlines tractography”. In: Neuroimage 119 (2015), pp. 338– 351. 26163802
  12. [14]Daducci Alessandro “ COMMIT: convex optimization modeling for microstructure informed tractography”. In: IEEE transactions on medical imaging 34.1 (2014), pp. 246– 257. 25167548
  13. [15]Pestilli Franco “ Evaluation and statistical inference for human connectomes”. In: Nature methods 11.10 (2014), p. 1058. PMC4180802 25194848
  14. [16]Sporns Olaf “ Organization, development and function of complex brain networks”. In: Trends in cognitive sciences 8.9 (2004), pp. 418– 425. 15350243
  15. [17]Yu Shan “ A small world of neuronal synchrony”. In: Cerebral cortex 18.12 (2008), pp. 2891– 2901. PMC2583154 18400792
  16. [18]Bassett Danielle Smith and Bullmore ED. “ Small-world brain networks”. In: The neuroscientist 12.6 (2006), pp. 512– 523. 17079517
  17. [19]Verma Ragini, Osmanlioglu Yusuf, and Ould Ismail Abdol Aziz. “ Multimodal Patho-Connectomics of Brain Injury”. In: International MICCAI Brainlesion Workshop. Springer. 2018, pp. 3– 14.
  18. [21]Mohammadian Mehrbod “ High angular resolution diffusion-weighted imaging in mild traumatic brain injury”. In: NeuroImage: Clinical 13 (2017), pp. 174– 180. PMC5144744 27981032
  19. [22]Glasser Matthew F “ The minimal preprocessing pipelines for the Human Connectome Project”. In: Neuroimage 80 (2013), pp. 105– 124. PMC3720813 23668970
  20. [23]Yeh Chun-Hung “ Correction for diffusion MRI fibre tracking biases: The consequences for structural connectomic metrics”. In: Neuroimage 142 (2016), pp. 150– 162. 27211472
  21. [25]Zalesky Andrew “ Connectome sensitivity or specificity: which is more important?” In: Neuroimage 142 (2016), pp. 407– 420. 27364472
  22. [26]Fornito Alex, Zalesky Andrew, and Breakspear Michael. “ Graph analysis of the human connectome: promise, progress, and pitfalls”. In: Neuroimage 80 (2013), pp. 426– 444. 23643999
  23. [27]Sotiropoulos Stamatios N and Zalesky Andrew. “ Building connectomes using diffusion MRI: why, how and but”. In: NMR in Biomedicine 32.4 (2019), e3752. 28654718 PMC6491971
  24. [28]Milgram Stanley. “ The small world problem”. In: Psychology today 2.1 (1967), pp. 60– 67.
  25. [29]Rubinov Mikail and Sporns Olaf. “ Complex network measures of brain connectivity: uses and interpretations”. In: Neuroimage 52.3 (2010), pp. 1059– 1069. 19819337
  26. [30]Dijkstra Edsger W. “ A note on two problems in connexion with graphs”. In: Numerische mathematik 1.1 (1959), pp. 269– 271.
  27. [31]Latora Vito and Marchiori Massimo. “ Efficient behavior of small-world networks”. In: Physical review letters 87.19 (2001), p. 198701. 11690461
  28. [32]Zhang Bin and Horvath Steve. “ A general framework for weighted gene coexpression network analysis”. In: Statistical applications in genetics and molecular biology 4.1 (2005). 16646834
  29. [33]Opsahl Tore and Panzarasa Pietro. “ Clustering in weighted networks”. In: Social networks 31.2 (2009), pp. 155– 163.
  30. [34]Newman Mark EJ. “ Analysis of weighted networks”. In: Physical review E 70.5 (2004), p. 056131. 15600716
  31. [35]Van Essen David C “ The Human Connectome Project: a data acquisition perspective”. In: Neuroimage 62.4 (2012), pp. 2222– 2231. PMC3606888 22366334
  32. [37]Sotiropoulos Stamatios N “ Advances in diffusion MRI acquisition and processing in the Human Connectome Project”. In: Neuroimage 80 (2013), pp. 125– 143. PMC3720790 23702418
  33. [38]Andersson Jesper LR, Skare Stefan, and Ashburner John. “ How to correct susceptibility distortions in spin-echo echo-planar images: application to diffusion tensor imaging”. In: Neuroimage 20.2 (2003), pp. 870– 888. 14568458
  34. [39]Jenkinson Mark “ Fsl”. In: Neuroimage 62.2 (2012), pp. 782– 790. 21979382
  35. [40]Andersson JLR “ A comprehensive Gaussian process framework for correcting distortions and movements in diffusion images”. In: Proceedings of the 20th Annual Meeting of ISMRM. Vol. 20. 2012, p. 2426.
  36. [41]Rabinowitz Amanda R “ Neuropsychological recovery trajectories in moderate to severe traumatic brain injury: influence of patient characteristics and diffuse axonal injury”. In: Journal of the International Neuropsychological Society 24.3 (2018), pp. 237– 246. 29032776 PMC5957498
  37. [42]Manjón José V “ Diffusion weighted image denoising using overcomplete local PCA”. In: PloS one 8.9 (2013), e73021. 24019889 PMC3760829
  38. [43]Smith Stephen M. “ Fast robust automated brain extraction”. In: Human brain mapping 17.3 (2002), pp. 143– 155. PMC6871816 12391568
  39. [44]Andersson Jesper LRand Sotiropoulos Stamatios N. “ An integrated approach to correction for off-resonance effects and subject movement in diffusion MR imaging”. In: Neuroimage 125 (2016), pp. 1063– 1078. PMC4692656 26481672
  40. [45]Smith Robert E “ Anatomically-constrained tractography: improved diffusion MRI streamlines tractography through effective use of anatomical information”. In: Neuroimage 62.3 (2012), pp. 1924– 1938. 22705374
  41. [46]Fischl Bruce. “ FreeSurfer”. In: Neuroimage 62.2 (2012), pp. 774– 781. PMC3685476 22248573
  42. [48]Jeurissen Ben “ Multi-tissue constrained spherical deconvolution for improved analysis of multi-shell diffusion MRI data”. In: NeuroImage 103 (2014), pp. 411– 426. 25109526
  43. [49]Tournier J-Donald “ Direct estimation of the fiber orientation density function from diffusion-weighted MRI data using spherical deconvolution”. In: NeuroImage 23.3 (2004), pp. 1176– 1185. 15528117
  44. [50]Dhollander Thijs, Raffelt David, and Connelly Alan. “ Unsupervised 3-tissue response function estimation from single-shell or multi-shell diffusion MR data without a co-registered T1 image”. In: ISMRM Workshop on Breaking the Barriers of Diffusion MRI. Vol. 5. 2016.
  45. [51]Tournier J-Donald, Calamante Fernando, and Connelly Alan. “ Robust determination of the fibre orientation distribution in diffusion MRI: non-negativity constrained super-resolved spherical deconvolution”. In: Neuroimage 35.4 (2007), pp. 1459– 1472. 17379540
  46. [52]Desikan Rahul S “ An automated labeling system for subdividing the human cerebral cortex on MRI scans into gyral based regions of interest”. In: Neuroimage 31.3 (2006), pp. 968– 980. 16530430
  47. [53]Panagiotaki Eleftheria “ Compartment models of the diffusion MR signal in brain white matter: a taxonomy and comparison”. In: Neuroimage 59.3 (2012), pp. 2241– 2254. 22001791
  48. [54]Blondel Vincent D “ Fast unfolding of communities in large networks”. In: Journal of statistical mechanics: theory and experiment 2008. 10 (2008), P10008.
  49. [55]Mann Henry B and Whitney Donald R. “ On a test of whether one of two random variables is stochastically larger than the other”. In: The annals of mathematical statistics (1947), pp. 50– 60.
  50. [56]Benjamini Yoav and Hochberg Yosef. “ Controlling the false discovery rate: a practical and powerful approach to multiple testing”. In: Journal of the Royal statistical society: series B (Methodological) 57.1 (1995), pp. 289– 300.

Cited by

Sorted by citations

Authors
Frigo, M., Deslauriers-Gauthier, S., Parker, D., Aziz Ould Ismail, A., John Kim, J., Verma, R., & Deriche, R.
Affiliations
  • Université Côte d'Azur (FR)
  • University of Pennsylvania (US)
Corresponding author
Frigo, Matteo
Venue
Journal of Neural Engineering
Published
2020-11-11
Volume
17
Issue
6
Pages
065002
ISSN
  • 1741-2552 (ISSN-L)
  • 1741-2560
OpenAlex
W3093146773
Cited by
19
References
4
Citations by year
2026: 3 · 2025: 3 · 2024: 2 · 2023: 4 · 2022: 3 · 2021: 4
FWCI
1.34
Type
journal article
Language
en
Open access
Locations
  • Journal of Neural Engineering (publishedVersion)
  • PubMed (publishedVersion)
  • PubMed Central (acceptedVersion)
  • HAL (submittedVersion, other-oa)
  • OSF Preprints (OSF Preprints) (submittedVersion)
Funders
  • H2020 European Research Council (694665)
  • Center for Scientific Review (R01NS065980)
  • Pennsylvania Department of Health (PACT)
  • NIH Blueprint for Neuroscience Research (1U54MH091657)
Topics
  • Health Sciences › Medicine › Radiology, Nuclear Medicine and Imaging › Advanced Neuroimaging Techniques and Applications
  • Life Sciences › Neuroscience › Cognitive Neuroscience › Functional Brain Connectivity Studies
  • Physical Sciences › Physics and Astronomy › Statistical and Nonlinear Physics › Complex Network Analysis Techniques
Keywords
structural connectome, diffusion MRI, brain network topology, traumatic brain injury, global efficiency, average path length, modularity, clustering coefficient
MeSH terms
Brain, Humans, Diffusion Tensor Imaging, Connectome

About these checks

Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.

Statistics and arithmetic are recomputed, not judged.

Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.

What counts as a claim ›How we measure confidence ›How we check this ›

Are you an author, or do you see a problem with this page? Request a review