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Automatic Removal of False Connections in Diffusion MRI Tractography Using Topology-Informed Pruning (TIP)

  • Fang-Cheng Yeh
  • Sandip Panesar
  • Jessica Barrios
  • David Fernandes
  • Kumar Abhinav
  • Antonio Meola
  • Juan C. Fernandez-Miranda
Review

Abstract

Diffusion MRI fiber tracking provides a non-invasive method for mapping the trajectories of human brain connections, but its false connection problem has been a major challenge. This study introduces topology-informed pruning (TIP), a method that automatically identifies singular tracts and eliminates them to improve the tracking accuracy. The accuracy of the tractography with and without TIP was evaluated by a team of 6 neuroanatomists in a blinded setting to examine whether TIP could improve the accuracy. The results showed that TIP improved the tracking accuracy by 11.93% in the single-shell scheme and by 3.47% in the grid scheme. The improvement is significantly different from a random pruning (p value < 0.001). The diagnostic agreement between TIP and neuroanatomists was comparable to the agreement between neuroanatomists. The proposed TIP algorithm can be used to automatically clean-up noisy fibers in deterministic tractography, with a potential to confirm the existence of a fiber connection in basic neuroanatomical studies or clinical neurosurgical planning.

Key Words

Deterministic fiber tracking Tractography Topology Structural connectome Diffusion MRI 

Supplementary material

13311_2018_663_MOESM1_ESM.pdf (1.2 mb)
ESM 1 (PDF 1224 kb)

References

  1. 1.
    Reveley C, Seth AK, Pierpaoli C, Silva AC, Yu D, Saunders RC et al. Superficial white matter fiber systems impede detection of long-range cortical connections in diffusion MR tractography. Proc Natl Acad Sci U S A 2015;112(21):E2820–8. doi: https://doi.org/10.1073/pnas.1418198112.CrossRefPubMedPubMedCentralGoogle Scholar
  2. 2.
    Thomas C, Ye FQ, Irfanoglu MO, Modi P, Saleem KS, Leopold DA et al. Anatomical accuracy of brain connections derived from diffusion MRI tractography is inherently limited. Proc Natl Acad Sci U S A. 2014;111(46):16574–9. doi: https://doi.org/10.1073/pnas.1405672111 CrossRefPubMedPubMedCentralGoogle Scholar
  3. 3.
    Maier-Hein KH, Neher PF, Houde JC, Cote MA, Garyfallidis E, Zhong J et al. The challenge of mapping the human connectome based on diffusion tractography. Nat Commun. 2017;8(1):1349. doi: https://doi.org/10.1038/s41467-017-01285-x.CrossRefPubMedPubMedCentralGoogle Scholar
  4. 4.
    Jbabdi S, Sotiropoulos SN, Haber SN, Van Essen DC, Behrens TE. Measuring macroscopic brain connections in vivo. Nat Neurosci. 2015;18(11):1546–55. doi: https://doi.org/10.1038/nn.4134.CrossRefPubMedPubMedCentralGoogle Scholar
  5. 5.
    Yeh FC, Panesar S, Fernandes D, Meola A, Yoshino M, Fernandez-Miranda JC et al. Population-averaged atlas of the macroscale human structural connectome and its network topology. Neuroimage. 2018;178:57–68. doi: https://doi.org/10.1016/j.neuroimage.2018.05.027.CrossRefPubMedPubMedCentralGoogle Scholar
  6. 6.
    Smith RE, Tournier JD, Calamante F, Connelly A. Anatomically-constrained tractography: improved diffusion MRI streamlines tractography through effective use of anatomical information. Neuroimage. 2012;62(3):1924–38. doi: https://doi.org/10.1016/j.neuroimage.2012.06.005.CrossRefPubMedPubMedCentralGoogle Scholar
  7. 7.
    Tournier JD, Mori S, Leemans A. Diffusion tensor imaging and beyond. Magn Reson Med. 2011;65(6):1532–56. doi: https://doi.org/10.1002/mrm.22924.CrossRefPubMedPubMedCentralGoogle Scholar
  8. 8.
    Basser PJ, Pajevic S, Pierpaoli C, Duda J, Aldroubi A. In vivo fiber tractography using DT-MRI data. Magn Reson Med. 2000;44(4):625–32. doi: https://doi.org/10.1002/1522-2594(200010)44:4<625::AID-MRM17>3.0.CO;2-O CrossRefGoogle Scholar
  9. 9.
    Yeh FC, Verstynen TD, Wang Y, Fernandez-Miranda JC, Tseng WY. Deterministic diffusion fiber tracking improved by quantitative anisotropy. PLoS ONE. 2013;8(11):e80713. doi: https://doi.org/10.1371/journal.pone.0080713 CrossRefPubMedPubMedCentralGoogle Scholar
  10. 10.
    Yeh FC, Wedeen VJ, Tseng WY. Generalized q-sampling imaging. IEEE Trans Med Imaging. 2010;29(9):1626–35. doi: https://doi.org/10.1109/TMI.2010.2045126.CrossRefPubMedPubMedCentralGoogle Scholar
  11. 11.
    Yeh FC, Liu L, Hitchens TK, Wu YL. Mapping immune cell infiltration using restricted diffusion MRI. Magn Reson Med. 2017;77(2):603–12. doi: https://doi.org/10.1002/mrm.26143.CrossRefPubMedPubMedCentralGoogle Scholar
  12. 12.
    Pestilli F, Yeatman JD, Rokem A, Kay KN, Wandell BA. Evaluation and statistical inference for human connectomes. Nat Methods. 2014;11(10):1058–63. doi: https://doi.org/10.1038/nmeth.3098.CrossRefPubMedPubMedCentralGoogle Scholar
  13. 13.
    Modo M, Hitchens TK, Liu JR, Richardson RM. Detection of aberrant hippocampal mossy fiber connections: Ex vivo mesoscale diffusion MRI and microtractography with histological validation in a patient with uncontrolled temporal lobe epilepsy. Hum Brain Mapp. 2016;37(2):780–95. doi: https://doi.org/10.1002/hbm.23066.CrossRefPubMedPubMedCentralGoogle Scholar
  14. 14.
    Meola A, Comert A, Yeh FC, Sivakanthan S, Fernandez-Miranda JC. The nondecussating pathway of the dentatorubrothalamic tract in humans: human connectome-based tractographic study and microdissection validation. J Neurosurg. 2016;124(5):1406–12. doi: https://doi.org/10.3171/2015.4.JNS142741.CrossRefPubMedPubMedCentralGoogle Scholar
  15. 15.
    Meola A, Comert A, Yeh FC, Stefaneanu L, Fernandez-Miranda JC. The controversial existence of the human superior fronto-occipital fasciculus: Connectome-based tractographic study with microdissection validation. Hum Brain Mapp. 2015;36(12):4964–71. doi: https://doi.org/10.1002/hbm.22990.CrossRefPubMedPubMedCentralGoogle Scholar
  16. 16.
    Yeatman JD, Weiner KS, Pestilli F, Rokem A, Mezer A, Wandell BA. The vertical occipital fasciculus: a century of controversy resolved by in vivo measurements. Proc Natl Acad Sci U S A. 2014;111(48):E5214–23. doi: https://doi.org/10.1073/pnas.1418503111.CrossRefPubMedPubMedCentralGoogle Scholar

Copyright information

© The American Society for Experimental NeuroTherapeutics, Inc. 2018

Authors and Affiliations

  1. 1.Department of Neurological SurgeryUniversity of Pittsburgh Medical CenterPittsburghUSA
  2. 2.Department of BioengineeringUniversity of Pittsburgh Medical CenterPittsburghUSA
  3. 3.Department of NeurosurgeryStanford University School of MedicineStanfordUSA

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