A registration method for improving quantitative assessment in probabilistic diffusion tractography

Jeff L Waugh, J. K. Kuster, M. L. Makhlouf, J. M. Levenstein, T. J. Multhaupt-Buell, S. K. Warfield, N. Sharma, A. J. Blood

Research output: Contribution to journalArticle

Abstract

Diffusion MRI-based probabilistic tractography is a powerful tool for non-invasively investigating normal brain architecture and alterations in structural connectivity associated with disease states. Both voxelwise and region-of-interest methods of analysis are capable of integrating population differences in tract amplitude (streamline count or density), given proper alignment of the tracts of interest. However, quantification of tract differences (between groups, or longitudinally within individuals) has been hampered by two related features of white matter. First, it is unknown to what extent healthy individuals differ in the precise location of white matter tracts, and to what extent experimental factors influence perceived tract location. Second, white matter lacks the gross neuroanatomical features (e.g., gyri, histological subtyping) that make parcellation of grey matter plausible – determining where tracts “should” lie within larger white matter structures is difficult. Accurately quantifying tractographic connectivity between individuals is thus inherently linked to the difficulty of identifying and aligning precise tract location. Tractography is often utilized to study neurological diseases in which the precise structural and connectivity abnormalities are unknown, underscoring the importance of accounting for individual differences in tract location when evaluating the strength of structural connectivity. We set out to quantify spatial variance in tracts aligned through a standard, whole-brain registration method, and to assess the impact of location mismatch on groupwise assessments of tract amplitude. We then developed a method for tract alignment that enhances the existing standard whole brain registration, and then tested whether this method improved the reliability of groupwise contrasts. Specifically, we conducted seed-based probabilistic diffusion tractography from primary motor, supplementary motor, and visual cortices, projecting through the corpus callosum. Streamline counts decreased rapidly with movement from the tract center (−35% per millimeter); tract misalignment of a few millimeters caused substantial compromise of amplitude comparisons. Alignment of tracts “peak-to-peak” is essential for accurate amplitude comparisons. However, for all transcallosal tracts registered through the whole-brain method, the mean separation distance between an individual subject's tract and the average tract (3.2 mm) precluded accurate comparison: at this separation, tract amplitudes were reduced by 74% from peak value. In contrast, alignment of subcortical tracts (thalamo-putaminal, pallido-rubral) was substantially better than alignment for cortical tracts; whole-brain registration was sufficient for these subcortical tracts. We demonstrated that location mismatches in cortical tractography were sufficient to produce false positive and false negative amplitude estimates in both groupwise and longitudinal comparisons. We then showed that our new tract alignment method substantially reduced location mismatch and improved both reliability and statistical power of subsequent quantitative comparisons.

Original languageEnglish (US)
Pages (from-to)288-306
Number of pages19
JournalNeuroImage
Volume189
DOIs
StatePublished - Apr 1 2019

Fingerprint

Diffusion Tensor Imaging
Brain
Diffusion Magnetic Resonance Imaging
Corpus Callosum
Motor Cortex
Visual Cortex
Individuality
Seeds
White Matter
Population

Keywords

  • Center of gravity
  • Dice similarity coefficient
  • Longitudinal
  • Quantitative
  • Registration
  • Tractography

ASJC Scopus subject areas

  • Neurology
  • Cognitive Neuroscience

Cite this

Waugh, J. L., Kuster, J. K., Makhlouf, M. L., Levenstein, J. M., Multhaupt-Buell, T. J., Warfield, S. K., ... Blood, A. J. (2019). A registration method for improving quantitative assessment in probabilistic diffusion tractography. NeuroImage, 189, 288-306. https://doi.org/10.1016/j.neuroimage.2018.12.057

A registration method for improving quantitative assessment in probabilistic diffusion tractography. / Waugh, Jeff L; Kuster, J. K.; Makhlouf, M. L.; Levenstein, J. M.; Multhaupt-Buell, T. J.; Warfield, S. K.; Sharma, N.; Blood, A. J.

In: NeuroImage, Vol. 189, 01.04.2019, p. 288-306.

Research output: Contribution to journalArticle

Waugh, JL, Kuster, JK, Makhlouf, ML, Levenstein, JM, Multhaupt-Buell, TJ, Warfield, SK, Sharma, N & Blood, AJ 2019, 'A registration method for improving quantitative assessment in probabilistic diffusion tractography' NeuroImage, vol. 189, pp. 288-306. https://doi.org/10.1016/j.neuroimage.2018.12.057
Waugh, Jeff L ; Kuster, J. K. ; Makhlouf, M. L. ; Levenstein, J. M. ; Multhaupt-Buell, T. J. ; Warfield, S. K. ; Sharma, N. ; Blood, A. J. / A registration method for improving quantitative assessment in probabilistic diffusion tractography. In: NeuroImage. 2019 ; Vol. 189. pp. 288-306.
@article{0c475ef580df4416aed5c6a2e79ca776,
title = "A registration method for improving quantitative assessment in probabilistic diffusion tractography",
abstract = "Diffusion MRI-based probabilistic tractography is a powerful tool for non-invasively investigating normal brain architecture and alterations in structural connectivity associated with disease states. Both voxelwise and region-of-interest methods of analysis are capable of integrating population differences in tract amplitude (streamline count or density), given proper alignment of the tracts of interest. However, quantification of tract differences (between groups, or longitudinally within individuals) has been hampered by two related features of white matter. First, it is unknown to what extent healthy individuals differ in the precise location of white matter tracts, and to what extent experimental factors influence perceived tract location. Second, white matter lacks the gross neuroanatomical features (e.g., gyri, histological subtyping) that make parcellation of grey matter plausible – determining where tracts “should” lie within larger white matter structures is difficult. Accurately quantifying tractographic connectivity between individuals is thus inherently linked to the difficulty of identifying and aligning precise tract location. Tractography is often utilized to study neurological diseases in which the precise structural and connectivity abnormalities are unknown, underscoring the importance of accounting for individual differences in tract location when evaluating the strength of structural connectivity. We set out to quantify spatial variance in tracts aligned through a standard, whole-brain registration method, and to assess the impact of location mismatch on groupwise assessments of tract amplitude. We then developed a method for tract alignment that enhances the existing standard whole brain registration, and then tested whether this method improved the reliability of groupwise contrasts. Specifically, we conducted seed-based probabilistic diffusion tractography from primary motor, supplementary motor, and visual cortices, projecting through the corpus callosum. Streamline counts decreased rapidly with movement from the tract center (−35{\%} per millimeter); tract misalignment of a few millimeters caused substantial compromise of amplitude comparisons. Alignment of tracts “peak-to-peak” is essential for accurate amplitude comparisons. However, for all transcallosal tracts registered through the whole-brain method, the mean separation distance between an individual subject's tract and the average tract (3.2 mm) precluded accurate comparison: at this separation, tract amplitudes were reduced by 74{\%} from peak value. In contrast, alignment of subcortical tracts (thalamo-putaminal, pallido-rubral) was substantially better than alignment for cortical tracts; whole-brain registration was sufficient for these subcortical tracts. We demonstrated that location mismatches in cortical tractography were sufficient to produce false positive and false negative amplitude estimates in both groupwise and longitudinal comparisons. We then showed that our new tract alignment method substantially reduced location mismatch and improved both reliability and statistical power of subsequent quantitative comparisons.",
keywords = "Center of gravity, Dice similarity coefficient, Longitudinal, Quantitative, Registration, Tractography",
author = "Waugh, {Jeff L} and Kuster, {J. K.} and Makhlouf, {M. L.} and Levenstein, {J. M.} and Multhaupt-Buell, {T. J.} and Warfield, {S. K.} and N. Sharma and Blood, {A. J.}",
year = "2019",
month = "4",
day = "1",
doi = "10.1016/j.neuroimage.2018.12.057",
language = "English (US)",
volume = "189",
pages = "288--306",
journal = "NeuroImage",
issn = "1053-8119",
publisher = "Academic Press Inc.",

}

TY - JOUR

T1 - A registration method for improving quantitative assessment in probabilistic diffusion tractography

AU - Waugh, Jeff L

AU - Kuster, J. K.

AU - Makhlouf, M. L.

AU - Levenstein, J. M.

AU - Multhaupt-Buell, T. J.

AU - Warfield, S. K.

AU - Sharma, N.

AU - Blood, A. J.

PY - 2019/4/1

Y1 - 2019/4/1

N2 - Diffusion MRI-based probabilistic tractography is a powerful tool for non-invasively investigating normal brain architecture and alterations in structural connectivity associated with disease states. Both voxelwise and region-of-interest methods of analysis are capable of integrating population differences in tract amplitude (streamline count or density), given proper alignment of the tracts of interest. However, quantification of tract differences (between groups, or longitudinally within individuals) has been hampered by two related features of white matter. First, it is unknown to what extent healthy individuals differ in the precise location of white matter tracts, and to what extent experimental factors influence perceived tract location. Second, white matter lacks the gross neuroanatomical features (e.g., gyri, histological subtyping) that make parcellation of grey matter plausible – determining where tracts “should” lie within larger white matter structures is difficult. Accurately quantifying tractographic connectivity between individuals is thus inherently linked to the difficulty of identifying and aligning precise tract location. Tractography is often utilized to study neurological diseases in which the precise structural and connectivity abnormalities are unknown, underscoring the importance of accounting for individual differences in tract location when evaluating the strength of structural connectivity. We set out to quantify spatial variance in tracts aligned through a standard, whole-brain registration method, and to assess the impact of location mismatch on groupwise assessments of tract amplitude. We then developed a method for tract alignment that enhances the existing standard whole brain registration, and then tested whether this method improved the reliability of groupwise contrasts. Specifically, we conducted seed-based probabilistic diffusion tractography from primary motor, supplementary motor, and visual cortices, projecting through the corpus callosum. Streamline counts decreased rapidly with movement from the tract center (−35% per millimeter); tract misalignment of a few millimeters caused substantial compromise of amplitude comparisons. Alignment of tracts “peak-to-peak” is essential for accurate amplitude comparisons. However, for all transcallosal tracts registered through the whole-brain method, the mean separation distance between an individual subject's tract and the average tract (3.2 mm) precluded accurate comparison: at this separation, tract amplitudes were reduced by 74% from peak value. In contrast, alignment of subcortical tracts (thalamo-putaminal, pallido-rubral) was substantially better than alignment for cortical tracts; whole-brain registration was sufficient for these subcortical tracts. We demonstrated that location mismatches in cortical tractography were sufficient to produce false positive and false negative amplitude estimates in both groupwise and longitudinal comparisons. We then showed that our new tract alignment method substantially reduced location mismatch and improved both reliability and statistical power of subsequent quantitative comparisons.

AB - Diffusion MRI-based probabilistic tractography is a powerful tool for non-invasively investigating normal brain architecture and alterations in structural connectivity associated with disease states. Both voxelwise and region-of-interest methods of analysis are capable of integrating population differences in tract amplitude (streamline count or density), given proper alignment of the tracts of interest. However, quantification of tract differences (between groups, or longitudinally within individuals) has been hampered by two related features of white matter. First, it is unknown to what extent healthy individuals differ in the precise location of white matter tracts, and to what extent experimental factors influence perceived tract location. Second, white matter lacks the gross neuroanatomical features (e.g., gyri, histological subtyping) that make parcellation of grey matter plausible – determining where tracts “should” lie within larger white matter structures is difficult. Accurately quantifying tractographic connectivity between individuals is thus inherently linked to the difficulty of identifying and aligning precise tract location. Tractography is often utilized to study neurological diseases in which the precise structural and connectivity abnormalities are unknown, underscoring the importance of accounting for individual differences in tract location when evaluating the strength of structural connectivity. We set out to quantify spatial variance in tracts aligned through a standard, whole-brain registration method, and to assess the impact of location mismatch on groupwise assessments of tract amplitude. We then developed a method for tract alignment that enhances the existing standard whole brain registration, and then tested whether this method improved the reliability of groupwise contrasts. Specifically, we conducted seed-based probabilistic diffusion tractography from primary motor, supplementary motor, and visual cortices, projecting through the corpus callosum. Streamline counts decreased rapidly with movement from the tract center (−35% per millimeter); tract misalignment of a few millimeters caused substantial compromise of amplitude comparisons. Alignment of tracts “peak-to-peak” is essential for accurate amplitude comparisons. However, for all transcallosal tracts registered through the whole-brain method, the mean separation distance between an individual subject's tract and the average tract (3.2 mm) precluded accurate comparison: at this separation, tract amplitudes were reduced by 74% from peak value. In contrast, alignment of subcortical tracts (thalamo-putaminal, pallido-rubral) was substantially better than alignment for cortical tracts; whole-brain registration was sufficient for these subcortical tracts. We demonstrated that location mismatches in cortical tractography were sufficient to produce false positive and false negative amplitude estimates in both groupwise and longitudinal comparisons. We then showed that our new tract alignment method substantially reduced location mismatch and improved both reliability and statistical power of subsequent quantitative comparisons.

KW - Center of gravity

KW - Dice similarity coefficient

KW - Longitudinal

KW - Quantitative

KW - Registration

KW - Tractography

UR - http://www.scopus.com/inward/record.url?scp=85060311703&partnerID=8YFLogxK

UR - http://www.scopus.com/inward/citedby.url?scp=85060311703&partnerID=8YFLogxK

U2 - 10.1016/j.neuroimage.2018.12.057

DO - 10.1016/j.neuroimage.2018.12.057

M3 - Article

VL - 189

SP - 288

EP - 306

JO - NeuroImage

JF - NeuroImage

SN - 1053-8119

ER -