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High angular resolution diffusion imaging reveals intravoxel white matter fiber heterogeneity
Abstract
Magnetic resonance (MR) diffusion tensor imaging (DTI) can resolve the white matter fiber orientation within a voxel provided that the fibers are strongly aligned. However, a given voxel may contain a distribution of fiber orientations due to, for example, intravoxel fiber crossing. The present study sought to test whether a geodesic, high b-value diffusion gradient sampling scheme could resolve multiple fiber orientations within a single voxel. In regions of fiber crossing the diffusion signal exhibited multiple local maxima/minima as a function of diffusion gradient orientation, indicating the presence of multiple intravoxel fiber orientations. The multimodality of the observed diffusion signal precluded the standard tensor reconstruction, so instead the diffusion signal was modeled as arising from a discrete mixture of Gaussian diffusion processes in slow exchange, and the underlying mixture of tensors was solved for using a gradient descent scheme. The multitensor reconstruction resolved multiple intravoxel fiber populations corresponding to known fiber anatomy. Ma
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“The DTI model cannot differentiate these components or even crossing fibers (Tuch et al., 2002; Jbabdi et al., 2010), which are estimated to occur in up to 90% of WM voxels at the typical dMRI resolution (Descoteaux et al., 2009; Jeurissen et al., 2013).”
From Diffusion MRI Indices and Their Relation to Cognitive Impairment in Brain Aging: The Updated Multi-protocol Approach in ADNI3 (2019) · cites this paper as Tuch et al., 2002
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“opment of new models based on high angular resolution diffusion imaging (HARDI) seeks to provide solutions to this problem (Tuch et al., 2002; Tuch, 2004; Jansons and Alexander, 2003; Wedeen et al., 2008).”
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“In contrast, Q-ball imaging (QBI) [21], high angular resolution diffusion imaging (HARDI) [22], and diffusion spectrum imaging (DSI) [23, 24] can resolve fibers crossing but demand larger pulsed field gradients.”
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“These tools generally implemented the 19 multi-tensor model (Alexander et al., 2001; Tuch et al., 2002) to simulate fiber crossing, fanning, kissing, 20”
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Association of iron levels in hair with brain structures and functions in young adults
Takeuchi, H., Taki, Y., Nouchi, R., Yokoyama, R., Kotozaki, Y., Nakagawa, S., Sekiguchi, A., Iizuka, K., Yamamoto, Y., Hanawa, S., et al. (2019) · Journal of Trace Elements in Medicine and Biology · doi:10.1016/j.jtemb.2019.126436 · Cited by 8
“However, in areas where fibers cross, the associations between myelination and FA become unclear [72], and the corpus callosum (which does not have crossed fibers) may be sensitive to the findings.”
BackgroundDiffusion Kurtosis Imaging Fiber Tractography of Major White Matter Tracts in Neurosurgery
Bopp, M. H. A., Emde, J., Carl, B., Nimsky, C., & Saß, B. (2021) · Brain Sciences · doi:10.3390/brainsci11030381 · Cited by 8
“Further complex and sophisticated methods of modeling diffusion properties exist, based on single- or multi-shell high-angular resolution diffusion imaging (HARDI) acquisition techniques [17,18], applying different models such as Q-ball imaging [19], diffusion spectrum imaging (DSI) [20], or compressed sensing techniq…”
BackgroundMethodLiu, X., Kinoshita, M., Shinohara, H., Hori, O., Ozaki, N., & Nakada, M. (2021) · Brain Topography · doi:10.1007/s10548-021-00879-5 · Cited by 8
“DTI can accurately define the fiber orientation of a voxel containing fibers with coherent directions, but cannot define directions of heterogeneous fibers presented with crossing or kissing patterns (Frank 2001, 2002; Tuch et al. 2002; Wiegell et al. 2000).”
BackgroundTensor kernels for simultaneous fiber model estimation and tractography
Yogesh Rathi, A., Malcolm, J. G., Michailovich, O., Westin, C., Shenton, M. E., & Sylvain Bouix, A. (2010) · Magnetic Resonance in Medicine · doi:10.1002/mrm.22292 · Cited by 8
“(34) showed that at a b-value of 1000 the maximum number of detectable fibers is two, several other studies restricted their analysis to two-fiber models due to problems with estimating more than two components (6,7,23).”
BackgroundReconstruction of Scattered Data in Fetal Diffusion MRI
Oubel, E., Koob, M., Studholme, C., Dietemann, J., & Rousseau, F. (2010) · Lecture notes in computer science · doi:10.1007/978-3-642-15705-9_70 · Cited by 8
“As the proposed method does not assume any diffusion model, the generated data can be used to study diffusion patterns even in IVOH.”
MethodFast diffusion imaging with high angular resolution
Chao, T. C., Chiou, J. G., Maier, S. E., & Madore, B. (2016) · Magnetic Resonance in Medicine · doi:10.1002/mrm.26163 · Cited by 8
“q̂y ;kd 1⁄4 min q̂ jsky ;d EyHF H d r̂y ;kd j 2 2 þ ljM (1)q̂y ;kd j 2 2 ; [2]”
Fiber Orientation Distribution Estimation Using a Peaceman--Rachford Splitting Method
Chen, Y., Dai, Y., & Han, D. (2016) · SIAM Journal on Imaging Sciences · doi:10.1137/15m1026626 · Cited by 8
“[57] raised a cheap DW-MRI sampling method named the high angular resolution diffusion imaging (HARDI), which collects DW-MRI signals in gradient orientations located on a semisphere with a fixed b-value.”
BackgroundMethodEarly blindness is associated with increased volume of the uncinate fasciculus
Bauer, C. M., Cattaneo, Z., & Merabet, L. B. (2018) · European Journal of Neuroscience · doi:10.1111/ejn.13848 · Cited by 8
“imaging (DTI) techniques provide information regarding the degree of water diffusivity in the brain in order to derive local axonal fiber orientation, HARDI utilizes a stronger diffusion gradient than DTI and is able to resolve multiple fiber orientations within each voxel (Tuch et al., 2002).”
BackgroundMethodInfluentialAccelerated High Spatial Resolution Diffusion-Weighted Imaging
Scherrer, B., Afacan, O., Taquet, M., Prabhu, S. P., Gholipour, A., & Warfield, S. K. (2015) · Lecture notes in computer science · doi:10.1007/978-3-319-19992-4_6 · Cited by 8
“This was achieved by assessing in two single fascicle regions 1) the average relative error of cFA; and 2) the average minimum angle (AMA) error [13].”
MethodWhite Matter Tractography and Diffusion‐Weighted Imaging
Vettel, J. M., Cooper, N., Garcia, J. O., Yeh, F.-C. F., & Verstynen, T. (2017) · Wiley eBooks · doi:10.1002/9780470015902.a0027162 · Cited by 9
Local structural connectivity directs seizure spread in focal epilepsyPreprint
Shah, P., Ashourvan, A., Mikhail, F., Pines, A., Kini, L. G., Shinohara, R., Bassett, D., Litt, B., & Davis, K. (2018) · bioRxiv · doi:10.1101/406793 · Cited by 14
“These approaches reveal a wide variety of network disruptions in epilepsy patients, both structurally [Raj et al., 2010; Taylor et al., 2015; Vaessen et al., 2012] and functionally [de Campos et al., 2016; Pedersen et al., 2015; Pittau et al., 2012].”
BackgroundTractEM: Fast Protocols for Whole Brain Deterministic Tractography-Based White Matter AtlasPreprint
Bayrak, R. G., Wang, X., Schilling, K. G., Greer, J. M., Hansen, C. B., Blaber, J. A., Williams, O. A., Beason‐Held, L. L., Resnick, S. M., Rogers, B. P., et al. (2019) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/651935 · Cited by 8
“HARDI models are capable of characterizing multiple directions and resolving crossing fiber issues (Tuch, 1999; Tuch et al., 2002; Descoteaux et al., 2007).”
BackgroundMulti-tensor fixel-based metrics in tractometry: application to multiple sclerosis
Hernández-Gutiérrez, E., Coronado‐Leija, R., Edde, M., Dumont, M., Houde, J., Baraković, M., Magon, S., Ramírez-Manzanares, A., & Descoteaux, M. (2024) · Frontiers in Neuroscience · doi:10.3389/fnins.2024.1467786 · Cited by 6
Toward an accurate multi-fiber assessment strategy for clinical practice
Scherrer, B., & Warfield, S. K. (2011) · IEEE International Symposium on Biomedical Imaging (ISBI) · doi:10.1109/isbi.2011.5872836 · Cited by 7
“Three major sampling schemes have been proposed for complex structure assessment: cartesian sampling, single-shell and multiple-shell spherical sampling (high angular resolution diffusion imaging, HARDI).”
BackgroundKaran, P., Edde, M., Gilbert, G., Baraković, M., Magon, S., & Descoteaux, M. (2024) · Magnetic Resonance in Medicine · doi:10.1002/mrm.30195 · Cited by 7
“Although this is not robust in voxels of crossing fibers, 21 which represent a large fraction of the voxels in the brain, 22,23 it still prevails in single-fiber voxels.”
Middlebrooks, E. H., Yağmurlu, K., Bennett, J., & Bidari, S. (2014) · Surgical and Radiologic Anatomy · doi:10.1007/s00276-014-1387-2 · Cited by 7
“Some examples include high angular resolution diffusion imaging (HARDI) [17], spherical harmonic decomposition [1], q-space imaging [10], diffusion spectrum imaging (DSI) [21], and generalized q-sampling imaging method (GQI) [27].”
BackgroundDiffusion tensor imaging: techniques and clinical applications
Zhou, X. J. (2005) · Annual International Conference of the IEEE Engineering in Medicine and Biology Society (EMBC) · doi:10.1109/iembs.2004.1404460 · Cited by 7
“Two examples are diffusion spectroscopic imaging (DSI) [10] and high angular resolution diffusion (HARD) imaging [11].”
BackgroundMessaritaki, E., Rudrapatna, S. U., Parker, G. D., Gray, W., & Jones, D. K. (2018) · Frontiers in Neurology · doi:10.3389/fneur.2018.01092 · Cited by 7
JEDI:JointEstimationDiffusionImaging of macroscopic and microscopic tissue properties
Frank, L. R., Zahneisen, B., & Galinsky, V. L. (2020) · Magnetic Resonance in Medicine · doi:10.1002/mrm.28141 · Cited by 7
Puri, A., Shakya, S., & Kumar, S. (2021) · Journal of Magnetic Resonance · doi:10.1016/j.jmr.2021.106931 · Cited by 7
Quantitative MR Markers in Non-Myelopathic Spinal Cord Compression: A Narrative Review
Valošek, J., Bednařík, P., Keřkovský, M., Hluštı́k, P., Bednařík, J., & Svátková, A. (2022) · Journal of Clinical Medicine · doi:10.3390/jcm11092301 · Cited by 6
“Usually, high angular resolution diffusion imaging [113] sequences are employed, utilizing diffusion gradient sampling on several whole q-space spheres (i.”
BackgroundKaran, P., Reymbaut, A., Gilbert, G., & Descoteaux, M. (2021) · Medical Image Analysis · doi:10.1016/j.media.2022.102476 · Cited by 7
Verrall, C., Chen, J., Yeh, C.-H., Mackay, M., d'Udekem, Y., Winlaw, D., Iyengar, A., Ayer, J., Gentles, T., Cordina, R., et al. (2022) · NeuroImage: Clinical · doi:10.1016/j.nicl.2022.103151 · Cited by 5
Analysis of Tongue Muscle Strain During Speech From Multimodal Magnetic Resonance Imaging
Shao, M., Xing, F., Carass, A., Liang, X., Zhuo, J., Stone, M. L., Woo, J., & Prince, J. L. (2023) · Journal of Speech Language and Hearing Research · doi:10.1044/2022_jslhr-22-00329 · Cited by 7
Metwalli, N. S., LaConte, S. M., & Hu, X. P. (2006) · Annual International Conference of the IEEE Engineering in Medicine and Biology Society (EMBC) · doi:10.1109/iembs.2006.259870 · Cited by 7
“This assumption of a Gaussian diffusion profile is not always met, especially in cases of voxels having multiple fiber orientations [3].”
BackgroundDiffusion tensor imaging in studying white matter complexity: A gap junction hypothesis
Abdallah, C. G., Tang, C. Y., Mathew, S. J., Martínez, J. A. B., Hof, P. R., Perera, T. D., Shungu, D. C., Gorman, J. M., & Coplan, J. D. (2010) · Neuroscience Letters · doi:10.1016/j.neulet.2010.03.070 · Cited by 7
“At present, conventional DTI is incapable of resolving multiple fiber orientations within an individual voxel [25], therefore, we surmise that a higher level of intersections of fiber tracts in the anterior regions of the brain likely accounts for the decrease in the level of anisotropy in these regions.”
BackgroundRatnarajah, N., Simmons, A., Bertoni, M., & Hojjatoleslami, A. (2012) · Magnetic Resonance Imaging · doi:10.1016/j.mri.2012.07.004 · Cited by 7
“HARDI-based methods, including multitensor models [3], spherical deconvolution [4] and Q-ball imaging (QBI) [5], require longer acquisition times than conventional DTI and are generally not suitable for clinical applications.”
BackgroundMethodCorreia, M., Newcombe, V., & Williams, G. B. (2011) · NeuroImage · doi:10.1016/j.neuroimage.2011.03.004 · Cited by 7
“In addition, it has been previously shown that IVOH can be detected already at b-values as low as 1000 s/mm2 (Tuch et al., 2002).”
BackgroundFiber Visualization with LIC Maps Using Multidirectional Anisotropic Glyph Samples
Höller, M., Otto, K.-M., Klose, U., Groeschel, S., & Ehricke, H.-H. (2014) · International Journal of Biomedical Imaging · doi:10.1155/2014/401819 · Cited by 7
“Directional color-coding of ODF glyphs helps to reveal local anisotropy directions [15, 16].”
BackgroundLee, D., Lee, D., & Han, B. (2016) · Medicine · doi:10.1097/md.0000000000003317 · Cited by 7
Metadata
- Authors
- Tuch, D. S., Reese, T. G., Wiegell, M. R., Makris, N., Belliveau, J. W., & Wedeen, V. J.
- Affiliations
- Massachusetts General Hospital (US)
- Corresponding author
- Wedeen, Van J.
- Venue
- Magnetic Resonance in Medicine
- Publisher
- Wiley
- Published
- 2002-09-26
- Volume
- 48
- Issue
- 4
- Pages
- 577-582
- ISSN
- 0740-3194 (ISSN-L)
- 1522-2594
- OpenAlex
- W2080198834
- Cited by
- 1,548
- References
- 27
- Citations by year
- 2026: 20 · 2025: 43 · 2024: 39 · 2023: 52 · 2022: 59 · 2021: 65 · 2020: 65 · 2019: 82 · 2018: 76 · 2017: 84 · 2016: 84 · 2015: 115 · 2014: 93 · 2013: 95 · 2012: 79
- FWCI
- 23.23
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Magnetic Resonance in Medicine (publishedVersion)
- PubMed (publishedVersion)
- Funders
- Sol Goldman Charitable Trust
- Topics
- Health Sciences › Medicine › Radiology, Nuclear Medicine and Imaging › Advanced Neuroimaging Techniques and Applications
- Health Sciences › Medicine › Radiology, Nuclear Medicine and Imaging › Advanced MRI Techniques and Applications
- Life Sciences › Neuroscience › Cognitive Neuroscience › Functional Brain Connectivity Studies
- Keywords
- high angular resolution diffusion imaging
- MeSH terms
- Brain, Computer Simulation, Humans, Image Processing, Computer-Assisted, Male, Nerve Fibers, Anisotropy, Diffusion Magnetic Resonance Imaging
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