Cited by 1,548Advanced Neuroimaging Techniques and ApplicationsAdvanced MRI Techniques and ApplicationsFunctional Brain Connectivity Studies

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High angular resolution diffusion imaging reveals intravoxel white matter fiber heterogeneity

Tuch, David S., Reese, Timothy G., Wiegell, Mette R., Makris, Nikos, Belliveau, John W., Wedeen, Van J.·2002·Magnetic Resonance in Medicine

DOI 10.1002/mrm.10268

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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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BackgroundMethod
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Diffusion Tensor Imaging and Related Techniques In Tuberous Sclerosis Complex: Review and Future Directions
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Background
FRATS: Functional Regression Analysis of DTI Tract Statistics
Hongtu Zhu, B., Styner, M. A., Tang, N., Liu, Z., Lin, W., & Gilmore, J. H. (2010) · IEEE Transactions on Medical Imaging · doi:10.1109/tmi.2010.2040625 · Cited by 41
“apply FRATS to water diffusion related parameters obtained from HARDI [42]–[44].”
Method
Diffusion tensor imaging of anterior commissural fibers in patients with schizophrenia
Choi, H., Kubicki, M. R., Whitford, T. J., Alvarado, J. L., Terry, D. P., Niznikiewicz, M. A., McCarley, R. W., Kwon, J. S., & Shenton, M. E. (2011) · Schizophrenia Research · doi:10.1016/j.schres.2011.04.016 · Cited by 41
“We note, however, that a diffusion tensor model is not always adequate, especially in voxels containing complex crossing tracts from differently oriented fibers (Alexander et al., 2002; Tuch et al., 2002).”
Background
Functional Neuroimaging: Fundamental Principles and Clinical Applications
Khanna, N., Altmeyer, W. B., Zhuo, J., & Steven, A. J. (2015) · The Neuroradiology Journal · doi:10.1177/1971400915576311 · Cited by 43
High-resolution distortion-free diffusion imaging using hybrid spin-warp and echo-planar PSF-encoding approach
In, M., Posnansky, O. P., & Speck, O. (2017) · NeuroImage · doi:10.1016/j.neuroimage.2017.01.008 · Cited by 41
“However, this limits the opportunity for acquisition of images with a high number of diffusion directions, which is often preferred as a way to characterize the underlying fiber connections in the presence of multiple intravoxel fiber orientations (Tuch et al., 2002).”
Background
Probabilistic White Matter Atlases of Human Auditory, Basal Ganglia, Language, Precuneus, Sensorimotor, Visual and Visuospatial Networks
Figley, T. D., Moghadam, B. M., Bhullar, N., Kornelsen, J., Courtney, S. M., & Figley, C. R. (2017) · Frontiers in Human Neuroscience · doi:10.3389/fnhum.2017.00306 · Cited by 40
“Although the aforementioned limitations apply to all current diffusion MRI approaches—including high angular resolution diffusion imaging (HARDI; Tuch et al., 2002), Q-ball imaging (Tuch, 2004), and diffusion spectrum imaging (DSI; Wedeen et al., 2005)—we also note some additional limitations of…”
Background
Probabilistic Tractography to Predict the Position of Cranial Nerves Displaced by Skull Base Tumors: Value for Surgical Strategy Through a Case Series of 62 Patients
Jacquesson, T., Cotton, F., Attyé, A., Zaouche, S., Tringali, S., Bosc, J., Robinson, P., Jouanneau, E., & Frindel, C. (2018) · Neurosurgery · doi:10.1093/neuros/nyy538 · Cited by 41
Sarcopenia and Neuroscience: Learning to Communicate
Clark, B. C., & Carson, R. G. (2021) · The Journals of Gerontology Series A · doi:10.1093/gerona/glab098 · Cited by 42
Why multiple b-values are required for multi-tensor models. evaluation with a constrained log-euclidean model
Scherrer, B., & Warfield, S. K. (2010) · IEEE International Symposium on Biomedical Imaging (ISBI) · doi:10.1109/isbi.2010.5490257 · Cited by 41
“In the literature, a number of approaches fit a multi-tensor model with only one b-value [3, 6, 4].”
BackgroundMethodInfluential
Feasibility of prefronto-caudate pathway tractography using high resolution diffusion tensor tractography data at 3 T
Kamali, A., Kramer, L. A., & Hasan, K. M. (2010) · Journal of Neuroscience Methods · doi:10.1016/j.jneumeth.2010.06.026 · Cited by 42
Corticospinal Tracts by Diffusion Tensor Tractography in Patients With Arteriovenous Malformations
Itoh, D., Aoki, S., Maruyama, K., Masutani, Y., Mori, H., Masumoto, T., Abe, O., Hayashi, N., Okubo, T., & Ohtomo, K. (2006) · Journal of Computer Assisted Tomography · doi:10.1097/00004728-200607000-00011 · Cited by 41
“Crossing fiber is a problem which is discussed elsewhere.(19) We are not sure if DTT-CSTs can be tracked in cases with diffuse AVM.”
Background
Diffusion MRI of the infant brain reveals unique asymmetry patterns during the first-half-year of development
Liu, T.-T., Gao, F.-S., Zheng, W., You, Y., Zhao, Z.-Y., Lv, Y., Chen, W., Zhang, H.-X., Ji, C., & Wu, D. (2021) · NeuroImage · doi:10.1016/j.neuroimage.2021.118465 · Cited by 37
RubiX: Combining Spatial Resolutions for Bayesian Inference of Crossing Fibers in Diffusion MRI
Sotiropoulos, S. N., Jbabdi, S., Andersson, J., Woolrich, M. W., Uǧurbil, K., & Behrens, T. E. J. (2013) · IEEE Transactions on Medical Imaging · doi:10.1109/tmi.2012.2231873 · Cited by 40
“Parametric [11]–[14] or nonparametric approaches [6], [15]–[19] exist that either estimate directly the dominant fiber orientations within each voxel or reconstruct orientation distribution functions (ODFs) on the sphere.”
Background
Deconvolution in diffusion spectrum imaging
Canales-Rodríguez, E. J., Iturria‐Medina, Y., Alemán‐Gómez, Y., & Melie‐García, L. (2009) · NeuroImage · doi:10.1016/j.neuroimage.2009.11.066 · Cited by 40
“…developed (Alexander, 2005; Anderson, 2005; Behrens et al., 2007; Canales-Rodríguez et al., 2009; Descoteaux et al., 2007; Liu et al., 2004; Melie-García et al., 2008; Özarslan et al., 2006; Ramírez-Manzanares et al., 2007; Tournier et al., 2004; Tuch et al., 2002; Tuch, 2004; Wedeen et al., 2005).”
MethodInfluential
Structural connectivity of visuotopic intraparietal sulcus
Bray, S., Arnold, A. E. G. F., Iaria, G., & MacQUEEN, G. M. (2013) · NeuroImage · doi:10.1016/j.neuroimage.2013.05.080 · Cited by 42
“A higher resolution diffusion protocol (Tuch et al., 2002) could enable a more detailed investigation into the homogeneity of connections within IPS regions.”
Diffusion-Tensor Neuronal Fiber Tractography and Manganese-enhanced MR Imaging of Primate Visual Pathway in the Common Marmoset: Preliminary Results
Yamada, M., Momoshima, S., Masutani, Y., Fujiyoshi, K., Abe, O., Nakamura, M., Aoki, S., Tamaoki, N., & Okano, H. (2008) · Radiology · doi:10.1148/radiol.2493072141 · Cited by 40
A New Method to Derive White Matter Conductivity From Diffusion Tensor MRI
Wang, K., Zhu, S., Mueller, B. A., Lim, K. O., Liu, Z., & He, B. (2008) · IEEE Transactions on Biomedical Engineering · doi:10.1109/tbme.2008.923159 · Cited by 40
“the fact that the intravoxel orientational heterogeneity is considerable under the typical voxel size of DT-MRI [15]–[17], [23].”
Background
Diffusion MRI Signal Augmentation: From Single Shell to Multi Shell with Deep Learning
Koppers, S., Haarburger, C., & Merhof, D. (2017) · Mathematics and visualization · doi:10.1007/978-3-319-54130-3_5 · Cited by 41
Diffusion tensor and volumetric magnetic resonance imaging findings in the brains of professional musicians
Acer, N., Bastepe-Gray, S. E., Sağıroğlu, A., Gümüş, K., Değirmencioğlu, L., Zararsız, G., & Özıç, M. Ü. (2017) · Journal of Chemical Neuroanatomy · doi:10.1016/j.jchemneu.2017.11.003 · Cited by 41
Optimization of graph construction can significantly increase the power of structural brain network studies
Messaritaki, E., Dimitriadis, S. I., & Jones, D. K. (2019) · NeuroImage · doi:10.1016/j.neuroimage.2019.05.052 · Cited by 39
“On the other hand, b -values of under 1500 s/mm 2 can be problematic when it comes to resolving crossing ﬁ bers with CSD tractography algorithms (Tuch et al., 2002; Tournier et al., 2004, 2008; Cho et al., 2008), which is important given the prevalence of such ﬁ bers in the human brain (Jeurissen…”
The role of diffusion tractography in refining glial tumor resection
Vanderweyen, D., Theaud, G., Sidhu, J., Rheault, F., Sarubbo, S., Descoteaux, M., & Fortin, D. (2020) · Brain Structure and Function · doi:10.1007/s00429-020-02056-z · Cited by 41
Neural Tractography Using an Unscented Kalman Filter
Malcolm, J. G., Shenton, M. E., & Yogesh Rathi, A. (2009) · Lecture notes in computer science · doi:10.1007/978-3-642-02498-6_11 · Cited by 40
“Several other studies have also found two tensors to be sufficient [6, 7, 38, 8].”
BackgroundMethodInfluential
From research to clinical practice: Implementation of functional magnetic imaging and white matter tractography in the clinical environment
Bick, A. S., Mayer, A., & Levin, N. (2011) · Journal of the Neurological Sciences · doi:10.1016/j.jns.2011.07.040 · Cited by 39
“High angular resolution diffusion imaging (HARDI) has been proposed for this purpose [62].”
Background
A regularized two‐tensor model fit to low angular resolution diffusion images using basis directions
Sotiropoulos, S. N., Bai, L., Morgan, P. S., Auer, D. P., Constantinescu, C. S., & Tench, C. R. (2008) · Journal of Magnetic Resonance Imaging · doi:10.1002/jmri.21380 · Cited by 39
Real-time measurement and correction of both B0 changes and subject motion in diffusion tensor imaging using a double volumetric navigated (DvNav) sequence
Alhamud, A., Taylor, P. A., van der Kouwe, A. J. W., & Meintjes, E. M. (2015) · NeuroImage · doi:10.1016/j.neuroimage.2015.11.022 · Cited by 40
“, 2003) or a longer diffusion table, such as in q-space imaging (Assaf and Cohen, 1999), HARDI (Tuch et al., 2002), and diffusion spectrum imaging (Wedeen et al.”
Influential
Diffuse Axonal Injury
Su, E. R., & Bell, M. J. (2015) · Frontiers in neuroscience · doi:10.1201/b18959-4 · Cited by 40
Cross‐sectional and longitudinal multimodal structural imaging in prodromal Huntington's disease
Harrington, D. L., Long, J. D., Durgerian, S., Mourany, L., Koenig, K. A., Bonner‐Jackson, A., Paulsen, J. S., for the PREDICT‐HD Investigators of the Huntington Study Group, & Rao, S. M. (2016) · Movement Disorders · doi:10.1002/mds.26803 · Cited by 39
“04/2530 ms/10 8; matrix 5 256 3 240; receiver bandwidth 5 220 kHz) and high angular resolution diffusion images (twicerefocused spin echo diffusion weighting, single-shot two-dimesional echo planar imaging readout, 2 mm isotropic resolution, 256 mm 3 256 mm field of view, 128 3 128 matrix, 50 2-mm thick slices, echo t…”
Background
White matter basis for the hub-and-spoke semantic representation: evidence from semantic dementia
Chen, Y., Huang, L., Chen, K., Ding, J., Zhang, Y., Yang, Q., Lv, Y., Han, Z., & Guo, Q. (2020) · Brain · doi:10.1093/brain/awaa057 · Cited by 40
“More gradient directions ( 4 60), in addition to more complex acquisition profiles (e.g. HARDI; Tuch et al. , 2002), are required in future studies.”
Background
Preliminary Experience with Visualization of Intracortical Fibers by Focused High-Resolution Diffusion Tensor Imaging
Jaermann, T., Zanche, N. D., Stämpfli, P., Pruessmann, K. P., Valavanis, A., Boesiger, P., & Kollias, S. (2007) · American Journal of Neuroradiology · doi:10.3174/ajnr.a0742 · Cited by 38
“Resolving intravoxel heterogeneity can be achieved either by increasing the spatial resolution, or by developing alternative strategies (eg, modeling of the diffusion process in the neural tissue) that are able to resolve multiple intravoxel fiber directions.(7,8) A few studies so far have described distinct anisotrop…”
Method
A filtered approach to neural tractography using the Watson directional function
Malcolm, J. G., Michailovich, O., Sylvain Bouix, A., Westin, C., Shenton, M. E., & Yogesh Rathi, A. (2009) · Medical Image Analysis · doi:10.1016/j.media.2009.10.003 · Cited by 38
“# For voxels containing a mixed diffusion pattern, a general weighted formulation may be written as, where s 0 is a baseline signal intensity, b is an acquisition-speciﬁc constant, w j are convex weights, and D j is a tensor describing a diffusion pattern (Tuch et al., 2002, 2005).”
BackgroundMethodInfluential
Axon Diameter Mapping in Crossing Fibers with Diffusion MRI
Zhang, H. G., Dyrby, T. B., & Alexander, D. C. (2011) · Lecture notes in computer science · doi:10.1007/978-3-642-23629-7_11 · Cited by 38
“Since the earliest breakthroughs in crossing fiber resolution [10,11], major progress has produced very effective modern techniques (See [12] for a review).”
Background
Cortical fibers orientation mapping using in-vivo whole brain 7 T diffusion MRI
Gülban, Ö. F., Martino, F. D., Vu, A. T., Yacoub, E. S., Uǧurbil, K., & Lenglet, C. (2018) · NeuroImage · doi:10.1016/j.neuroimage.2018.05.010 · Cited by 39
“, 1994), high angular resolution diffusion imaging (Tuch et al., 2002), diffusion spectrum imaging (Wedeen et al.”
Subtle white matter alterations in schizophrenia identified with a new measure of fiber density
Stämpfli, P., Sommer, S., Manoliu, A., Burrer, A., Schmidt, A., Herdener, M., Seifritz, E., Kaiser, S., & Kirschner, M. (2019) · Scientific Reports · doi:10.1038/s41598-019-40070-2 · Cited by 40
Detecting microstructural white matter abnormalities of frontal pathways in children with ADHD using advanced diffusion models
Wu, W., McAnulty, G. B., Hamoda, H. M., Sarill, K., Karmacharya, S., Gagoski, B. A., Ning, L., Grant, P. E., Shenton, M. E., Waber, D. P., et al. (2019) · Brain Imaging and Behavior · doi:10.1007/s11682-019-00108-5 · Cited by 40
Self-citation
Adaptive Kernels for Multi-fiber Reconstruction
Barmpoutis, A., Jian, B., & Vemuri, B. C. (2009) · Lecture notes in computer science · doi:10.1007/978-3-642-02498-6_28 · Cited by 38
“The approach in [6] assumes the signal in each voxel can be split into a weighted sum of contributions from different diffusion tensors individually.”
Background
Learning a Reliable Estimate of the Number of Fiber Directions in Diffusion MRI
Schultz, T. (2012) · Lecture notes in computer science · doi:10.1007/978-3-642-33454-2_61 · Cited by 38
“When analyzing a diffusion MRI signal that arises as an average over n fiber compartments with principal directions vi and relative weights wi, two or more of the vi may be so close to collinearity that, given noisy measurements with limited angular and spectral resolution, it becomes impossible to separate them with…”
BackgroundMethod
DTI Parameter Optimisation for Acquisition at 1.5T: SNR Analysis and Clinical Application
Laganà, M. M., Rovaris, M., Ceccarelli, A., Venturelli, C., Marini, S., & Baselli, G. (2010) · Computational Intelligence and Neuroscience · doi:10.1155/2010/254032 · Cited by 38
“Several studies have been performed to reduce the errors on fiber tracking [30–33], but these methodologies are still being developed, none are used routinely, and most of them are time consuming and require strong computational power.”
Background
Informed constrained spherical deconvolution (iCSD)
Roine, T., Jeurissen, B., Perrone, D., Aelterman, J., Philips, W. R., Leemans, A., & Sijbers, J. (2015) · Medical Image Analysis · doi:10.1016/j.media.2015.01.001 · Cited by 37
“To overcome this, high angular resolution diffusion imaging (HARDI) (Tuch et al., 2002; Jansons and Alexander, 2003; Tournier et al., 2004; Tuch, 2004; Anderson, 2005; Alexander, 2005; Hosey et al., 2005; Tournier et al., 2007; Dell’Acqua et al., 2007; Descoteaux et al., 2007; Behrens et al., 2007;…”
Influential
Motor and extramotor neurodegeneration in amyotrophic lateral sclerosis: A 3T high angular resolution diffusion imaging (HARDI) study
Trojsi, F., Corbo, D., Caiazzo, G., Piccirillo, G., Monsurrò, M. R., Cirillo, S., Esposito, F., & Tedeschi, G. (2013) · Amyotrophic Lateral Sclerosis and Frontotemporal Degeneration · doi:10.3109/21678421.2013.785569 · Cited by 37
Diffusion Tensor MRI of the Heart – In Vivo Imaging of Myocardial Fiber Architecture
Froeling, M., Strijkers, G. J., Nederveen, A. J., Chamuleau, S. A. J., & Luijten, P. R. (2014) · Current Cardiovascular Imaging Reports · doi:10.1007/s12410-014-9276-y · Cited by 37
The Emerging Role of Tractography in Deep Brain Stimulation: Basic Principles and Current Applications
Rodrigues, N. B., Mithani, K., Meng, Y., Lipsman, N., & Hamani, C. (2018) · Brain Sciences · doi:10.3390/brainsci8020023 · Cited by 40
“resolution diffusion imaging (HARDI) [11], Q-Ball imaging (QBI) [12], hybrid diffusion imaging (HYDI) [13], diffusion spectrum imaging (DSI) [14], spherical deconvolutional models [15], composite”
BackgroundMethod
Whole mouse brain connectomics
Johnson, G. A., Wang, N., Anderson, R. J., Chen, M., Cofer, G. P., Gee, J. C., Pratson, F., Tustison, N. J., & WHITE, L. E. (2018) · The Journal of Comparative Neurology · doi:10.1002/cne.24560 · Cited by 36
“…have probed the question of what is “sufficient” which is in turn dependent on the algorithm, signal to noise of the data and spatial resolution (Jones, 2004; Jones & Cercignani, 2010; Jones, Knösche, & Turner, 2013; Tournier, Calamante, & Connelly, 2013; Tuch et al., 2002; Vos et al., 2016).”
Background
A Missing Connection: A Review of the Macrostructural Anatomy and Tractography of the Acoustic Radiation
Maffei, C., Sarubbo, S., & Jovicich, J. (2019) · Frontiers in Neuroanatomy · doi:10.3389/fnana.2019.00027 · Cited by 41
“Resolving the fiber crossing is a wellknown challenge in dMRI (Tuch et al., 2002; Dell’Acqua and Catani, 2012; Jeurissen et al., 2013).”
Background
Increased posterior default mode network activity and structural connectivity in young adult APOE-ε4 carriers: a multimodal imaging investigation
Hodgetts, C. J., Shine, J. P., Williams, H., Postans, M., Sims, R., Williams, J. H., Lawrence, A. D., & Graham, K. S. (2018) · Neurobiology of Aging · doi:10.1016/j.neurobiolaging.2018.08.026 · Cited by 40
Frontrunner in Translation: Progressive Supranuclear Palsy
Shoeibi, A., Olfati, N., & Litvan, I. (2019) · Frontiers in Neurology · doi:10.3389/fneur.2019.01125 · Cited by 39

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.
ORCID: Reese, Timothy G.
Makris, Nikos
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
DOI: 10.1002/mrm.10268
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
Licence: onlinelibrary.wiley.com/termsAndConditions#vor (vor)
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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High angular resolution diffusion imaging reveals intravoxel white matter fiber heterogeneity

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