Comparison of multiple tractography methods for reconstruction of the retinogeniculate visual pathway using diffusion MRI

The retinogeniculate visual pathway (RGVP) conveys visual information from the retina to the lateral geniculate nucleus. Anatomically, the RGVP can be separated into four subdivisions, including two decussating and two non-decussating fiber pathways, which cannot be identified by conventional magnetic resonance imaging (MRI). Diffusion MRI tractography has the potential to trace these subdivisions and is increasingly used to study the anatomy of the RGVP. However, it is not yet known which fiber tracking strategy is most suitable for tractographic reconstruction of the RGVP. In this study, four different tractography algorithms, including constrained spherical deconvolution (CSD) model based probabilistic (iFOD1) and deterministic (SD-Stream) methods, and multi-fiber (UKF-2T) and single-fiber (UKF-1T) unscented Kalman filter (UKF) tractography methods, are compared for reconstruction of the RGVP. Experiments are performed using diffusion MRI data of 57 subjects in the Human Connectome Project. The RGVP is identified using regions of interest created by two clinical experts. Anatomical measurements are used to assess the advantages and limitations of the four tracking strategies, including the reconstruction rate of the four RGVP subdivisions, the percentage of decussating fibers, the correlation between volumes of the traced RGVPs and a T1w-based RGVP segmentation, and an expert judgment to rank the anatomical appearance of the reconstructed RGVPs. Overall, we conclude that UKF-2T and iFOD1 produce the best RGVP reconstruction results. The iFOD1 method can better quantitatively estimate the percentage of decussating fibers, while the UKF-2T method produces reconstructed RGVPs that are judged to better correspond to the known anatomy.

[1]  E R Laws,et al.  Transsphenoidal decompression of the optic nerve and chiasm. Visual results in 62 patients. , 1977, Journal of neurosurgery.

[2]  Uri Tabori,et al.  Visual outcomes in children with neurofibromatosis type 1-associated optic pathway glioma following chemotherapy: a multicenter retrospective analysis. , 2012, Neuro-oncology.

[3]  David Fitzpatrick,et al.  Central Projections of Retinal Ganglion Cells , 2001 .

[4]  Alan Connelly,et al.  MRtrix: Diffusion tractography in crossing fiber regions , 2012, Int. J. Imaging Syst. Technol..

[5]  Sebastien Ourselin,et al.  Clinical Applications for Diffusion MRI and Tractography of Cranial Nerves Within the Posterior Fossa: A Systematic Review , 2019, Front. Neurosci..

[6]  L W CHACKO,et al.  THE LAMINAR PATTERN OF THE LATERAL GENICULATE BODY IN THE PRIMATES , 1948, Journal of neurology, neurosurgery, and psychiatry.

[7]  Bas Rokers,et al.  Linking Neural and Clinical Measures of Glaucoma with Diffusion Magnetic Resonance Imaging (dMRI) , 2018 .

[8]  F. Cornelissen,et al.  Fixel-Based Analysis of Visual Pathway White Matter in Primary Open-Angle Glaucoma. , 2019, Investigative ophthalmology & visual science.

[9]  Brian A. Wandell,et al.  Plasticity and Stability of the Visual System in Human Achiasma , 2012, Neuron.

[10]  Alan Connelly,et al.  SIFT2: Enabling dense quantitative assessment of brain white matter connectivity using streamlines tractography , 2015, NeuroImage.

[11]  Daniel C Alexander,et al.  Multiple‐Fiber Reconstruction Algorithms for Diffusion MRI , 2005, Annals of the New York Academy of Sciences.

[12]  W. I. McDonald,et al.  MRI of the optic nerve in benign intracranial hypertension , 1996, Neuroradiology.

[13]  Alexandra J. Golby,et al.  Anatomical assessment of trigeminal nerve tractography using diffusion MRI: A comparison of acquisition b-values and single- and multi-fiber tracking strategies , 2020, NeuroImage: Clinical.

[14]  Carole Frindel,et al.  Overcoming Challenges of Cranial Nerve Tractography: A Targeted Review , 2018, Neurosurgery.

[15]  Mark Jenkinson,et al.  The minimal preprocessing pipelines for the Human Connectome Project , 2013, NeuroImage.

[16]  Uta Schick,et al.  Surgical management of meningiomas involving the optic nerve sheath. , 2004, Journal of neurosurgery.

[17]  G. T. Plant,et al.  Detection of optic nerve atrophy following a single episode of unilateral optic neuritis by MRI using a fat-saturated short-echo fast FLAIR sequence , 2001, Neuroradiology.

[18]  Kirby G. Vosburgh,et al.  3D Slicer: A Platform for Subject-Specific Image Analysis, Visualization, and Clinical Support , 2014 .

[19]  F. Cotton,et al.  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. , 2018, Neurosurgery.

[20]  Brendan Behan,et al.  Comparison of Diffusion-Weighted MRI Reconstruction Methods for Visualization of Cranial Nerves in Posterior Fossa Surgery , 2017, Front. Neurosci..

[21]  Alexandra J. Golby,et al.  Deep white matter analysis (DeepWMA): Fast and consistent tractography segmentation , 2020, Medical Image Anal..

[22]  J. Salazar,et al.  Anatomy of the Human Optic Nerve: Structure and Function , 2018, Optic Nerve.

[23]  W. Green,et al.  The histology of human glaucoma cupping and optic nerve damage: clinicopathologic correlation in 21 eyes. , 1979, Ophthalmology.

[24]  Peter F. Neher,et al.  The challenge of mapping the human connectome based on diffusion tractography , 2017, Nature Communications.

[25]  Stephen J. Jones,et al.  A serial MRI study following optic nerve mean area in acute optic neuritis. , 2004, Brain : a journal of neurology.

[26]  K. Cho,et al.  Ischemic Injury of the Papillomacular Bundle Is a Predictive Marker of Poor Vision in Eyes With Branch Retinal Artery Occlusion. , 2016, American journal of ophthalmology.

[27]  Hompson,et al.  A LONGITUDINAL STUDY OF ABNORMALITIES ON MRI AND DISABILITY FROM MULTIPLE SCLEROSIS , 2002 .

[28]  David J. Schaeffer,et al.  Microstructural differences in visual white matter tracts in people with aniridia , 2018, Neuroreport.

[29]  L. R. Dice.  Measures of the Amount of Ecologic Association Between Species , 1945 .

[30]  Fang-Cheng Yeh,et al.  Tractography for Surgical Neuro-Oncology Planning: Towards a Gold Standard , 2018, Neurotherapeutics.

[31]  John S Werner,et al.  Compromised Integrity of Central Visual Pathways in Patients With Macular Degeneration. , 2017, Investigative ophthalmology & visual science.

[32]  Yu-Chien Wu,et al.  Comparison of multi-shot and single shot echo-planar diffusion tensor techniques for the optic pathway in patients with neurofibromatosis type 1 , 2019, Neuroradiology.

[33]  D. Leopold,et al.  Anatomical accuracy of brain connections derived from diffusion MRI tractography is inherently limited , 2014, Proceedings of the National Academy of Sciences.

[34]  Ben Jeurissen,et al.  Diffusion MRI fiber tractography of the brain , 2019, NMR in biomedicine.

[35]  Kálmán v. Sántha.  Über das Verhalten der primären optischen Zentren bei einseitiger peripherer Blindheit , 2005, Albrecht von Graefes Archiv für Ophthalmologie.

[36]  Noritaka Komune,et al.  Prevention of postoperative visual field defect after the occipital transtentorial approach: anatomical study. , 2017, Journal of neurosurgery.

[37]  Rainer Goebel,et al.  High-resolution diffusion tensor imaging and tractography of the human optic chiasm at 9.4 T , 2008, NeuroImage.

[38]  Alexandra J. Golby,et al.  Performance of unscented Kalman filter tractography in edema: Analysis of the two-tensor model , 2017, NeuroImage: Clinical.

[39]  H. Krejčová,et al.  High Tension Versus Normal Tension Glaucoma. A Comparison of Structural and Functional Examinations , 2011 .

[40]  P. Basser,et al.  In vivo fiber tractography using DT‐MRI data , 2000, Magnetic resonance in medicine.

[41]  Felix C. Morency,et al.  A test-retest study on Parkinson's PPMI dataset yields statistically significant white matter fascicles , 2017, NeuroImage: Clinical.

[42]  Kristian Aquilina,et al.  Optic pathway glioma in children: does visual deficit correlate with radiology in focal exophytic lesions? , 2015, Child's Nervous System.

[43]  J Sijbers,et al.  Influence of User-Defined Parameters on Diffusion Tensor Tractography of the Corticospinal Tract , 2007, The neuroradiology journal.

[44]  Ye Wu,et al.  Test–retest reproducibility of white matter parcellation using diffusion MRI tractography fiber clustering , 2019, Human brain mapping.

[45]  A. Krainik,et al.  Track‐weighted imaging for neuroretina: Evaluations in healthy volunteers and ischemic optic neuropathy , 2018, Journal of magnetic resonance imaging : JMRI.

[46]  D. Parker,et al.  Analysis of partial volume effects in diffusion‐tensor MRI , 2001, Magnetic resonance in medicine.

[47]  M. Kupersmith,et al.  A long-term visual outcome comparison in patients with optic nerve sheath meningioma managed with observation, surgery, radiotherapy, or surgery and radiotherapy. , 2002, Ophthalmology.

[48]  Daniel S Reich,et al.  Diffusion Tensor Imaging of the Optic Tracts in Multiple Sclerosis: Association with Retinal Thinning and Visual Disability , 2011, Journal of neuroimaging : official journal of the American Society of Neuroimaging.

[49]  K. Davis,et al.  Diffusivity signatures characterize trigeminal neuralgia associated with multiple sclerosis , 2016, Multiple sclerosis.

[50]  B. Wandell.  Clarifying Human White Matter. , 2016, Annual review of neuroscience.

[51]  Atira Bick,et al.  The impact of localized grey matter damage on neighboring connectivity: posterior cortical atrophy and the visual network , 2018, Brain Imaging and Behavior.

[52]  W. G. Cochran.  The comparison of percentages in matched samples. , 1950, Biometrika.

[53]  N. Raz,et al.  Focal demyelinative damage and neighboring white matter integrity: an optic neuritis study , 2015, Multiple sclerosis.

[54]  Foram Gala,et al.  Magnetic resonance imaging of optic nerve , 2015, Indian Journal of Radiology and Imaging.

[55]  Yi Wang,et al.  Assessment of optic nerve and optic tract alterations in patients with orbital space-occupying lesions using probabilistic diffusion tractography. , 2019, International journal of ophthalmology.

[56]  Thomas Welton,et al.  Aberrant visual pathway development in albinism: From retina to cortex , 2018, Human brain mapping.

[57]  Lipeng Ning,et al.  MK-curve - Characterizing the relation between mean kurtosis and alterations in the diffusion MRI signal , 2019, NeuroImage.

[58]  P. Basser,et al.  MR diffusion tensor spectroscopy and imaging. , 1994, Biophysical journal.

[59]  Tobias Kober,et al.  Investigation of lateral geniculate nucleus volume and diffusion tensor imaging in patients with normal tension glaucoma using 7 tesla magnetic resonance imaging , 2018, PloS one.

[60]  Mark W. Woolrich,et al.  Probabilistic diffusion tractography with multiple fibre orientations: What can we gain? , 2007, NeuroImage.

[61]  Y. Anık,et al.  Correlation of the measurements of optical coherence tomography and diffuse tension imaging of optic pathways in amblyopia , 2017, International Ophthalmology.

[62]  J. Berman,et al.  Fractional anisotropy of the optic radiations is associated with visual acuity loss in optic pathway gliomas of neurofibromatosis type 1. , 2013, Neuro-oncology.

[63]  C Kupfer,et al.  Quantitative histology of optic nerve, optic tract and lateral geniculate nucleus of man. , 1967, Journal of anatomy.

[64]  Michael Wall,et al.  High- and low-risk profiles for the development of multiple sclerosis within 10 years after optic neuritis: experience of the optic neuritis treatment trial. , 2003, Archives of ophthalmology.

[65]  M. Jenkinson.  Non-linear registration aka Spatial normalisation , 2007 .

[66]  Lenworth N. Johnson.  The 5-year risk of MS after optic neuritis , 1998, Neurology.

[67]  Gabriele Schackert,et al.  Comparison of probabilistic and deterministic fiber tracking of cranial nerves. , 2017, Journal of neurosurgery.

[68]  L. Becerra,et al.  Direct optic nerve pulvinar connections defined by diffusion MR tractography in humans: Implications for photophobia , 2012, Human brain mapping.

[69]  Raphael Guzman,et al.  Application of diffusion tensor tractography in pediatric optic pathway glioma. , 2012, Journal of neurosurgery. Pediatrics.

[70]  Yogesh Rathi,et al.  An anatomically curated fiber clustering white matter atlas for consistent white matter tract parcellation across the lifespan , 2018, NeuroImage.

[71]  Essa Yacoub,et al.  The WU-Minn Human Connectome Project: An overview , 2013, NeuroImage.

[72]  Alexandra J. Golby,et al.  Corticospinal tract modeling for neurosurgical planning by tracking through regions of peritumoral edema and crossing fibers using two-tensor unscented Kalman filter tractography , 2016, International Journal of Computer Assisted Radiology and Surgery.

[73]  Alexandra J. Golby,et al.  Creation of a novel trigeminal tractography atlas for automated trigeminal nerve identification , 2020, NeuroImage.

[74]  J. Sahel,et al.  The development of white matter structural changes during the process of deterioration of the visual field , 2019, Scientific Reports.

[75]  Jean-Philippe Thiran,et al.  COMMIT: Convex Optimization Modeling for Microstructure Informed Tractography , 2015, IEEE Transactions on Medical Imaging.

[76]  Noa Raz,et al.  Cortical and white matter mapping in the visual system-more than meets the eye: on the importance of functional imaging to understand visual system pathologies , 2014, Front. Integr. Neurosci..

[77]  Jelle Veraart,et al.  Gibbs ringing in diffusion MRI , 2016, Magnetic resonance in medicine.

[78]  C W RUCKER,et al.  Notching of the optic chiasm by overlying arteries in pituitary tumors. , 1954, Transactions of the American Ophthalmological Society.

[79]  Yong Wang,et al.  Differences between generalized Q-sampling imaging and diffusion tensor imaging in visualization of crossing neural fibers in the brain , 2019, Surgical and Radiologic Anatomy.

[80]  Jens Frahm,et al.  Reconstruction and Dissection of the Entire Human Visual Pathway Using Diffusion Tensor MRI , 2009, Front. Neuroanat..

[81]  Alexandra J. Golby,et al.  Free water modeling of peritumoral edema using multi-fiber tractography: Application to tracking the arcuate fasciculus for neurosurgical planning , 2018, PloS one.

[82]  Franco Pestilli,et al.  White matter consequences of retinal receptor and ganglion cell damage. , 2014, Investigative ophthalmology & visual science.

[83]  Arata Watanabe,et al.  Effect of intracranial pressure on the diameter of the optic nerve sheath. , 2008, Journal of neurosurgery.

[84]  Society of magnetic resonance in medicine , 1990 .

[85]  D. Louis Collins,et al.  Symmetric Atlasing and Model Based Segmentation: An Application to the Hippocampus in Older Adults , 2006, MICCAI.

[86]  Aviv A. Mezer,et al.  Diffusivity and quantitative T1 profile of human visual white matter tracts after retinal ganglion cell damage , 2019, NeuroImage: Clinical.

[87]  Bas Rokers,et al.  Eye Movements , Strabismus , Amblyopia and Neuro-Ophthalmology Retinothalamic White Matter Abnormalities in Amblyopia , 2018 .

[88]  Jonathan D. Trobe,et al.  The 5-year risk of MS after optic neuritis , 1998, Neurology.

[89]  Kartini Rahmat,et al.  Novel use of 3T MRI in assessment of optic nerve volume in glaucoma , 2014, Graefe's Archive for Clinical and Experimental Ophthalmology.

[90]  N. Makris,et al.  High angular resolution diffusion imaging reveals intravoxel white matter fiber heterogeneity , 2002, Magnetic resonance in medicine.

[91]  Carsten Finke,et al.  Anatomical Wiring and Functional Networking Changes in the Visual System Following Optic Neuritis , 2018, JAMA neurology.

[92]  Martha Elizabeth Shenton,et al.  Filtered Multitensor Tractography , 2010, IEEE Transactions on Medical Imaging.

[93]  Antony B. Morland,et al.  Quantifying nerve decussation abnormalities in the optic chiasm , 2019, NeuroImage: Clinical.

[94]  E. Hoving,et al.  The role of diffusion tensor imaging in brain tumor surgery: A review of the literature , 2014, Clinical Neurology and Neurosurgery.

[95]  Fang-Cheng Yeh,et al.  Visualization of Cranial Nerves Using High-Definition Fiber Tractography. , 2016, Neurosurgery.

[96]  C. Matthies,et al.  Probabilistic Fiber-Tracking Reveals Degeneration of the Contralateral Auditory Pathway in Patients with Vestibular Schwannoma , 2016, American Journal of Neuroradiology.

[97]  Peter Boesiger,et al.  Reconstruction of the human visual system based on DTI fiber tracking , 2007, Journal of magnetic resonance imaging : JMRI.

[98]  Arthur W. Toga,et al.  Automated retinofugal visual pathway reconstruction with multi-shell HARDI and FOD-based analysis , 2016, NeuroImage.

[99]  Kerstin Pannek,et al.  How many streamlines are required for reliable probabilistic tractography? Solutions for microstructural measurements and neurosurgical planning , 2020, NeuroImage.

[100]  Jun Ma,et al.  Preoperative Visualization of Cranial Nerves in Skull Base Tumor Surgery Using Diffusion Tensor Imaging Technology. , 2016, Turkish neurosurgery.

[101]  Alan Connelly,et al.  Direct estimation of the fiber orientation density function from diffusion-weighted MRI data using spherical deconvolution , 2004, NeuroImage.

[102]  Richard Bowman,et al.  Delineation of the visual pathway in paediatric optic pathway glioma patients using probabilistic tractography, and correlations with visual acuity , 2017, NeuroImage: Clinical.

[103]  M. Wintermark,et al.  Diffusion MRI tractography for improved transcranial MRI-guided focused ultrasound thalamotomy targeting for essential tremor , 2018, NeuroImage: Clinical.

[104]  Daniel S. Marcus,et al.  Obscuring Surface Anatomy in Volumetric Imaging Data , 2012, Neuroinformatics.

[105]  Brian A. Wandell,et al.  Ensemble Tractography , 2016, PLoS Comput. Biol..

[106]  W. Green,et al.  Optic nerve damage in human glaucoma. III. Quantitative correlation of nerve fiber loss and visual field defect in glaucoma, ischemic neuropathy, papilledema, and toxic neuropathy. , 1982, Archives of ophthalmology.

[107]  B. Wandell,et al.  Cortical Maps and White Matter Tracts following Long Period of Visual Deprivation and Retinal Image Restoration , 2010, Neuron.

[108]  Alexander Klistorner,et al.  Physiological Correlates and Predictors of Functional Recovery After Chiasmal Decompression , 2015, Journal of neuro-ophthalmology : the official journal of the North American Neuro-Ophthalmology Society.

[109]  Gary F. Egan,et al.  Optic nerve diffusion changes and atrophy jointly predict visual dysfunction after optic neuritis , 2009, NeuroImage.

[110]  Carl-Fredrik Westin,et al.  SlicerDMRI: Diffusion MRI and Tractography Research Software for Brain Cancer Surgery Planning and Visualization , 2020, JCO clinical cancer informatics.

[111]  Francesco Padormo,et al.  Quantitative Assessment of Secondary White Matter Injury in the Visual Pathway by Pituitary Adenomas: A Multimodal Study at 7 Tesla MRI , 2019, Journal of Neurological Surgery Part B: Skull Base.

[112]  Alan Connelly,et al.  Robust determination of the fibre orientation distribution in diffusion MRI: Non-negativity constrained super-resolved spherical deconvolution , 2007, NeuroImage.

[113]  Masaaki Hori,et al.  Alterations of the optic pathway between unilateral and bilateral optic nerve damage in multiple sclerosis as revealed by the combined use of advanced diffusion kurtosis imaging and visual evoked potentials. , 2017, Magnetic resonance imaging.

[114]  Carl-Fredrik Westin,et al.  SlicerDMRI: Open Source Diffusion MRI Software for Brain Cancer Research. , 2017, Cancer research.

[115]  N. De Stefano,et al.  Early changes of brain connectivity in primary open angle glaucoma , 2016, Human brain mapping.

[116]  S. Hickman,et al.  Optic Nerve Imaging in Multiple Sclerosis , 2007, Journal of neuroimaging : official journal of the American Society of Neuroimaging.