Creation of a novel trigeminal tractography atlas for automated trigeminal nerve identification

Diffusion MRI (dMRI) tractography has been successfully used to study the trigeminal nerves (TGNs) in many clinical and research applications. Currently, identification of the TGN in tractography data requires expert nerve selection using manually drawn regions of interest (ROIs), which is prone to inter-observer variability, time-consuming and carries high clinical and labor costs. To overcome these issues, we propose to create a novel anatomically curated TGN tractography atlas that enables automated identification of the TGN from dMRI tractography. In this paper, we first illustrate the creation of a trigeminal tractography atlas. Leveraging a well-established computational pipeline and expert neuroanatomical knowledge, we generate a data-driven TGN fiber clustering atlas using tractography data from 50 subjects from the Human Connectome Project. Then, we demonstrate the application of the proposed atlas for automated TGN identification in new subjects, without relying on expert ROI placement. Quantitative and visual experiments are performed with comparison to expert TGN identification using dMRI data from two different acquisition sites. We show highly comparable results between the automatically and manually identified TGNs in terms of spatial overlap and visualization, while our proposed method has several advantages. First, our method performs automated TGN identification, and thus it provides an efficient tool to reduce expert labor costs and inter-operator bias relative to expert manual selection. Second, our method is robust to potential imaging artifacts and/or noise that can prevent successful manual ROI placement for TGN selection and hence yields a higher successful TGN identification rate.

[1]  M. Mallar Chakravarty,et al.  Polygenic Risk and Neural Substrates of Attention-Deficit/Hyperactivity Disorder Symptoms in Youths With a History of Mild Traumatic Brain Injury , 2019, Biological Psychiatry.

[2]  Sugoto Mukherjee,et al.  Imaging of Vascular Compression Syndromes. , 2017, Radiologic clinics of North America.

[3]  Soni Neetu,et al.  Microstructural abnormalities of the trigeminal nerve by diffusion-tensor imaging in trigeminal neuralgia without neurovascular compression , 2016, The neuroradiology journal.

[4]  Lauren O'Donnell,et al.  Post-Traumatic Cerebral Microhemorrhages and their Effects Upon White Matter Connectivity in the Aging Human Brain , 2019, 2019 41st Annual International Conference of the IEEE Engineering in Medicine and Biology Society (EMBC).

[5]  Sharmin Sultana,et al.  Development of an Atlas-Based Segmentation of Cranial Nerves Using Shape-Aware Discrete Deformable Models for Neurosurgical Planning and Simulation , 2017 .

[6]  Jan Sijbers,et al.  Probabilistic fiber tracking using the residual bootstrap with constrained spherical deconvolution , 2011, Human brain mapping.

[7]  Alexandra J. Golby,et al.  Automated connectivity-based groupwise cortical atlas generation: Application to data of neurosurgical patients with brain tumors for cortical parcellation prediction , 2017, 2017 IEEE 14th International Symposium on Biomedical Imaging (ISBI 2017).

[8]  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.

[9]  Rickey E Carter,et al.  Retrospective Analysis of Interobserver Spatial Variability in the Localization of Broca's and Wernicke's Areas Using Three Different fMRI Language Paradigms , 2015, Journal of neuroimaging : official journal of the American Society of Neuroimaging.

[10]  Fan Zhang,et al.  Image Registration to Compensate for EPI Distortion in Patients with Brain Tumors: An Evaluation of Tract‐Specific Effects , 2018, Journal of neuroimaging : official journal of the American Society of Neuroimaging.

[11]  Peter Savadjiev,et al.  Whole brain white matter connectivity analysis using machine learning: An application to autism , 2017, NeuroImage.

[12]  Juha Öhman,et al.  Repeatability and variation of region-of-interest methods using quantitative diffusion tensor MR imaging of the brain , 2012, BMC Medical Imaging.

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

[14]  J. Casselman,et al.  MRI of the cranial nerves--more than meets the eye: technical considerations and advanced anatomy. , 2008, Neuroimaging clinics of North America.

[15]  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.

[16]  Paul Suetens,et al.  Global tractography of multi-shell diffusion-weighted imaging data using a multi-tissue model , 2015, NeuroImage.

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

[18]  Jitendra Malik,et al.  Spectral grouping using the Nystrom method , 2004, IEEE Transactions on Pattern Analysis and Machine Intelligence.

[19]  Jean-Francois Mangin,et al.  Clustering of Whole-Brain White Matter Short Association Bundles Using HARDI Data , 2017, Front. Neuroinform..

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

[21]  M. Leandri,et al.  Trigeminal neuralgia in pontine ischaemia. , 1997, Journal of neurology, neurosurgery, and psychiatry.

[22]  Carole Frindel,et al.  Full tractography for detecting the position of cranial nerves in preoperative planning for skull base surgery: technical note. , 2020, Journal of neurosurgery.

[23]  David Metcalf,et al.  A Digital Brain Atlas for Surgical Planning, Model-Driven Segmentation, and Teaching , 1996, IEEE Trans. Vis. Comput. Graph..

[24]  Francesco Sammartino,et al.  Diffusion tensor imaging assessment of microstructural brainstem integrity in Chiari malformation Type I. , 2016, Journal of neurosurgery.

[25]  William M. Wells,et al.  Comparison between two white matter segmentation strategies: An investigation into white matter segmentation consistency , 2017, 2017 IEEE 14th International Symposium on Biomedical Imaging (ISBI 2017).

[26]  L. O'Donnell,et al.  Reconstruction of the arcuate fasciculus for surgical planning in the setting of peritumoral edema using two-tensor unscented Kalman filter tractography , 2015, NeuroImage: Clinical.

[27]  Peter Savadjiev,et al.  Genetic load determines atrophy in hand cortico‐striatal pathways in presymptomatic Huntington's disease , 2018, Human brain mapping.

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

[29]  L. Zollei,et al.  A combined fMRI and DTI examination of functional language lateralization and arcuate fasciculus structure: Effects of degree versus direction of hand preference , 2010, Brain and Cognition.

[30]  Paul J. Laurienti,et al.  An automated method for neuroanatomic and cytoarchitectonic atlas-based interrogation of fMRI data sets , 2003, NeuroImage.

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

[32]  Jean-Francois Mangin,et al.  Reproducibility of superficial white matter tracts using diffusion-weighted imaging tractography , 2017, NeuroImage.

[33]  W. Eric L. Grimson,et al.  Automated Atlas-Based Clustering of White Matter Fiber Tracts from DTMRI , 2005, MICCAI.

[34]  Alexandra J. Golby,et al.  Deep White Matter Analysis: Fast, Consistent Tractography Segmentation Across Populations and dMRI Acquisitions , 2019, MICCAI.

[35]  Shunrou Fujiwara,et al.  High‐resolution Diffusion Tensor Imaging for the Detection of Diffusion Abnormalities in the Trigeminal Nerves of Patients with Trigeminal Neuralgia Caused by Neurovascular Compression , 2011, Journal of neuroimaging : official journal of the American Society of Neuroimaging.

[36]  P. Jannetta,et al.  Arterial compression of the trigeminal nerve at the pons in patients with trigeminal neuralgia. , 1967, Journal of neurosurgery.

[37]  A. Yoshida,et al.  Physiological and morphological characteristics of periodontal mesencephalic trigeminal neurons in the cat — intra-axonal staining with HRP , 1989, Brain Research.

[38]  Yogesh Rathi,et al.  Joint Multi-Fiber NODDI Parameter Estimation and Tractography Using the Unscented Information Filter , 2016, Front. Neurosci..

[39]  Carl-Fredrik Westin,et al.  Automatic Tractography Segmentation Using a High-Dimensional White Matter Atlas , 2007, IEEE Transactions on Medical Imaging.

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

[41]  Steven J Scrivani,et al.  Trigeminal neuralgia. , 2022, Oral surgery, oral medicine, oral pathology, oral radiology, and endodontics.

[42]  H. Urbach,et al.  Imaging of Neurovascular Compression Syndromes: Trigeminal Neuralgia, Hemifacial Spasm, Vestibular Paroxysmia, and Glossopharyngeal Neuralgia , 2016, American Journal of Neuroradiology.

[43]  Alexandra Sturm,et al.  An Eight-week, Open-trial, Pilot Feasibility Study of Trigeminal Nerve Stimulation in Youth With Attention-deficit/Hyperactivity Disorder , 2015, Brain Stimulation.

[44]  Anna Vilanova,et al.  Evaluation of fiber clustering methods for diffusion tensor imaging , 2005, VIS 05. IEEE Visualization, 2005..

[45]  Yogesh Rathi,et al.  Investigation into local white matter abnormality in emotional processing and sensorimotor areas using an automatically annotated fiber clustering in major depressive disorder , 2018, NeuroImage.

[46]  Ian A. Cook,et al.  Trigeminal nerve stimulation in major depressive disorder: First proof of concept in an open pilot trial , 2011, Epilepsy & Behavior.

[47]  A. Golby,et al.  Trigeminal neuralgia resulting from infarction of the root entry zone of the trigeminal nerve: case report. , 1998, Neurosurgery.

[48]  Osamu Abe,et al.  3T PROPELLER diffusion tensor fiber tractography: a feasibility study for cranial nerve fiber tracking , 2007, Radiation Medicine.

[49]  W. Eric L. Grimson,et al.  Consistency Clustering: A Robust Algorithm for Group-wise Registration, Segmentation and Automatic Atlas Construction in Diffusion MRI , 2009, International Journal of Computer Vision.

[50]  S. Love,et al.  Trigeminal neuralgia: pathology and pathogenesis. , 2001, Brain : a journal of neurology.

[51]  J L Go,et al.  The trigeminal nerve. , 2001, Seminars in ultrasound, CT, and MR.

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

[53]  J. Arvidsson,et al.  Transganglionic degeneration in trigeminal primary sensory neurons , 1975, Brain Research.

[54]  Tohru Kurabayashi,et al.  Trigeminal neuralgia: evaluation of neuralgic manifestation and site of neurovascular compression with 3D CISS MR imaging and MR angiography. , 2003, Radiology.

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

[56]  Mark W. Woolrich,et al.  FSL , 2012, NeuroImage.

[57]  R. Kikinis,et al.  Interactive Diffusion Tensor Tractography Visualization for Neurosurgical Planning , 2011, Neurosurgery.

[58]  Ninon Burgos,et al.  New advances in the Clinica software platform for clinical neuroimaging studies , 2019 .

[59]  A. Singleton,et al.  The Parkinson Progression Marker Initiative (PPMI) , 2011, Progress in Neurobiology.

[60]  Makoto Oishi,et al.  [Depiction of the trigeminal nerve deviated by a tumor lesion, using probabilistic diffusion tensor tractography]. , 2011, No shinkei geka. Neurological surgery.

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

[62]  A Meyer-Lindenberg,et al.  Ferréol-Besnier disease with associated recurrent meningitis. , 1997, Journal of neurology, neurosurgery, and psychiatry.

[63]  Jean-Francois Mangin,et al.  An Example-Based Multi-Atlas Approach to Automatic Labeling of White Matter Tracts , 2015, PloS one.

[64]  C. Westin,et al.  Automated white matter fiber tract identification in patients with brain tumors , 2016, NeuroImage: Clinical.

[65]  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.

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

[67]  Karen D. Davis,et al.  Predicting pain relief: Use of pre-surgical trigeminal nerve diffusion metrics in trigeminal neuralgia , 2017, NeuroImage: Clinical.

[68]  Bruce Fischl,et al.  FreeSurfer , 2012, NeuroImage.

[69]  Liu Lizhi,et al.  The significance of diffusion tensor magnetic resonance imaging for patients with nasopharyngeal carcinoma and trigeminal nerve invasion , 2017, Medicine.

[70]  Arzu Arslan,et al.  Driven equilibrium (drive) MR imaging of the cranial nerves V-VIII: comparison with the T2-weighted 3D TSE sequence. , 2004, European journal of radiology.

[71]  Aage R. M ller Trigeminal Neuralgia Resulting from Infarction of the Root Entry Zone of the Trigeminal Nerve: Case Report , 1998 .

[72]  David Qixiang Chen,et al.  Three-Dimensional In Vivo Modeling of Vestibular Schwannomas and Surrounding Cranial Nerves With Diffusion Imaging Tractography , 2011, Neurosurgery.

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

[74]  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.

[75]  Arthur W. Toga,et al.  Atlas-guided tract reconstruction for automated and comprehensive examination of the white matter anatomy , 2010, NeuroImage.

[76]  W. Joo,et al.  Microsurgical anatomy of the trigeminal nerve , 2014, Clinical anatomy.

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

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

[79]  Ozlem Coskun,et al.  MR Tractography in Short Lasting Unilateral Neuralgiform Headache Attacks with Conjunctival Injection and Tearing (SUNCT) Patients: Case Reports. , 2017, Pain medicine.

[80]  Erlend Hodneland,et al.  Registration of FA and T1-Weighted MRI Data of Healthy Human Brain Based on Template Matching and Normalized Cross-Correlation , 2013, Journal of Digital Imaging.

[81]  Roberto García-Leal,et al.  Neurovascular Relations of the Trigeminal Nerve in Asymptomatic Individuals Studied with High‐Resolution Three‐Dimensional Magnetic Resonance Imaging , 2019, Anatomical record.

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

[83]  C. Westin,et al.  Resolving crossings in the corticospinal tract by two-tensor streamline tractography: Method and clinical assessment using fMRI , 2009, NeuroImage.

[84]  Thomas R. Barrick,et al.  Atlas-based segmentation of white matter tracts of the human brain using diffusion tensor tractography and comparison with classical dissection , 2008, NeuroImage.

[85]  Hideo Ono,et al.  The trigeminal root: an anatomical study using magnetic resonance imaging , 2018, Surgical and Radiologic Anatomy.

[86]  Chan-A. Park,et al.  7.0 Tesla MRI tractography in patients with trigeminal neuralgia. , 2018, Magnetic resonance imaging.

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

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

[89]  Yunyun Duan,et al.  Microstructural abnormalities in the trigeminal nerves of patients with trigeminal neuralgia revealed by multiple diffusion metrics. , 2013, European journal of radiology.

[90]  T. Hummel,et al.  Chemosensory event-related potentials in response to trigeminal and olfactory stimulation in idiopathic Parkinson's disease , 1997, Neurology.

[91]  Zhigang Qi,et al.  Identification of cranial nerves around trigeminal schwannomas using diffusion tensor tractography: a technical note and report of 3 cases , 2016, Acta Neurochirurgica.

[92]  Carl-Fredrik Westin,et al.  Unbiased Groupwise Registration of White Matter Tractography , 2012, MICCAI.

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