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Neuroimage. 2021 Nov;243:118502. doi: 10.1016/j.neuroimage.2021.118502. Epub 2021 Aug 22.

Tractography dissection variability: What happens when 42 groups dissect 14 white matter bundles on the same dataset?.

NeuroImage

Kurt G Schilling, François Rheault, Laurent Petit, Colin B Hansen, Vishwesh Nath, Fang-Cheng Yeh, Gabriel Girard, Muhamed Barakovic, Jonathan Rafael-Patino, Thomas Yu, Elda Fischi-Gomez, Marco Pizzolato, Mario Ocampo-Pineda, Simona Schiavi, Erick J Canales-Rodríguez, Alessandro Daducci, Cristina Granziera, Giorgio Innocenti, Jean-Philippe Thiran, Laura Mancini, Stephen Wastling, Sirio Cocozza, Maria Petracca, Giuseppe Pontillo, Matteo Mancini, Sjoerd B Vos, Vejay N Vakharia, John S Duncan, Helena Melero, Lidia Manzanedo, Emilio Sanz-Morales, Ángel Peña-Melián, Fernando Calamante, Arnaud Attyé, Ryan P Cabeen, Laura Korobova, Arthur W Toga, Anupa Ambili Vijayakumari, Drew Parker, Ragini Verma, Ahmed Radwan, Stefan Sunaert, Louise Emsell, Alberto De Luca, Alexander Leemans, Claude J Bajada, Hamied Haroon, Hojjatollah Azadbakht, Maxime Chamberland, Sila Genc, Chantal M W Tax, Ping-Hong Yeh, Rujirutana Srikanchana, Colin D Mcknight, Joseph Yuan-Mou Yang, Jian Chen, Claire E Kelly, Chun-Hung Yeh, Jerome Cochereau, Jerome J Maller, Thomas Welton, Fabien Almairac, Kiran K Seunarine, Chris A Clark, Fan Zhang, Nikos Makris, Alexandra Golby, Yogesh Rathi, Lauren J O'Donnell, Yihao Xia, Dogu Baran Aydogan, Yonggang Shi, Francisco Guerreiro Fernandes, Mathijs Raemaekers, Shaun Warrington, Stijn Michielse, Alonso Ramírez-Manzanares, Luis Concha, Ramón Aranda, Mariano Rivera Meraz, Garikoitz Lerma-Usabiaga, Lucas Roitman, Lucius S Fekonja, Navona Calarco, Michael Joseph, Hajer Nakua, Aristotle N Voineskos, Philippe Karan, Gabrielle Grenier, Jon Haitz Legarreta, Nagesh Adluru, Veena A Nair, Vivek Prabhakaran, Andrew L Alexander, Koji Kamagata, Yuya Saito, Wataru Uchida, Christina Andica, Masahiro Abe, Roza G Bayrak, Claudia A M Gandini Wheeler-Kingshott, Egidio D'Angelo, Fulvia Palesi, Giovanni Savini, Nicolò Rolandi, Pamela Guevara, Josselin Houenou, Narciso López-López, Jean-François Mangin, Cyril Poupon, Claudio Román, Andrea Vázquez, Chiara Maffei, Mavilde Arantes, José Paulo Andrade, Susana Maria Silva, Vince D Calhoun, Eduardo Caverzasi, Simone Sacco, Michael Lauricella, Franco Pestilli, Daniel Bullock, Yang Zhan, Edith Brignoni-Perez, Catherine Lebel, Jess E Reynolds, Igor Nestrasil, René Labounek, Christophe Lenglet, Amy Paulson, Stefania Aulicka, Sarah R Heilbronner, Katja Heuer, Bramsh Qamar Chandio, Javier Guaje, Wei Tang, Eleftherios Garyfallidis, Rajikha Raja, Adam W Anderson, Bennett A Landman, Maxime Descoteaux

Affiliations

  1. Department of Radiology and Radiological Sciences, Vanderbilt University Medical Center, Nashville, TN, United States. Electronic address: [email protected].
  2. SCIL, Université de Sherbrooke, Québec, Canada.
  3. Groupe dImagerie Neurofonctionnelle, Institut Des Maladies Neurodegeneratives, CNRS, CEA University of Bordeaux, Bordeaux, France.
  4. Department of Electrical Engineering and Computer Science, Vanderbilt University, Nashville, TN, United States.
  5. Department of Neurological Surgery, University of Pittsburgh, Pittsburgh, PA, United States.
  6. CIBM Center for BioMedical Imaging, Lausanne, Switzerland.
  7. Translational Imaging in Neurology (ThINK), Department of Medicine and Biomedical Engineering, University Hospital and University of Basel, Basel, Switzerland.
  8. Signal Processing Lab (LTS5), École Polytechnique Fédérale de Lausanne, Lausanne, Switzerland.
  9. Department of Applied Mathematics and Computer Science, Technical University of Denmark, Kongens Lyngby, Denmark.
  10. Department of Computer Science, University of Verona, Italy.
  11. Department of Neuroscience, Karolinska Institutet, Stockholm, Sweden.
  12. Lysholm Department of Neuroradiology, National Hospital for Neurology & Neurosurgery, UCL Hospitals NHS Foundation Trust, London, United Kingdom.
  13. Department of Advanced Biomedical Sciences, University "Federico II", Naples, Italy.
  14. Department of Neurosciences and Reproductive and Odontostomatological Sciences, University "Federico II", Naples, Italy.
  15. Department of Neuroscience, Brighton and Sussex Medical School, University of Sussex, Brighton, United Kingdom.
  16. Centre for Medical Image Computing, University College London, London, United Kingdom.
  17. Department of Clinical and Experimental Epilepsy, University College London, London, United Kingdom.
  18. Epilepsy Society MRI Unit, Chalfont St Peter, United Kingdom.
  19. Departamento de Psicobiología y Metodología en Ciencias del Comportamiento - Universidad Complutense de Madrid, Spain Laboratorio de Análisis de Imagen Médica y Biometría (LAIMBIO), Universidad Rey Juan Carlos, Madrid, Spain.
  20. Facultad de Ciencias de la Salud, Universidad Rey Juan Carlos, Madrid, Spain.
  21. Laboratorio de Análisis de Imagen Médica y Biometría (LAIMBIO), Universidad Rey Juan Carlos, Madrid, Spain.
  22. Departamento de Anatomía, Facultad de Medicina, Universidad Complutense de Madrid, Madrid, Spain.
  23. Sydney Imaging and School of Biomedical Engineering, The University of Sydney, Sydney, Australia.
  24. School of Biomedical Engineering, The University of Sydney, Sydney, Australia.
  25. Laboratory of Neuro Imaging, Stevens Neuroimaging and Informatics Institute, Keck School of Medicine of USC, University of Southern California, Los Angeles, CA, United States.
  26. Center for Integrative Connectomics, Stevens Neuroimaging and Informatics Institute, Keck School of Medicine of USC, University of Southern California, Los Angeles, CA, United States.
  27. Department of Radiology, University of Pennsylvania, Philadelphia, PA, United States.
  28. KU Leuven, Department of Imaging and Pathology, Translational MRI, B-3000, Leuven, Belgium.
  29. PROVIDI Lab, UMC Utrecht, The Netherlands.
  30. Department of Physiology and Biochemistry, Faculty of Medicine and Surgery, University of Malta, Malta.
  31. Division of Neuroscience & Experimental Psychology, Faculty of Biology, Medicine and Health, The University of Manchester, Manchester Academic Health Science Centre, Manchester, United Kingdom.
  32. AINOSTICS Limited, London, United Kingdom.
  33. Cardiff University Brain Research Imaging Centre (CUBRIC), Cardiff University, Cardiff, United Kingdom.
  34. National Intrepid Center of Excellence, Walter Reed National Military Medical Center, Bethesda, MD, USA.
  35. Department of Radiology and Radiological Sciences, Vanderbilt University Medical Center, Nashville, TN, United States.
  36. Department of Neurosurgery, Neuroscience Advanced Clinical Imaging Suite (NACIS), Royal Children's Hospital, Parkville, Melbourne, Australia.
  37. Developmental Imaging, Murdoch Children's Research Institute, Melbourne, Australia.
  38. Victorian Infant Brain Studies, Murdoch Children's Research Institute, Melbourne, Australia.
  39. Institute for Radiological Research, Chang Gung University & Chang Gung Memorial Hospital, Taoyuan, Taiwan.
  40. Poitiers University Hospital, France.
  41. MRI Clinical Science Specialist, General Electric Healthcare, Australia.
  42. National Neuroscience Institute, Singapore.
  43. Neurosurgery department, Hôpital Pasteur, University Hospital of Nice, Côte d'Azur University, France.
  44. Developmental Imaging and Biophysics Section, UCL GOS Institute of Child Health, London.
  45. Brigham & Women's Hospital and Harvard Medical School, Boston, Massachusetts, USA.
  46. University of Southern California, Keck School of Medicine, Neuroimaging and Informatics Institute, Los Angeles, California, United States.
  47. Department of Neuroscience and Biomedical Engineering, Aalto University School of Science, Espoo, Finland.
  48. UMC Utrecht Brain Center, Department of Neurology&Neurosurgery, Utrecht, the Netherlands.
  49. Sir Peter Mansfield Imaging Centre, School of Medicine, University of Nottingham, UK.
  50. Department of Neurosurgery, School for Mental Health and Neuroscience, Maastricht University.
  51. Centro de Investigación en Matemáticas A.C. (CIMAT), Guanajuato, Mexico.
  52. Universidad Nacional Autonoma de Mexico, Institute of Neurobiology, Mexico City, Mexico.
  53. Centro de Investigación Científica y de Educación Superior de Ensenada (CICESE-UT3), Cátedras-CONACyT, Ensenada, Mexico.
  54. Department of Psychology, Stanford University, Stanford, California, USA.
  55. Department of Neurosurgery, Charité - Universitätsmedizin Berlin, Berlin, Germany.
  56. Kimel Family Translational Imaging-Genetics Laboratory, Research Imaging Centre, Centre for Addiction and Mental Health, Toronto, Ontario.
  57. University of Wisconsin-Madison, Madison, WI, USA.
  58. Department of Radiology, Juntendo University Graduate School of Medicine, Tokyo Japan.
  59. NMR Research Unit, Queen Square MS Centre, Department of Neuroinflammation, UCL Queen Square Institute of Neurology, Faculty of Brain Sciences, University College London, London, United Kingdom.
  60. Department of Brain and Behavioral Sciences, University of Pavia, Italy.
  61. Brain MRI 3T Research Center, IRCCS Mondino Foundation, Pavia, Italy.
  62. Universidad de Concepción, Faculty of Engineering, Concepción, Chile.
  63. Université Paris-Saclay, CEA, CNRS, Neurospin, Gif-sur-Yvette, France.
  64. Athinoula A. Martinos Center for Biomedical Imaging, Massachusetts General Hospital and Harvard Medical School, Boston, Massachusetts, USA.
  65. Department of Biomedicine, Unit of Anatomy, Faculty of Medicine of the University of Porto, Al. Professor Hernâni Monteiro, Porto, Portugal.
  66. Tri-institutional Center for Translational Research in Neuroimaging and Data Science (TReNDS), Georgia State University, Georgia Institute of Technology, Emory University, Atlanta, GA 30303, United States.
  67. Neurology Department UCSF Weill Institute for Neurosciences, University of California, San Francisco.
  68. Memory and Aging Center. UCSF Weill Institute for Neurosciences, University of California, San Francisco, USA.
  69. Department of Psychology, The University of Texas at Austin, TX 78731, USA.
  70. Brain Cognition and Brain Disease Institute, Shenzhen Institutes of Advanced Technology, Chinese Academy of Sciences, Shenzhen, 518055, China.
  71. Developmental-Behavioral Pediatrics Division, Department of Pediatrics, Stanford School of Medicine, Stanford, CA, United States.
  72. Department of Radiology, University of Calgary, 2500 University Drive NW, Calgary, AB, Canada, T2N 1N4.
  73. Division of Clinical Behavioral Neuroscience, Department of Pediatrics, University of Minnesota, Minneapolis, MN, USA.
  74. Center for Magnetic Resonance Research, Department of Radiology, University of Minnesota, Minneapolis, MN, USA.
  75. Department of Paediatric Neurology, University Hospital and Medicine Faculty, Masaryk University, Brno, Czech Republic.
  76. Department of Neuroscience, University of Minnesota, Minneapolis, MN, USA.
  77. Center for Research and Interdisciplinarity (CRI), INSERM U1284, Université de Paris, Paris, France.
  78. Department of Intelligent Systems Engineering, Indiana University, Bloomington, IN, USA.
  79. Department of Computer Science, Indiana University, Bloomington, IN, USA.
  80. University of Arkansas for Medical Sciences, Little Rock, AR, USA.
  81. Department of Radiology and Radiological Sciences, Vanderbilt University Medical Center, Nashville, TN, USA.

PMID: 34433094 DOI: 10.1016/j.neuroimage.2021.118502

Abstract

White matter bundle segmentation using diffusion MRI fiber tractography has become the method of choice to identify white matter fiber pathways in vivo in human brains. However, like other analyses of complex data, there is considerable variability in segmentation protocols and techniques. This can result in different reconstructions of the same intended white matter pathways, which directly affects tractography results, quantification, and interpretation. In this study, we aim to evaluate and quantify the variability that arises from different protocols for bundle segmentation. Through an open call to users of fiber tractography, including anatomists, clinicians, and algorithm developers, 42 independent teams were given processed sets of human whole-brain streamlines and asked to segment 14 white matter fascicles on six subjects. In total, we received 57 different bundle segmentation protocols, which enabled detailed volume-based and streamline-based analyses of agreement and disagreement among protocols for each fiber pathway. Results show that even when given the exact same sets of underlying streamlines, the variability across protocols for bundle segmentation is greater than all other sources of variability in the virtual dissection process, including variability within protocols and variability across subjects. In order to foster the use of tractography bundle dissection in routine clinical settings, and as a fundamental analytical tool, future endeavors must aim to resolve and reduce this heterogeneity. Although external validation is needed to verify the anatomical accuracy of bundle dissections, reducing heterogeneity is a step towards reproducible research and may be achieved through the use of standard nomenclature and definitions of white matter bundles and well-chosen constraints and decisions in the dissection process.

Copyright © 2021. Published by Elsevier Inc.

Keywords: Bundle segmentation; Dissection; Fiber pathways; Tractography; White matter

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