Cited by 182Advanced Neuroimaging Techniques and ApplicationsFunctional Brain Connectivity StudiesMedical Image Segmentation Techniques

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

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Schilling, Kurt G., Rheault, François, Petit, Laurent, Hansen, Colin B., Nath, Vishwesh, Yeh, Fang-Cheng, Girard, Gabriel, Barakovic, Muhamed, Rafael-Patino, Jonathan, Yu, Thomas, Fischi-Gomez, Elda, Pizzolato, Marco, Ocampo-Pineda, Mario, Schiavi, Simona, Canales-Rodríguez, Erick J., Daducci, Alessandro, Granziera, Cristina, Innocenti, Giorgio, Thiran, Jean-Philippe, Mancini, Laura, Wastling, Stephen, Cocozza, Sirio, Petracca, Maria, Pontillo, Giuseppe, Mancini, Matteo, Vos, Sjoerd B., Vakharia, Vejay N., Duncan, John S., Melero, Helena, Manzanedo, Lidia, Sanz-Morales, Emilio, Peña-Melián, Ángel, Calamante, Fernando, Attyé, Arnaud, Cabeen, Ryan P., Korobova, Laura, Toga, Arthur W., Vijayakumari, Anupa Ambili, Parker, Drew, Verma, Ragini, Radwan, Ahmed, Sunaert, Stefan, Emsell, Louise, De Luca, Alberto, Leemans, Alexander, Bajada, Claude J., Haroon, Hamied, Azadbakht, Hojjatollah, Chamberland, Maxime, Genc, Sila, Tax, Chantal M.W., Yeh, Ping-Hong, Srikanchana, Rujirutana, Mcknight, Colin D., Yang, Joseph Yuan-Mou, Chen, Jian, Kelly, Claire E., Yeh, Chun-Hung, Cochereau, Jerome, Maller, Jerome J., Welton, Thomas, Almairac, Fabien, Seunarine, Kiran K, Clark, Chris A., Zhang, Fan, Makris, Nikos, Golby, Alexandra, Rathi, Yogesh, O'Donnell, Lauren J., Xia, Yihao, Aydogan, Dogu Baran, Shi, Yonggang, Fernandes, Francisco Guerreiro, Raemaekers, Mathijs, Warrington, Shaun, Michielse, Stijn, Ramírez-Manzanares, Alonso, Concha, Luis, Aranda, Ramón, Meraz, Mariano Rivera, Lerma-Usabiaga, Garikoitz, Roitman, Lucas, Fekonja, Lucius S., Calarco, Navona, Joseph, Michael, Nakua, Hajer, Voineskos, Aristotle N., Karan, Philippe, Grenier, Gabrielle, Legarreta, Jon Haitz, Adluru, Nagesh, Nair, Veena A., Prabhakaran, Vivek, Alexander, Andrew L., Kamagata, Koji, Saito, Yuya, Uchida, Wataru, Andica, Christina, Abe, Masahiro, Bayrak, Roza G., Wheeler-Kingshott, Claudia A.M. Gandini, D'Angelo, Egidio, Palesi, Fulvia, Savini, Giovanni, Rolandi, Nicolò, Guevara, Pamela, Houenou, Josselin, López-López, Narciso, Mangin, Jean-François, Poupon, Cyril, Román, Claudio, Vázquez, Andrea, Maffei, Chiara, Arantes, Mavilde, Andrade, José Paulo, Silva, Susana Maria, Calhoun, Vince D., Caverzasi, Eduardo, Sacco, Simone, Lauricella, Michael, Pestilli, Franco, Bullock, Daniel, Zhan, Yang, Brignoni-Perez, Edith, Lebel, Catherine, Reynolds, Jess E, Nestrasil, Igor, Labounek, René, Lenglet, Christophe, Paulson, Amy, Aulicka, Stefania, Heilbronner, Sarah R., Heuer, Katja, Chandio, Bramsh Qamar, Guaje, Javier, Tang, Wei, Garyfallidis, Eleftherios, Raja, Rajikha, Anderson, Adam W., Landman, Bennett A., Descoteaux, Maxime·2021·NeuroImage

DOI 10.1016/j.neuroimage.2021.118502PMC PMC8855321

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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.

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Authors: Schilling, K. G., Rheault, F., Petit, L., Hansen, C. B., Nath, V., Yeh, F.-C., Girard, G., Barakovic, M., Rafael-Patino, J., Yu, T., Fischi-Gomez, E., Pizzolato, M., Ocampo-Pineda, M., Schiavi, S., Canales-Rodríguez, E. J., Daducci, A., Granziera, C., Innocenti, G., Thiran, J.-P., Mancini, L., Wastling, S., Cocozza, S., Petracca, M., Pontillo, G., Mancini, M., Vos, S. B., Vakharia, V. N., Duncan, J. S., Melero, H., Manzanedo, L., Sanz-Morales, E., Peña-Melián, Á., Calamante, F., Attyé, A., Cabeen, R. P., Korobova, L., Toga, A. W., Vijayakumari, A. A., Parker, D., Verma, R., Radwan, A., Sunaert, S., Emsell, L., De Luca, A., Leemans, A., Bajada, C. J., Haroon, H., Azadbakht, H., Chamberland, M., Genc, S., Tax, C. M. W., Yeh, P.-H., Srikanchana, R., Mcknight, C. D., Yang, J. Y.-M., Chen, J., Kelly, C. E., Yeh, C.-H., Cochereau, J., Maller, J. J., Welton, T., Almairac, F., Seunarine, K. K., Clark, C. A., Zhang, F., Makris, N., Golby, A., Rathi, Y., O'Donnell, L. J., Xia, Y., Aydogan, D. B., Shi, Y., Fernandes, F. G., Raemaekers, M., Warrington, S., Michielse, S., Ramírez-Manzanares, A., Concha, L., Aranda, R., Meraz, M. R., Lerma-Usabiaga, G., Roitman, L., Fekonja, L. S., Calarco, N., Joseph, M., Nakua, H., Voineskos, A. N., Karan, P., Grenier, G., Legarreta, J. H., Adluru, N., Nair, V. A., Prabhakaran, V., Alexander, A. L., Kamagata, K., Saito, Y., Uchida, W., Andica, C., Abe, M., Bayrak, R. G., Wheeler-Kingshott, C. A. M. G., D'Angelo, E., Palesi, F., Savini, G., Rolandi, N., Guevara, P., Houenou, J., López-López, N., Mangin, J.-F., Poupon, C., Román, C., Vázquez, A., Maffei, C., Arantes, M., Andrade, J. P., Silva, S. M., Calhoun, V. D., Caverzasi, E., Sacco, S., Lauricella, M., Pestilli, F., Bullock, D., Zhan, Y., Brignoni-Perez, E., Lebel, C., Reynolds, J. E., Nestrasil, I., Labounek, R., Lenglet, C., Paulson, A., Aulicka, S., Heilbronner, S. R., Heuer, K., Chandio, B. Q., Guaje, J., Tang, W., Garyfallidis, E., Raja, R., Anderson, A. W., Landman, B. A., & Descoteaux, M.
Affiliations: Vanderbilt University Medical Center (US)
Université de Sherbrooke (CA)
Centre National de la Recherche Scientifique (FR)
Vanderbilt University (US)
University of Pittsburgh (US)
Centre d'Imagerie BioMedicale (CH)
École Polytechnique Fédérale de Lausanne (CH)
Technical University of Denmark (DK)
University of Verona (IT)
University of Basel (CH)
Karolinska Institutet (SE)
National Hospital for Neurology and Neurosurgery (GB)
University of Naples Federico II (IT)
University of Malta (MT)
Brighton and Sussex Medical School (GB)
University College London (GB)
Epilepsy Society (GB)
Universidad Complutense de Madrid (ES)
Universidad Rey Juan Carlos (ES)
The University of Sydney (AU)
University of Southern California (US)
Murdoch Children's Research Institute (AU)
University of Pennsylvania (US)
KU Leuven (BE)
University Medical Center Utrecht (NL)
Manchester Academic Health Science Centre (GB)
Cardiff University (GB)
Walter Reed National Military Medical Center (US)
Royal Children's Hospital (AU)
National Neuroscience Institute (SG)
Université Côte d'Azur (FR)
Brigham and Women's Hospital (US)
University of Nottingham (GB)
Maastricht University (NL)
Mathematics Research Center (MX)
Universidad Nacional Autónoma de México (MX)
Centro de Investigación Científica y de Educación Superior de Ensenada (MX)
Stanford University (US)
Charité – Universitätsmedizin Berlin (DE)
Centre for Addiction and Mental Health (CA)
University of Wisconsin–Madison (US)
University of Pavia (IT)
Fondazione Istituto Neurologico Nazionale Casimiro Mondino (IT)
University of Concepción (CL)
Harvard University (US)
Universidade do Porto (PT)
Georgia Institute of Technology (US)
University of California, San Francisco (US)
The University of Texas at Austin (US)
Chinese Academy of Sciences (CN)
University of Calgary (CA)
University of Minnesota (US)
Inserm (FR)
Indiana University Bloomington (US)
University of Arkansas for Medical Sciences (US)
Corresponding author: Schilling, Kurt G.
ORCID: Schilling, Kurt G.
Rheault, François
Petit, Laurent
Hansen, Colin B.
Nath, Vishwesh
Yeh, Fang-Cheng
Girard, Gabriel
Yu, Thomas
Pizzolato, Marco
Schiavi, Simona
Canales-Rodríguez, Erick J.
Daducci, Alessandro
Granziera, Cristina
Thiran, Jean-Philippe
Mancini, Laura
Wastling, Stephen
Cocozza, Sirio
Petracca, Maria
Pontillo, Giuseppe
Mancini, Matteo
Vos, Sjoerd B.
Vakharia, Vejay N.
Duncan, John S.
Melero, Helena
Peña-Melián, Ángel
Calamante, Fernando
Attyé, Arnaud
Cabeen, Ryan P.
Toga, Arthur W.
Vijayakumari, Anupa Ambili
Parker, Drew
Verma, Ragini
Radwan, Ahmed
Sunaert, Stefan
Emsell, Louise
Leemans, Alexander
Bajada, Claude J.
Haroon, Hamied
Chamberland, Maxime
Genc, Sila
Tax, Chantal M.W.
Yeh, Ping-Hong
Srikanchana, Rujirutana
Mcknight, Colin D.
Yang, Joseph Yuan-Mou
Chen, Jian
Kelly, Claire E.
Yeh, Chun-Hung
Maller, Jerome J.
Welton, Thomas
Almairac, Fabien
Seunarine, Kiran K
Clark, Chris A.
Zhang, Fan
Makris, Nikos
Golby, Alexandra
Xia, Yihao
Aydogan, Dogu Baran
Shi, Yonggang
Fernandes, Francisco Guerreiro
Raemaekers, Mathijs
Warrington, Shaun
Michielse, Stijn
Ramírez-Manzanares, Alonso
Concha, Luis
Aranda, Ramón
Fekonja, Lucius S.
Calarco, Navona
Joseph, Michael
Nakua, Hajer
Voineskos, Aristotle N.
Karan, Philippe
Legarreta, Jon Haitz
Adluru, Nagesh
Nair, Veena A.
Prabhakaran, Vivek
Alexander, Andrew L.
Kamagata, Koji
Saito, Yuya
Uchida, Wataru
Andica, Christina
Abe, Masahiro
Bayrak, Roza G.
D'Angelo, Egidio
Palesi, Fulvia
Savini, Giovanni
Rolandi, Nicolò
Guevara, Pamela
Houenou, Josselin
López-López, Narciso
Mangin, Jean-François
Poupon, Cyril
Román, Claudio
Maffei, Chiara
Arantes, Mavilde
Andrade, José Paulo
Silva, Susana Maria
Calhoun, Vince D.
Caverzasi, Eduardo
Sacco, Simone
Pestilli, Franco
Bullock, Daniel
Zhan, Yang
Lebel, Catherine
Reynolds, Jess E
Labounek, René
Lenglet, Christophe
Paulson, Amy
Heuer, Katja
Chandio, Bramsh Qamar
Guaje, Javier
Tang, Wei
Garyfallidis, Eleftherios
Raja, Rajikha
Anderson, Adam W.
Landman, Bennett A.
Descoteaux, Maxime
Venue: NeuroImage
Publisher: Elsevier BV
Published: 2021-11
Volume: 243
Pages: 118502
ISSN: 1053-8119 (ISSN-L)
DOI: 10.1016/j.neuroimage.2021.118502
PMC: PMC8855321
OpenAlex: W3091774503
Cited by: 182
References: 101
Citations by year: 2026: 24 · 2025: 31 · 2024: 38 · 2023: 27 · 2022: 45 · 2021: 15
FWCI: 16.51
Type: journal article
Language: en
Open access: gold
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Funders: National Science Foundation (1916518, T32EB001628, 1636893, 1912270, P30 NS076408, P41 EB027061, P41EB015898, 785907, UL1 RR024975-01, 1734853, MH103213)
Vanderbilt University (UL1 RR024975-01, UL1 RR024975, VR3029, ViSE/VICTR VR3029)
Vanderbilt Institute for Clinical and Translational Research (VR3029, RR024975, UL1 RR024975-01, UL1 RR024975)
Waisman Center (HD090256, U54 HD090256)
Université de Sherbrooke
Wellcome Trust (17331, 215944, 213722, MR/N013913/1, 215944/Z/19/Z, 213722/Z/18/Z)
Children’s Hospital of Wisconsin Research Institute
Children's Hospital Foundation
Compute Canada
Murdoch Children's Research Institute
Royal Children's Hospital Foundation (RCH-1000)
National Institute for Health and Care Research (NF-SI-0515-10000)
European Commission (HORIZON2020, 785907, 215944, 754462, HBP SGA2, 945539)
University of Nottingham
Deutsche Forschungsgemeinschaft (785907, EXC 2025, 945539)
Agence Nationale de la Recherche (ANR-19-CE45-0022, 785907, 945539)
Schweizerischer Nationalfonds zur Förderung der Wissenschaftlichen Forschung (213722, PZ00P2, 185814, 215944)
University of Melbourne
Consejo Nacional de Ciencia y Tecnología (FB0008)
Nederlandse Organisatie voor Wetenschappelijk Onderzoek (17331, U54 HD090256, 785907, 215944/Z/19/Z)
Ministry of Science and Technology, Taiwan (MOST 109, 001-MY3, MOST109-2222-E182-001-MY3)
State Government of Victoria (RCH 1000)
Agencia Nacional de Investigación y Desarrollo (1190701, FB0008, FONDECYT 1190701)
National Institutes of Health (1734853, 785907, 945539, VR3029, ViSE/VICTR VR3029, HD090256, RR024975, EB027061, NS076408)
Intellectual and Developmental Disabilities Research Center
Natural Sciences and Engineering Research Council of Canada (EB027061, P41EB015902)
Medical Research Council (1957092, MR/N013913/1, 785907, 945539)
Australian Research Council (DP170101815)
National Health and Medical Research Council (1117724, 1091593)
Japan Society for the Promotion of Science (20F20113)
Fundação para a Ciência e a Tecnologia (UID/IC/4255/2013)
National Institute on Aging (P30AG066530)
National Institute of Mental Health (K24MH116366, R01MH111917, 945539, MH103213, R01MH119222, NIMH T32, 1734853, T32MH103213)
National Institute of Neurological Disorders and Stroke (P30NS076408)
National Institute of Biomedical Imaging and Bioengineering (1734853, P41EB015902, VR3029, R01EB029272, R01EB017230, EB027061, P41EB015922, P41EB015898, T32EB001628, P41EB028741, P41EB027061)
National Institute of Child Health and Human Development (HD090256)
National Center for Research Resources (215944/Z/19/Z, Grant UL1 RR024975-01, RR024975, P41RR013218, UL1RR024975, RR024975‐01, 17331)
Eunice Kennedy Shriver National Institute of Child Health and Human Development (U54HD090256, P50HD103537)
Topics: Health Sciences › Medicine › Radiology, Nuclear Medicine and Imaging › Advanced Neuroimaging Techniques and Applications
Life Sciences › Neuroscience › Cognitive Neuroscience › Functional Brain Connectivity Studies
Physical Sciences › Computer Science › Computer Vision and Pattern Recognition › Medical Image Segmentation Techniques
Keywords: tractography, virtual dissection, diffusion MRI, reproducibility, human brain white matter
MeSH terms: Algorithms, Dissection, Humans, Image Processing, Computer-Assisted, Neural Pathways, Diffusion Tensor Imaging, White Matter

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

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