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

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 ManciniStephen 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

Research output: Contribution to journalArticlepeer-review

29 Scopus citations

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.

Original languageEnglish (US)
Article number118502
JournalNeuroImage
Volume243
Early online dateAug 22 2021
DOIs
StatePublished - Nov 2021

Bibliographical note

Funding Information:
This work was conducted in part using the resources of the Advanced Computing Center for Research and Education at Vanderbilt University, Nashville, TN. KS, BL, CH were supported by the National Institutes of Health under award numbers R01EB017230, and T32EB001628, and in part by ViSE/VICTR VR3029 and the National Center for Research Resources, Grant UL1 RR024975-01. This work was also possible thanks to the support of the Institutional Research Chair in NeuroInformatics of Université de Sherbrooke, NSERC and Compute Canada (MD, FR). MP received funding from the European Union's Horizon 2020 research and innovation programme under the Marie Skłodowska-Curie grant agreement No 754462. The Wisconsin group acknowledges the support from a core grant to the Waisman Center from the National Institute of Child Health and Human Development (IDDRC U54 HD090256). NSF OAC-1916518, NSF IIS-1912270, NSF IIS-1636893, NSF BCS-1734853, NIH NIBIB 1R01EB029272-01, and a Microsoft Faculty Fellowship to F.P. LF acknowledges the support of the Cluster of Excellence Matters of Activity. Image Space Material funded by the Deutsche Forschungsgemeinschaft (DFG, German Research Foundation) under Germany´s Excellence Strategy – EXC 2025. SW is supported by a Medical Research Council PhD Studentship UK [MR/N013913/1]. The Nottingham group's processing was performed using the University of Nottingham's Augusta HPC service and the Precision Imaging Beacon Cluster. JPA, MA and SMS acknowledges the support of FCT - Fundação para a Ciência e a Tecnologia within CINTESIS, R&D Unit (reference UID/IC/4255/2013). MM was funded by the Wellcome Trust through a Sir Henry Wellcome Postdoctoral Fellowship [213722/Z/18/Z]. EJC-R is supported by the Swiss National Science Foundation (SNSF, Ambizione grant PZ00P2 185814/1). CMWT is supported by a Sir Henry Wellcome Fellowship (215944/Z/19/Z) and a Veni grant from the Dutch Research Council (NWO) (17331). FC acknowledges the support of the National Health and Medical Research Council of Australia (APP1091593 and APP1117724) and the Australian Research Council (DP170101815). NSF OAC-1916518, NSF IIS-1912270, NSF IIS-1636893, NSF BCS-1734853, Microsoft Faculty Fellowship to F.P. D.B. was partially supported by NIH NIMH T32-MH103213 to William Hetrick (Indiana University). CL is partly supported by NIH grants P41 EB027061 and P30 NS076408 “Institutional Center Cores for Advanced Neuroimaging. JYMY received positional funding from the Royal Children's Hospital Foundation (RCH 1000). JYMY, JC, and CEK acknowledge the support of the Royal Children's Hospital Foundation, Murdoch Children's Research Institute, The University of Melbourne Department of Paediatrics, and the Victorian Government's Operational Infrastructure Support Program. C-HY is grateful to the Ministry of Science and Technology of Taiwan (MOST 109-2222-E-182-001-MY3) for the support. LC acknowledges support from CONACYT and UNAM. ARM acknowledges support from CONACYT. LJO, YR, and FZ were supported by NIH P41EB015902 and R01MH119222. AJG was supported by P41EB015898. NM was supported by R01MH119222, K24MH116366, and R01MH111917. This project has received funding from the European Union's Horizon 2020 Research and Innovation Programme under Grant Agreement No. 785907 & 945539 (HBP SGA2 & SGA3), and from the ANR IFOPASUBA- 19-CE45-0022-01. PG, CR, NL and AV were partially supported by ANID-Basal FB0008 and ANID-FONDECYT 1190701 grants. We would like to acknowledge John C Gore, Hiromasa Takemura, Anastasia Yendiki, and Riccardo Galbusera for their helplful suggestions regarding the analysis, figures, and discussions.

Funding Information:
This work was conducted in part using the resources of the Advanced Computing Center for Research and Education at Vanderbilt University, Nashville, TN. KS, BL, CH were supported by the National Institutes of Health under award numbers R01EB017230, and T32EB001628, and in part by ViSE/VICTR VR3029 and the National Center for Research Resources, Grant UL1 RR024975-01. This work was also possible thanks to the support of the Institutional Research Chair in NeuroInformatics of Universit? de Sherbrooke, NSERC and Compute Canada (MD, FR). MP received funding from the European Union's Horizon 2020 research and innovation programme under the Marie Sk?odowska-Curie grant agreement No 754462. The Wisconsin group acknowledges the support from a core grant to the Waisman Center from the National Institute of Child Health and Human Development (IDDRC U54 HD090256). NSF OAC-1916518, NSF IIS-1912270, NSF IIS-1636893, NSF BCS-1734853, NIH NIBIB 1R01EB029272-01, and a Microsoft Faculty Fellowship to F.P. LF acknowledges the support of the Cluster of Excellence Matters of Activity. Image Space Material funded by the Deutsche Forschungsgemeinschaft (DFG, German Research Foundation) under Germany?s Excellence Strategy ? EXC 2025. SW is supported by a Medical Research Council PhD Studentship UK [MR/N013913/1]. The Nottingham group's processing was performed using the University of Nottingham's Augusta HPC service and the Precision Imaging Beacon Cluster. JPA, MA and SMS acknowledges the support of FCT - Funda??o para a Ci?ncia e a Tecnologia within CINTESIS, R&D Unit (reference UID/IC/4255/2013). MM was funded by the Wellcome Trust through a Sir Henry Wellcome Postdoctoral Fellowship [213722/Z/18/Z]. EJC-R is supported by the Swiss National Science Foundation (SNSF, Ambizione grant PZ00P2 185814/1). CMWT is supported by a Sir Henry Wellcome Fellowship (215944/Z/19/Z) and a Veni grant from the Dutch Research Council (NWO) (17331). FC acknowledges the support of the National Health and Medical Research Council of Australia (APP1091593 and APP1117724) and the Australian Research Council (DP170101815). NSF OAC-1916518, NSF IIS-1912270, NSF IIS-1636893, NSF BCS-1734853, Microsoft Faculty Fellowship to F.P. D.B. was partially supported by NIH NIMH T32-MH103213 to William Hetrick (Indiana University). CL is partly supported by NIH grants P41 EB027061 and P30 NS076408 ?Institutional Center Cores for Advanced Neuroimaging. JYMY received positional funding from the Royal Children's Hospital Foundation (RCH 1000). JYMY, JC, and CEK acknowledge the support of the Royal Children's Hospital Foundation, Murdoch Children's Research Institute, The University of Melbourne Department of Paediatrics, and the Victorian Government's Operational Infrastructure Support Program. C-HY is grateful to the Ministry of Science and Technology of Taiwan (MOST 109-2222-E-182-001-MY3) for the support. LC acknowledges support from CONACYT and UNAM. ARM acknowledges support from CONACYT. LJO, YR, and FZ were supported by NIH P41EB015902 and R01MH119222. AJG was supported by P41EB015898. NM was supported by R01MH119222, K24MH116366, and R01MH111917. This project has received funding from the European Union's Horizon 2020 Research and Innovation Programme under Grant Agreement No. 785907 & 945539 (HBP SGA2 & SGA3), and from the ANR IFOPASUBA- 19-CE45-0022-01. PG, CR, NL and AV were partially supported by ANID-Basal FB0008 and ANID-FONDECYT 1190701 grants. We would like to acknowledge John C Gore, Hiromasa Takemura, Anastasia Yendiki, and Riccardo Galbusera for their helplful suggestions regarding the analysis, figures, and discussions.

Publisher Copyright:
© 2021

Keywords

  • Bundle segmentation
  • Dissection
  • Fiber pathways
  • Tractography
  • White matter

PubMed: MeSH publication types

  • Journal Article
  • Research Support, N.I.H., Extramural
  • Research Support, Non-U.S. Gov't
  • Research Support, U.S. Gov't, Non-P.H.S.

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