The challenge of mapping the human connectome based on diffusion tractography

Klaus H. Maier-Hein; Peter F. Neher; Jean-Christophe Houde; Marc-Alexandre Cote; Eleftherios Garyfallidis; Jidan Zhong; Maxime Chamberland; Fang-Cheng Yeh; Ying-Chia Lin; Qing Ji; Wilburn E. Reddick; John O. Glass; David Qixiang Chen; Yuanjing Feng; Chengfeng Gao; Ye Wu; Jieyan Ma; H. Renjie; Qiang Li; Carl-Fredrik Westin; Samuel Deslauriers-Gauthier; J. Omar Ocegueda Gonzalez; Michael Paquette; Samuel St-Jean; Gabriel Girard; Francois Rheault; Jasmeen Sidhu; Chantal M. W. Tax; Fenghua Guo; Hamed Y. Mesri; Szabolcs David; Martijn Froeling; Anneriet M. Heemskerk; Alexander Leemans; Arnaud Bore; Basile Pinsard; Christophe Bedetti; Matthieu Desrosiers; Simona Brambati; Julien Doyon; Alessia Sarica; Roberta Vasta; Antonio Cerasa; Aldo Quattrone; Jason Yeatman; Ali R. Khan; Wes Hodges; Simon Alexander; David Romascano; Muhamed Barakovic; Anna Auria; Oscar Esteban; Alia Lemkaddem; Jean-Philippe Thiran; H. Ertan Cetingul; Benjamin L. Odry; Boris Mailhe; Mariappan S. Nadar; Fabrizio Pizzagalli; Gautam Prasad; Julio E. Villalon-Reina; Justin Galvis; Paul M. Thompson; Francisco De Santiago Requejo; Pedro Luque Laguna; Luis Miguel Lacerda; Rachel Barrett; Flavio Dell'Acqua; Marco Catani; Laurent Petit; Emmanuel Caruyer; Alessandro Daducci; Tim Bjørn Dyrby; Tim Holland-Letz; Claus C. Hilgetag; Bram Stieltjes; Maxime Descoteaux

doi:10.1038/s41467-017-01285-x

The challenge of mapping the human connectome based on diffusion tractography

Klaus H. Maier-Hein
, Peter F. Neher
, Jean-Christophe Houde
, Marc-Alexandre Cote
, Eleftherios Garyfallidis
, Jidan Zhong
, Maxime Chamberland
, Fang-Cheng Yeh
, Ying-Chia Lin
, Qing Ji
, Wilburn E. Reddick
, John O. Glass
, David Qixiang Chen
, Yuanjing Feng
, Chengfeng Gao
, Ye Wu
, Jieyan Ma
, H. Renjie
, Qiang Li
, Carl-Fredrik Westin

Samuel Deslauriers-Gauthier, J. Omar Ocegueda Gonzalez, Michael Paquette, Samuel St-Jean, Gabriel Girard, Francois Rheault, Jasmeen Sidhu, Chantal M. W. Tax, Fenghua Guo, Hamed Y. Mesri, Szabolcs David, Martijn Froeling, Anneriet M. Heemskerk, Alexander Leemans, Arnaud Bore, Basile Pinsard, Christophe Bedetti, Matthieu Desrosiers, Simona Brambati, Julien Doyon, Alessia Sarica, Roberta Vasta, Antonio Cerasa, Aldo Quattrone, Jason Yeatman, Ali R. Khan, Wes Hodges, Simon Alexander, David Romascano, Muhamed Barakovic, Anna Auria, Oscar Esteban, Alia Lemkaddem, Jean-Philippe Thiran, H. Ertan Cetingul, Benjamin L. Odry, Boris Mailhe, Mariappan S. Nadar, Fabrizio Pizzagalli, Gautam Prasad, Julio E. Villalon-Reina, Justin Galvis, Paul M. Thompson, Francisco De Santiago Requejo, Pedro Luque Laguna, Luis Miguel Lacerda, Rachel Barrett, Flavio Dell'Acqua, Marco Catani, Laurent Petit, Emmanuel Caruyer, Alessandro Daducci, Tim Bjørn Dyrby, Tim Holland-Letz, Claus C. Hilgetag, Bram Stieltjes, Maxime Descoteaux

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Abstract

Tractography based on non-invasive diffusion imaging is central to the study of human brain connectivity. To date, the approach has not been systematically validated in ground truth studies. Based on a simulated human brain data set with ground truth tracts, we organized an open international tractography challenge, which resulted in 96 distinct submissions from 20 research groups. Here, we report the encouraging finding that most state-of-the-art algorithms produce tractograms containing 90% of the ground truth bundles (to at least some extent). However, the same tractograms contain many more invalid than valid bundles, and half of these invalid bundles occur systematically across research groups. Taken together, our results demonstrate and confirm fundamental ambiguities inherent in tract reconstruction based on orientation information alone, which need to be considered when interpreting tractography and connectivity results. Our approach provides a novel framework for estimating reliability of tractography and encourages innovation to address its current limitations.

Original language	English
Article number	1349
Journal	Nature Communications
Volume	8
Issue number	1
Number of pages	13
ISSN	2041-1723
DOIs	https://doi.org/10.1038/s41467-017-01285-x
Publication status	Published - 2017

Bibliographical note

© 2017 The Authors. Open Access: This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons license, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons license and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this license, visit http://creativecommons.org/licenses/by/4.0/.

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Maier-Hein, K. H., Neher, P. F., Houde, J.-C., Cote, M.-A., Garyfallidis, E., Zhong, J., Chamberland, M., Yeh, F.-C., Lin, Y.-C., Ji, Q., Reddick, W. E., Glass, J. O., Chen, D. Q., Feng, Y., Gao, C., Wu, Y., Ma, J., Renjie, H., Li, Q., ... Descoteaux, M. (2017). The challenge of mapping the human connectome based on diffusion tractography. Nature Communications, 8(1), Article 1349. https://doi.org/10.1038/s41467-017-01285-x

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title = "The challenge of mapping the human connectome based on diffusion tractography",

abstract = "Tractography based on non-invasive diffusion imaging is central to the study of human brain connectivity. To date, the approach has not been systematically validated in ground truth studies. Based on a simulated human brain data set with ground truth tracts, we organized an open international tractography challenge, which resulted in 96 distinct submissions from 20 research groups. Here, we report the encouraging finding that most state-of-the-art algorithms produce tractograms containing 90\% of the ground truth bundles (to at least some extent). However, the same tractograms contain many more invalid than valid bundles, and half of these invalid bundles occur systematically across research groups. Taken together, our results demonstrate and confirm fundamental ambiguities inherent in tract reconstruction based on orientation information alone, which need to be considered when interpreting tractography and connectivity results. Our approach provides a novel framework for estimating reliability of tractography and encourages innovation to address its current limitations.",

author = "Maier-Hein, \{Klaus H.\} and Neher, \{Peter F.\} and Jean-Christophe Houde and Marc-Alexandre Cote and Eleftherios Garyfallidis and Jidan Zhong and Maxime Chamberland and Fang-Cheng Yeh and Ying-Chia Lin and Qing Ji and Reddick, \{Wilburn E.\} and Glass, \{John O.\} and Chen, \{David Qixiang\} and Yuanjing Feng and Chengfeng Gao and Ye Wu and Jieyan Ma and H. Renjie and Qiang Li and Carl-Fredrik Westin and Samuel Deslauriers-Gauthier and \{Ocegueda Gonzalez\}, \{J. Omar\} and Michael Paquette and Samuel St-Jean and Gabriel Girard and Francois Rheault and Jasmeen Sidhu and Tax, \{Chantal M. W.\} and Fenghua Guo and Mesri, \{Hamed Y.\} and Szabolcs David and Martijn Froeling and Heemskerk, \{Anneriet M.\} and Alexander Leemans and Arnaud Bore and Basile Pinsard and Christophe Bedetti and Matthieu Desrosiers and Simona Brambati and Julien Doyon and Alessia Sarica and Roberta Vasta and Antonio Cerasa and Aldo Quattrone and Jason Yeatman and Khan, \{Ali R.\} and Wes Hodges and Simon Alexander and David Romascano and Muhamed Barakovic and Anna Auria and Oscar Esteban and Alia Lemkaddem and Jean-Philippe Thiran and Cetingul, \{H. Ertan\} and Odry, \{Benjamin L.\} and Boris Mailhe and Nadar, \{Mariappan S.\} and Fabrizio Pizzagalli and Gautam Prasad and Villalon-Reina, \{Julio E.\} and Justin Galvis and Thompson, \{Paul M.\} and Requejo, \{Francisco De Santiago\} and Laguna, \{Pedro Luque\} and Lacerda, \{Luis Miguel\} and Rachel Barrett and Flavio Dell'Acqua and Marco Catani and Laurent Petit and Emmanuel Caruyer and Alessandro Daducci and Dyrby, \{Tim Bj{\o}rn\} and Tim Holland-Letz and Hilgetag, \{Claus C.\} and Bram Stieltjes and Maxime Descoteaux",

note = "{\textcopyright} 2017 The Authors. Open Access: This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The images or other third party material in this article are included in the article{\textquoteright}s Creative Commons license, unless indicated otherwise in a credit line to the material. If material is not included in the article{\textquoteright}s Creative Commons license and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this license, visit http://creativecommons.org/licenses/by/4.0/.",

year = "2017",

doi = "10.1038/s41467-017-01285-x",

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journal = "Nature Communications",

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Maier-Hein, KH, Neher, PF, Houde, J-C, Cote, M-A, Garyfallidis, E, Zhong, J, Chamberland, M, Yeh, F-C, Lin, Y-C, Ji, Q, Reddick, WE, Glass, JO, Chen, DQ, Feng, Y, Gao, C, Wu, Y, Ma, J, Renjie, H, Li, Q, Westin, C-F, Deslauriers-Gauthier, S, Ocegueda Gonzalez, JO, Paquette, M, St-Jean, S, Girard, G, Rheault, F, Sidhu, J, Tax, CMW, Guo, F, Mesri, HY, David, S, Froeling, M, Heemskerk, AM, Leemans, A, Bore, A, Pinsard, B, Bedetti, C, Desrosiers, M, Brambati, S, Doyon, J, Sarica, A, Vasta, R, Cerasa, A, Quattrone, A, Yeatman, J, Khan, AR, Hodges, W, Alexander, S, Romascano, D, Barakovic, M, Auria, A, Esteban, O, Lemkaddem, A, Thiran, J-P, Cetingul, HE, Odry, BL, Mailhe, B, Nadar, MS, Pizzagalli, F, Prasad, G, Villalon-Reina, JE, Galvis, J, Thompson, PM, Requejo, FDS, Laguna, PL, Lacerda, LM, Barrett, R, Dell'Acqua, F, Catani, M, Petit, L, Caruyer, E, Daducci, A, Dyrby, TB, Holland-Letz, T, Hilgetag, CC, Stieltjes, B & Descoteaux, M 2017, 'The challenge of mapping the human connectome based on diffusion tractography', Nature Communications, vol. 8, no. 1, 1349. https://doi.org/10.1038/s41467-017-01285-x

TY - JOUR

T1 - The challenge of mapping the human connectome based on diffusion tractography

AU - Maier-Hein, Klaus H.

AU - Neher, Peter F.

AU - Houde, Jean-Christophe

AU - Cote, Marc-Alexandre

AU - Garyfallidis, Eleftherios

AU - Zhong, Jidan

AU - Chamberland, Maxime

AU - Yeh, Fang-Cheng

AU - Lin, Ying-Chia

AU - Ji, Qing

AU - Reddick, Wilburn E.

AU - Glass, John O.

AU - Chen, David Qixiang

AU - Feng, Yuanjing

AU - Gao, Chengfeng

AU - Wu, Ye

AU - Ma, Jieyan

AU - Renjie, H.

AU - Li, Qiang

AU - Westin, Carl-Fredrik

AU - Deslauriers-Gauthier, Samuel

AU - Ocegueda Gonzalez, J. Omar

AU - Paquette, Michael

AU - St-Jean, Samuel

AU - Girard, Gabriel

AU - Rheault, Francois

AU - Sidhu, Jasmeen

AU - Tax, Chantal M. W.

AU - Guo, Fenghua

AU - Mesri, Hamed Y.

AU - David, Szabolcs

AU - Froeling, Martijn

AU - Heemskerk, Anneriet M.

AU - Leemans, Alexander

AU - Bore, Arnaud

AU - Pinsard, Basile

AU - Bedetti, Christophe

AU - Desrosiers, Matthieu

AU - Brambati, Simona

AU - Doyon, Julien

AU - Sarica, Alessia

AU - Vasta, Roberta

AU - Cerasa, Antonio

AU - Quattrone, Aldo

AU - Yeatman, Jason

AU - Khan, Ali R.

AU - Hodges, Wes

AU - Alexander, Simon

AU - Romascano, David

AU - Barakovic, Muhamed

AU - Auria, Anna

AU - Esteban, Oscar

AU - Lemkaddem, Alia

AU - Thiran, Jean-Philippe

AU - Cetingul, H. Ertan

AU - Odry, Benjamin L.

AU - Mailhe, Boris

AU - Nadar, Mariappan S.

AU - Pizzagalli, Fabrizio

AU - Prasad, Gautam

AU - Villalon-Reina, Julio E.

AU - Galvis, Justin

AU - Thompson, Paul M.

AU - Requejo, Francisco De Santiago

AU - Laguna, Pedro Luque

AU - Lacerda, Luis Miguel

AU - Barrett, Rachel

AU - Dell'Acqua, Flavio

AU - Catani, Marco

AU - Petit, Laurent

AU - Caruyer, Emmanuel

AU - Daducci, Alessandro

AU - Dyrby, Tim Bjørn

AU - Holland-Letz, Tim

AU - Hilgetag, Claus C.

AU - Stieltjes, Bram

AU - Descoteaux, Maxime

N1 - © 2017 The Authors. Open Access: This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons license, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons license and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this license, visit http://creativecommons.org/licenses/by/4.0/.

PY - 2017

Y1 - 2017

N2 - Tractography based on non-invasive diffusion imaging is central to the study of human brain connectivity. To date, the approach has not been systematically validated in ground truth studies. Based on a simulated human brain data set with ground truth tracts, we organized an open international tractography challenge, which resulted in 96 distinct submissions from 20 research groups. Here, we report the encouraging finding that most state-of-the-art algorithms produce tractograms containing 90% of the ground truth bundles (to at least some extent). However, the same tractograms contain many more invalid than valid bundles, and half of these invalid bundles occur systematically across research groups. Taken together, our results demonstrate and confirm fundamental ambiguities inherent in tract reconstruction based on orientation information alone, which need to be considered when interpreting tractography and connectivity results. Our approach provides a novel framework for estimating reliability of tractography and encourages innovation to address its current limitations.

AB - Tractography based on non-invasive diffusion imaging is central to the study of human brain connectivity. To date, the approach has not been systematically validated in ground truth studies. Based on a simulated human brain data set with ground truth tracts, we organized an open international tractography challenge, which resulted in 96 distinct submissions from 20 research groups. Here, we report the encouraging finding that most state-of-the-art algorithms produce tractograms containing 90% of the ground truth bundles (to at least some extent). However, the same tractograms contain many more invalid than valid bundles, and half of these invalid bundles occur systematically across research groups. Taken together, our results demonstrate and confirm fundamental ambiguities inherent in tract reconstruction based on orientation information alone, which need to be considered when interpreting tractography and connectivity results. Our approach provides a novel framework for estimating reliability of tractography and encourages innovation to address its current limitations.

U2 - 10.1038/s41467-017-01285-x

DO - 10.1038/s41467-017-01285-x

M3 - Journal article

C2 - 29116093

SN - 2041-1723

VL - 8

JO - Nature Communications

JF - Nature Communications

IS - 1

M1 - 1349

ER -

The challenge of mapping the human connectome based on diffusion tractography

Abstract

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