The challenge of mapping the human connectome based on diffusion tractography

Klaus H. Maier-Hein; Peter F. Neher; Jean-Christophe Houde; Marc Alexandre Côté; 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 González; Michael Paquette; Samuel St-Jean; Gabriel Girard; François Rheault; Jasmeen Sidhu; Chantal M.W. Tax; Fenghua Guo; Hamed Y. Mesri; Szabolcs Dávid; Martijn Froeling; Anneriet M. Heemskerk; Alexander Leemans; Arnaud Boré; 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 Auría; 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 B. 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 Côté, 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 WestinSamuel Deslauriers-Gauthier, J. Omar Ocegueda González, Michael Paquette, Samuel St-Jean, Gabriel Girard, François Rheault, Jasmeen Sidhu, Chantal M.W. Tax, Fenghua Guo, Hamed Y. Mesri, Szabolcs Dávid, Martijn Froeling, Anneriet M. Heemskerk, Alexander Leemans, Arnaud Boré, 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 Auría, 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 B. Dyrby, Tim Holland-Letz, Claus C. Hilgetag, Bram Stieltjes, Maxime Descoteaux

Research output: Contribution to journal › Article › Academic › peer-review

910 Citations (Scopus)

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
DOIs	https://doi.org/10.1038/s41467-017-01285-x
Publication status	Published - 1 Dec 2017
Externally published	Yes

Bibliographical note

Funding Information:
K.H.M.-H. was supported by the German Research Foundation (DFG), grants MA 6340/10-1, MA 6340/12-1. M.D. was supported by the NSERC Discovery Grant program as well as the institutional Université de Sherbrooke Research Chair in Neuroinformatics. C.M.W.T. was supported by a grant (No. 612.001.104) from the Physical Sciences division of the Netherlands Organization for Scientific Research (NWO). The research of H.Y.M., S.D., S.S., A.M.H., and A.L. was supported by VIDI grant 639.072.411 from NWO. The research of F.G. was funded by the Chinese Scholarship Council (CSC). M.Ch. was supported by the Alexander Graham Bell Canada Graduate Scholarships-Doctoral Program (CGS-D3) from the Natural Sciences and Engineering Research Council of Canada (NSERC). M.C. was supported by the Investigator Award No. 103759/ Z/14/Z from the Wellcome Trust. C.C.H. was supported by DFG SFB grants 936/A1, Z3 and TRR 169/A2. The research of J.-P.T., D.R., M.B., A.A., A.L., and A.D. was supported by the Center for Biomedical Imaging (CIBM) of the Geneva-Lausanne Universities and the EPFL, as well as the foundations Leenaards and Louis-Jeantet, and by the Swiss National Science Foundation grants 205321_144529 and 31003A_157063. W.E.R. was supported by CA90246 from National Cancer Institute. The research of Y.F., C.G., Y.W., J.M., H.R., Q.L., and C.-F.W. was supported by grant 61379020 from National Nature Science Foundation of China. C.-F.W. was supported by NIH grants P41EB015902 and P41EB015898.

Publisher Copyright:
© 2017 The Author(s).

Funding

K.H.M.-H. was supported by the German Research Foundation (DFG), grants MA 6340/10-1, MA 6340/12-1. M.D. was supported by the NSERC Discovery Grant program as well as the institutional Université de Sherbrooke Research Chair in Neuroinformatics. C.M.W.T. was supported by a grant (No. 612.001.104) from the Physical Sciences division of the Netherlands Organization for Scientific Research (NWO). The research of H.Y.M., S.D., S.S., A.M.H., and A.L. was supported by VIDI grant 639.072.411 from NWO. The research of F.G. was funded by the Chinese Scholarship Council (CSC). M.Ch. was supported by the Alexander Graham Bell Canada Graduate Scholarships-Doctoral Program (CGS-D3) from the Natural Sciences and Engineering Research Council of Canada (NSERC). M.C. was supported by the Investigator Award No. 103759/ Z/14/Z from the Wellcome Trust. C.C.H. was supported by DFG SFB grants 936/A1, Z3 and TRR 169/A2. The research of J.-P.T., D.R., M.B., A.A., A.L., and A.D. was supported by the Center for Biomedical Imaging (CIBM) of the Geneva-Lausanne Universities and the EPFL, as well as the foundations Leenaards and Louis-Jeantet, and by the Swiss National Science Foundation grants 205321_144529 and 31003A_157063. W.E.R. was supported by CA90246 from National Cancer Institute. The research of Y.F., C.G., Y.W., J.M., H.R., Q.L., and C.-F.W. was supported by grant 61379020 from National Nature Science Foundation of China. C.-F.W. was supported by NIH grants P41EB015902 and P41EB015898.

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10.1038/s41467-017-01285-x

Cite this

Maier-Hein, K. H., Neher, P. F., Houde, J.-C., Côté, 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

@article{75e3b0cbe8354312b5e6296bf35c6083,

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 C{\^o}t{\'e}, {Marc Alexandre} and Eleftherios Garyfallidis and Jidan Zhong and Maxime Chamberland and Yeh, {Fang Cheng} and Lin, {Ying Chia} 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 Westin, {Carl Fredrik} and Samuel Deslauriers-Gauthier and Gonz{\'a}lez, {J. Omar Ocegueda} and Michael Paquette and Samuel St-Jean and Gabriel Girard and Fran{\c c}ois Rheault and Jasmeen Sidhu and Tax, {Chantal M.W.} and Fenghua Guo and Mesri, {Hamed Y.} and Szabolcs D{\'a}vid and Martijn Froeling and Heemskerk, {Anneriet M.} and Alexander Leemans and Arnaud Bor{\'e} 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 Aur{\'i}a and Oscar Esteban and Alia Lemkaddem and Thiran, {Jean Philippe} 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 B.} and Tim Holland-Letz and Hilgetag, {Claus C.} and Bram Stieltjes and Maxime Descoteaux",

note = "Funding Information: K.H.M.-H. was supported by the German Research Foundation (DFG), grants MA 6340/10-1, MA 6340/12-1. M.D. was supported by the NSERC Discovery Grant program as well as the institutional Universit{\'e} de Sherbrooke Research Chair in Neuroinformatics. C.M.W.T. was supported by a grant (No. 612.001.104) from the Physical Sciences division of the Netherlands Organization for Scientific Research (NWO). The research of H.Y.M., S.D., S.S., A.M.H., and A.L. was supported by VIDI grant 639.072.411 from NWO. The research of F.G. was funded by the Chinese Scholarship Council (CSC). M.Ch. was supported by the Alexander Graham Bell Canada Graduate Scholarships-Doctoral Program (CGS-D3) from the Natural Sciences and Engineering Research Council of Canada (NSERC). M.C. was supported by the Investigator Award No. 103759/ Z/14/Z from the Wellcome Trust. C.C.H. was supported by DFG SFB grants 936/A1, Z3 and TRR 169/A2. The research of J.-P.T., D.R., M.B., A.A., A.L., and A.D. was supported by the Center for Biomedical Imaging (CIBM) of the Geneva-Lausanne Universities and the EPFL, as well as the foundations Leenaards and Louis-Jeantet, and by the Swiss National Science Foundation grants 205321_144529 and 31003A_157063. W.E.R. was supported by CA90246 from National Cancer Institute. The research of Y.F., C.G., Y.W., J.M., H.R., Q.L., and C.-F.W. was supported by grant 61379020 from National Nature Science Foundation of China. C.-F.W. was supported by NIH grants P41EB015902 and P41EB015898. Publisher Copyright: {\textcopyright} 2017 The Author(s).",

year = "2017",

month = dec,

day = "1",

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

language = "English",

volume = "8",

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issn = "2041-1723",

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Maier-Hein, KH, Neher, PF, Houde, J-C, Côté, MA, Garyfallidis, E, Zhong, J, Chamberland, M, Yeh, FC, Lin, YC, Ji, Q, Reddick, WE, Glass, JO, Chen, DQ, Feng, Y, Gao, C, Wu, Y, Ma, J, Renjie, H, Li, Q, Westin, CF, Deslauriers-Gauthier, S, González, JOO, Paquette, M, St-Jean, S, Girard, G, Rheault, F, Sidhu, J, Tax, CMW, Guo, F, Mesri, HY, Dávid, S, Froeling, M, Heemskerk, AM, Leemans, A, Boré, 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, Auría, A, Esteban, O, Lemkaddem, A, Thiran, JP, 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 - Côté, 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 - González, J. Omar Ocegueda

AU - Paquette, Michael

AU - St-Jean, Samuel

AU - Girard, Gabriel

AU - Rheault, François

AU - Sidhu, Jasmeen

AU - Tax, Chantal M.W.

AU - Guo, Fenghua

AU - Mesri, Hamed Y.

AU - Dávid, Szabolcs

AU - Froeling, Martijn

AU - Heemskerk, Anneriet M.

AU - Leemans, Alexander

AU - Boré, 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 - Auría, 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 B.

AU - Holland-Letz, Tim

AU - Hilgetag, Claus C.

AU - Stieltjes, Bram

AU - Descoteaux, Maxime

N1 - Funding Information: K.H.M.-H. was supported by the German Research Foundation (DFG), grants MA 6340/10-1, MA 6340/12-1. M.D. was supported by the NSERC Discovery Grant program as well as the institutional Université de Sherbrooke Research Chair in Neuroinformatics. C.M.W.T. was supported by a grant (No. 612.001.104) from the Physical Sciences division of the Netherlands Organization for Scientific Research (NWO). The research of H.Y.M., S.D., S.S., A.M.H., and A.L. was supported by VIDI grant 639.072.411 from NWO. The research of F.G. was funded by the Chinese Scholarship Council (CSC). M.Ch. was supported by the Alexander Graham Bell Canada Graduate Scholarships-Doctoral Program (CGS-D3) from the Natural Sciences and Engineering Research Council of Canada (NSERC). M.C. was supported by the Investigator Award No. 103759/ Z/14/Z from the Wellcome Trust. C.C.H. was supported by DFG SFB grants 936/A1, Z3 and TRR 169/A2. The research of J.-P.T., D.R., M.B., A.A., A.L., and A.D. was supported by the Center for Biomedical Imaging (CIBM) of the Geneva-Lausanne Universities and the EPFL, as well as the foundations Leenaards and Louis-Jeantet, and by the Swiss National Science Foundation grants 205321_144529 and 31003A_157063. W.E.R. was supported by CA90246 from National Cancer Institute. The research of Y.F., C.G., Y.W., J.M., H.R., Q.L., and C.-F.W. was supported by grant 61379020 from National Nature Science Foundation of China. C.-F.W. was supported by NIH grants P41EB015902 and P41EB015898. Publisher Copyright: © 2017 The Author(s).

PY - 2017/12/1

Y1 - 2017/12/1

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.

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U2 - 10.1038/s41467-017-01285-x

DO - 10.1038/s41467-017-01285-x

M3 - Article

C2 - 29116093

AN - SCOPUS:85033392554

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

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