The challenge of mapping the human connectome based on diffusion tractography

Klaus H Maier‐Hein ,Simona Maria Brambati ,Carl‐Fredrik Westin ,J Omar Ocegueda González ,Marc-Alexandre Côté ,Ali R Khan ,Francisco De Santiago Requejo ,Jasmeen Sidhu ,Peter Neher ,Laurent Petit ,Alexander Leemans ,Muhamed Baraković ,Aldo Quattrone ,Anneriet M Heemskerk ,Benjamin L Odry ,Jidan Zhong ,Tim Holland‐Letz ,Jean‐Philippe Thiran ,Antonio Cerasa ,Szabolcs Dávid ,Luís Lacerda ,Fabrizio Pizzagalli ,Fang‐Cheng Yeh ,Qing Ji ,Jieyan Ma ,Jason D Yeatman ,Samuel Deslauriers-Gauthier ,Ying‐Chia Lin ,Chengfeng Gao ,Pedro Luque Laguna ,Julien Doyon ,Jean‐Christophe Houde ,Arnaud Boré ,Justin Galvis ,Alessia Sarica ,David Romascano ,Claus C Hilgetag ,Marco Catani ,Emmanuel Caruyer ,Shelton S Alexander ,Julio E Villalon‐Reina ,Roberta Vasta ,David Qixiang Chen ,Paul M Thompson ,Wes Hodges ,Alia Lemkaddem ,Gabriel Girard ,Yuanjing Feng ,Eleftherios Garyfallidis ,John O Glass ,Rachel Barrett ,Bram Stieltjes ,Boris Mailhé ,Gautam Prasad ,Chantal M W Tax ,Wilburn E Reddick ,Christophe Bedetti ,Samuel St-Jean ,Alessandro Daducci ,Hua Ren-Jie ,Matthieu Desrosiers ,Hamed Y Mesri ,Anna Auría ,Martijn Froeling ,Basile Pinsard ,Michael Paquette ,Qiang Li ,Maxime Chamberland ,Mariappan S Nadar ,Flavio Dell’acqua ,François Rheault ,Ye Wu ,Fenghua Guo ,Oscar Estéban ,Tim B Dyrby ,H Ertan Çetingül ,Maxime Descoteaux

doi:10.1038/s41467-017-01285-x

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.

Highlights

The principle of inferring connectivity from local orientation fields can lead to problems as soon as pathways overlap, cross, branch, and have complex geometries[7, 35, 36]
We defined our models based on the fiber bundle geometry of a high-quality Human Connectome Project (HCP) data set that was constructed from multiple whole-brain global tractography maps[39] (Fig. 1)
Bundles of medium difficulty were the corpus callosum (CC), inferior longitudinal fasciculus (ILF), superior longitudinal fasciculus (SLF), and uncinate fasciculus (UF) with an average of more than 50% volumetric recovery (50%

Summary

Introduction

The principle of inferring connectivity from local orientation fields can lead to problems as soon as pathways overlap, cross, branch, and have complex geometries[7, 35, 36]. We employed simulated DWI of a brain-like geometry as a novel reliability estimation method that allowed for a quantitative evaluation of the submissions based on the Tractometer connectivity metrics[38]. At the closing of the competition, we evaluated 96 distinct tractography pipelines submitted by 20 different research groups, in order to assess how well the algorithms were able to reproduce the known connectivity. An important positive finding is that most proposed algorithms are able to produce tractograms containing 90% of the ground truth bundles, recovering about one-third of their volumetric extent.

Methods

Results

Conclusion