Cited by 83Advanced Neuroimaging Techniques and ApplicationsFunctional Brain Connectivity StudiesAdvanced MRI Techniques and Applications

On the cortical connectivity in the macaque brain: a comparison of diffusion tractography and histological tracing data

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Girard, Gabriel, Caminiti, Roberto, Battaglia-Mayer, Alexandra, St-Onge, Etienne, Ambrosen, Karen S., Eskildsen, Simon F., Krug, Kristine, Dyrby, Tim B. +3 more·2020·NeuroImage

Abstract

Diffusion-weighted magnetic resonance imaging (DW-MRI) tractography is a non-invasive tool to probe neural connections and the structure of the white matter. It has been applied successfully in studies of neurological disorders and normal connectivity. Recent work has revealed that tractography produces a high incidence of false-positive connections, often from "bottleneck" white matter configurations. The rich literature in histological connectivity analysis studies in the macaque monkey enables quantitative evaluation of the performance of tractography algorithms. In this study, we use the intricate connections of frontal, cingulate, and parietal areas, well established by the anatomical literature, to derive a symmetrical histological connectivity matrix composed of 59 cortical areas. We evaluate the performance of fifteen diffusion tractography algorithms, including global, deterministic, and probabilistic state-of-the-art methods for the connectivity predictions of 1711 distinct pairs of areas, among which 680 are reported connected by the literature. The diffusion connectivity analysis was performed on a different ex-vivo macaque brain, acquired using multi-shell DW-MRI protocol, at high spatial and angular resolutions. Across all tested algorithms, the true-positive and true-negative connections were dominant over false-positive and false-negative connections, respectively. Moreover, three-quarters of streamlines had endpoints location in agreement with histological data, on average. Furthermore, probabilistic streamline tractography algorithms show the best performances in predicting which areas are connected. Altogether, we propose a method for quantitative evaluation of tractography algorithms, which aims at improving the sensitivity and the specificity of diffusion-based connectivity analysis. Overall, those results confirm the usefulness of tractography in predicting connectivity, although errors are produced. Many of the errors result from bottleneck white matter configurations near the cortical grey matter and should be the target of future implementation of methods.

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Crossref · 10.1016/j.neuroimage.2020.117201

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  • Animal studies using invasive tract-tracing techniques have shown good agreement between NOS and biological connectivity measured using ex vivo tract-tracing data.

    “Several studies conducted on animals using invasive tract-tracing techniques have shown good agreement between the NOS and the biological connectivity as measured using ex vivo tract-tracing data (Delettre et al., 2019; Girard et al., 2020; van den Heuvel et al., 2015a).”

    From Quantitative mapping of the brain’s structural connectivity using diffusion MRI tractography: A review (2022) · cites this paper as Girard et al., 2020

    The Conclusion reports good agreement between ex-vivo macaque tractography and connections identified by histological tracing. But §4.5 says the comparison was of binary connectivity, not histological cell counts or connection strength; it therefore does not establish good quantitative agreement between the number of streamlines (NOS) and biological connectivity. (LLM, conf=0.85)

    Experimental — accuracy not yet measured
  • Neural tracer data is the gold standard for mesoscale connectivity studies in a number of model organisms.

    “Neural tracer data is the gold standard for mesoscale connectivity studies in a number of model organisms (Bota et al., 2015; Girard et al., 2020; Jbabdi et al., 2015; Markov et al., 2014; 2013; Oh et al., 2014).”
  • Girard et al. (2020) rigorously benchmarked 15 tractography algorithms and regularization approaches against tracer data in macaque cortex, but did not present analysis of downstream network measures.

    “A recent study by Girard et al. (2020) rigorously benchmarked 15 tractography algorithms and a number of regularization approaches such as the “anatomically constrained tractography” framework (Smith et al., 2012) and the SIFT2 post-processing algorithm (Smith et al., 2015) against tracer data in the macaque cortex, though it did not present analysis of downstream network measures.”

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Research works printed but not linked: 3

  1. Daducci, A. , Dal Palu, A. , Lemkaddem, A. , Thiran, J.-P. , 2014. COMMIT: Convex optimiza- tion modeling for micro-structure informed tractography. IEEE Trans. Med. Imaging 34 (1) .
  2. Pajevic, S. , Pierpaoli, C. , 1999. Color schemes to represent the orientation of anisotropic tissues from diffusion tensor data: application to white matter fiber tract mapping in the human brain. Magn. Reson. Med. 42 (3), 526-540 .
  3. Tournier, J.-D. , Calamante, F. , Connelly, A. , 2010. Improved probabilistic streamlines trac- tography by 2 nd order integration over fibre orientation distributions. In: Proceed- ings of the International Symposium on Magnetic Resonance in Medicine. Stockholm, Sweden .

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Authors
Girard, G., Caminiti, R., Battaglia-Mayer, A., St-Onge, E., Ambrosen, K. S., Eskildsen, S. F., Krug, K., Dyrby, T. B., Descoteaux, M., Thiran, J.-P., & Innocenti, G. M.
Affiliations
  • Centre Hospitalier Universitaire Vaudois (CH)
  • Italian Institute of Technology (IT)
  • Hvidovre Hospital (DK)
  • Aarhus University (DK)
  • University of Oxford (GB)
  • Université de Sherbrooke (CA)
  • Karolinska Institutet (SE)
Corresponding author
Girard, Gabriel
Venue
NeuroImage
Publisher
Elsevier BV
Published
2020-11
Volume
221
Pages
117201
ISSN
1053-8119 (ISSN-L)
OpenAlex
W3046367338
Cited by
83
References
171
Citations by year
2026: 8 · 2025: 21 · 2024: 5 · 2023: 14 · 2022: 20 · 2021: 15
FWCI
5.99
Type
journal article
Language
en
Open access
Locations
  • NeuroImage (publishedVersion, cc-by-nc-nd)
  • PubMed (publishedVersion)
  • SERVAL (Université de Lausanne) (publishedVersion, cc-by-nc-nd)
  • IRIS (submittedVersion, cc-by-nc-nd)
  • IRIS Research product catalog (Sapienza University of Rome) (submittedVersion, cc-by-nc-nd)
  • DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
  • Informationszentrum Lebenswissenschaften (ZB MED) (submittedVersion, cc-by-nc-nd)
  • Infoscience (Ecole Polytechnique Fédérale de Lausanne) (submittedVersion, cc-by-nc-nd)
  • Scopus (Elsevier) (submittedVersion, cc-by-nc-nd)
  • Technical University of Denmark, DTU Orbit (Technical University of Denmark, DTU) (submittedVersion, cc-by-nc-nd)
Funders
  • Deutsche Forschungsgemeinschaft (406269671)
  • Istituto Italiano di Tecnologia (000000247)
  • Centre d'Imagerie BioMédicale
  • Ministero dell’Istruzione, dell’Università e della Ricerca (AWSW2Y_002, 94KEER_002)
  • École Polytechnique Fédérale de Lausanne
Topics
  • Health Sciences › Medicine › Radiology, Nuclear Medicine and Imaging › Advanced Neuroimaging Techniques and Applications
  • Life Sciences › Neuroscience › Cognitive Neuroscience › Functional Brain Connectivity Studies
  • Health Sciences › Medicine › Radiology, Nuclear Medicine and Imaging › Advanced MRI Techniques and Applications
Keywords
cortical connectivity, diffusion tractography, macaque brain, probabilistic tractography, deterministic tractography, multi-shell diffusion MRI, white matter structure
MeSH terms
Animals, Cerebral Cortex, Histological Techniques, Macaca mulatta, Male, Nerve Net, Diffusion Tensor Imaging, Neuroanatomical Tract-Tracing Techniques, White Matter

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