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

Girard, Gabriel; Caminiti, Roberto; Battaglia-Mayer, Alexandra; St-Onge, Etienne; Ambrosen, Karen S; Eskildsen, Simon Fristed; Krug, Kristine; Dyrby, Tim B.; Descoteaux, Maxime; Thiran, Jean‐Philippe; Innocenti, Giorgio M.

doi:10.1016/j.neuroimage.2020.117201

Cited by 59 publications

(68 citation statements)

References 148 publications

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“…the 0.39 reported in Girard et al (2020). Moreover, in the network studied here, we found 90.4% of the connectivity weights between ROIs with reported non-zero labelled cell count, 10.2% more than reported by Girard et al (2020). This suggests a strong predictive power of tractography for the connectivity of the monkeys IPS, which was also confirmed by the lack of connections with prefrontal areas shown by both histological and tractography results.…”

Section: Diffusion-based Connectivity Estimationssupporting

confidence: 82%

Section: Diffusion-based Connectivity Estimationssupporting

confidence: 47%

“…Across the four matching site's location, tractography misestimated the connectivity the most on ROIs F2, PE, M1, VIP and LIP. The source of these errors can be the intricate white matter geometries and configurations, such as crossing and kissing, causing tractography to follow incorrect orientations (see Jeurissen et al 2017 andGirard et al, 2020).…”

Section: Tractography Misestimated Connectionsmentioning

confidence: 99%

“…The diffusion-weighted MRI (DW-MRI) data from ex-vivo brain of a male Macaca mulatta (M105, 4 years and 10 months old, 10.1 kg body weight) available from Ambrosen et al (2020) was used. The brain was perfused following the protocol illustrated in Ahmed et al (2012) and prepared for MRI ex-vivo scanning as described by Dyrby et al (2011).…”

Section: Diffusion-weighted Mri Experimentsmentioning

confidence: 99%

“…The difficulties of histological studies can tentatively be overcome by diffusion-weighted MRI tractography (DW-MRI). Albeit known limitations, such as the identification of false-positive connections and biases toward reconstructing short and strong connections (Jones et al, 2013;Van Essen et al, 2014;Jbabdi et al, 2015;Knosche et al, 2015;Jeurissen et al, 2017;Maier-Hein et al, 2017;Aydogan et al, 2018;Schilling et al, 2019a,b;Girard et al, 2020), tractography shows promising results when compared to histology (Dauguet et al, 2007;Dyrby et al, 2007;Seehaus et al, 2012;Jbabdi et al, 2013;Thomas et al, 2014;Azadbakht et al, 2015;Calabrese et al, 2015;Gyengesi et al, 2015;van den Heuvel et al, 2015;Knosche et al, 2015;Donahue et al, 2016;Delettre et al, 2019;Ambrosen et al, 2020;Girard et al, 2020). Particularly, Calabrese et al (2015), Donahue et al (2016) and Ambrosen et al (2020) have reported positive results when comparing labelled cells count from tracer injections in the monkey brain with connectivity weights derived from DW-MRI tractography.…”

Section: Introductionmentioning

confidence: 99%

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The Complex Hodological Architecture of the Macaque Dorsal Intraparietal Areas as Emerging From Neural Tracers and Dw-Mri Tractography

Caminiti

Girard

Battaglia-Mayer

et al. 2021

Preprint

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In macaque monkeys, dorsal intraparietal areas are involved in several daily visuo-motor actions. However, their border and sources of cortical afferents remain loosely defined. Through a retrograde tracer and MRI diffusion-based tractography study here we show a complex organization of the dorsal bank of the IPS, which can be subdivided into a rostral area PEip, projecting to the spinal cord, and a caudal area MIP lacking such projections. Both areas include a rostral and a caudal sector, emerging from their ipsilateral, gradient-like connectivity profiles. As tractography estimations, we used the cross-sectional volume of the white matter bundles connecting each area with other parietal and frontal regions, after selecting ROIs corresponding to the injection sites of retrograde tracers. A quantitative analysis between the proportions of cells projecting to all sectors of PEip and MIP along the continuum of the dorsal bank of the IPS and tractography revealed a significant correlation between the two data sets for most connections. Moreover, tractography revealed false positive but plausible streamlines awaiting histological validation.

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Section: Diffusion-based Connectivity Estimationssupporting

confidence: 82%

Section: Diffusion-based Connectivity Estimationssupporting

confidence: 47%

Section: Tractography Misestimated Connectionsmentioning

confidence: 99%

Section: Diffusion-weighted Mri Experimentsmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

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The Complex Hodological Architecture of the Macaque Dorsal Intraparietal Areas as Emerging From Neural Tracers and Dw-Mri Tractography

Caminiti

Girard

Battaglia-Mayer

et al. 2021

Preprint

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Striatonigrostriatal connectivity‐based cross‐species parcellation of human and macaque substantia nigra

Xia

Zeng

Gao

et al. 2023

Human Brain Mapping

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Anatomical and functional heterogeneous substantia nigra (SN) has been extensively studied in humans and animals like rhesus monkeys given its crucial role in modulating a broad range of behaviors. Increasingly important cross-species research of SN may require connectionally homogeneous and homologous subregions of SN as objective and stable starting points from which the evolutionary characteristics of brain could be inspected. However, existing atlases of SN were all inaccurate mappings as a cross-species connectome atlas due to inadequate homology constraint during their constructions, and arbitrary paired use of these atlases might cause unreliable findings. In this study, a reliable blind-source cross-species parcellation of SN was developed based on the following rationale: striatonigrostriatal circuits form major structure of nigral connectivity; different nigral components have unique striatonigrostriatal connectivity; and inter-species corresponding human and macaque nigral components have similar striatonigrostriatal connectivity. Specifically, all voxels in human and macaque SN were grouped together and then classified based on interspecies identically characterized striatonigrostriatal connectivity attributes. Our results delineated a pars compacta-pars reticulate-like parcellation and further demonstrated its reliability by illustrating best-matched whole-brain structural and functional connectivity profiles of inter-species corresponding nigral subregions. Detailed inter-species and inter-regional differences in multi-aspect connectivities of these nigral subregions were inspected. It is expected that this cross-species connectome atlas of SN can offer biologically reliable cornerstones and important information to facilitate future cross-species research.

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Reconstructing the somatotopic organization of the corticospinal tract remains a challenge for modern tractography methods

He,

Zhang,

Pan

et al. 2023

Human Brain Mapping

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The corticospinal tract (CST) is a critically important white matter fiber tract in the human brain that enables control of voluntary movements of the body. The CST exhibits a somatotopic organization, which means that the motor neurons that control specific body parts are arranged in order within the CST. Diffusion magnetic resonance imaging (MRI) tractography is increasingly used to study the anatomy of the CST. However, despite many advances in tractography algorithms over the past decade, modern, state‐of‐the‐art methods still face challenges. In this study, we compare the performance of six widely used tractography methods for reconstructing the CST and its somatotopic organization. These methods include constrained spherical deconvolution (CSD) based probabilistic (iFOD1) and deterministic (SD‐Stream) methods, unscented Kalman filter (UKF) tractography methods including multi‐fiber (UKF2T) and single‐fiber (UKF1T) models, the generalized q‐sampling imaging (GQI) based deterministic tractography method, and the TractSeg method. We investigate CST somatotopy by dividing the CST into four subdivisions per hemisphere that originate in the leg, trunk, hand, and face areas of the primary motor cortex. A quantitative and visual comparison is performed using diffusion MRI data (N = 100 subjects) from the Human Connectome Project. Quantitative evaluations include the reconstruction rate of the eight anatomical subdivisions, the percentage of streamlines in each subdivision, and the coverage of the white matter–gray matter (WM–GM) interface. CST somatotopy is further evaluated by comparing the percentage of streamlines in each subdivision to the cortical volumes for the leg, trunk, hand, and face areas. Overall, UKF2T has the highest reconstruction rate and cortical coverage. It is the only method with a significant positive correlation between the percentage of streamlines in each subdivision and the volume of the corresponding motor cortex. However, our experimental results show that all compared tractography methods are biased toward generating many trunk streamlines (ranging from 35.10% to 71.66% of total streamlines across methods). Furthermore, the coverage of the WM–GM interface in the largest motor area (face) is generally low (under 40%) for all compared tractography methods. Different tractography methods give conflicting results regarding the percentage of streamlines in each subdivision and the volume of the corresponding motor cortex, indicating that there is generally no clear relationship, and that reconstruction of CST somatotopy is still a large challenge. Overall, we conclude that while current tractography methods have made progress toward the well‐known challenge of improving the reconstruction of the lateral projections of the CST, the overall problem of performing a comprehensive CST reconstruction, including clinically important projections in the lateral (hand and face areas) and medial portions (leg area), remains an important challenge for diffusion MRI tractography.

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

Cited by 59 publications

References 148 publications

The Complex Hodological Architecture of the Macaque Dorsal Intraparietal Areas as Emerging From Neural Tracers and Dw-Mri Tractography

The Complex Hodological Architecture of the Macaque Dorsal Intraparietal Areas as Emerging From Neural Tracers and Dw-Mri Tractography

Striatonigrostriatal connectivity‐based cross‐species parcellation of human and macaque substantia nigra

Reconstructing the somatotopic organization of the corticospinal tract remains a challenge for modern tractography methods

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