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Exploring the macaque precentral intragyral white matter using ultra-high field 11.7T dMRI
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International audience. Introduction: Within the gyral white matter, three types of fibers converge: association, projection, and commissural. Currently, models of gyral white matter structural organization based on autoradiographic studies conducted in non-human primates (Schmahmann and Pandya, 2010; Dannhoff et al. 2023) describe their trajectory until the fibers arrive near the grey matter. However, there is little information characterizing their organization within the gyrus. The development of ultra-high field ex vivo MRI and advances in tractography algorithms, at the mesoscopic resolution, now allow us access to this intermingled fibers’ organization. We sought to investigate the structural organization of white matter in the precentral gyrus (PrCG) of the macaque brain, using an ultra-high field 11.7T di!usion MRI dataset.Methods: The post-mortem brain of a healthy adult male cynomolgus macaque (Macaca Fascicularis) was scanned on a preclinical Bruker BioSpec MRI 11.7T with an MSME sequence (TR=350ms, TE=20ms, 100µm3 isotropic resolution, total scan duration=30h) for the anatomical dataset and with a 3D-segmented EPI PGSE sequence (32 segments; 3-shells q-space sampling at b=1500/4500/8000 s/mm, along 25/60/90 di!usion directions; TE=24.33ms; TR=250ms; 250µm3 isotropic resolution; total scan duration=99h) for the di!usion dataset. Regularized streamline probabilistic tractography was performed using Ginkgo, seeding within a mask corresponding to the white matter plus the grey/white matter interface (27 seeds per voxel, forward step=62.5um, maximum aperture angle of 15°), stopping streamlining at the mask boundary or when the GFA falls below 0.02. Regions of interest (ROIs) were manually segmented, by 2 independent observers: PrCG, cortical grey matter, basal ganglia as one ROI, brainstem and cerebellum as one ROI, several slices of the internal capsules, anterior commissure, and the corpus callosum. They were used to filter the tractogram into projection, association, and commissural fibers. We used the virtual dissection tools in DSI Studio to further filter the resulting tracts and remove artifactual fibers. Results: Among the fibers ending in the PrCG, 65% were association fibers mostly short and strongly curved, corresponding to intergyral fibers poorly described in the literature. Projection fibers accounted for 17% of the fibers and commissural fibers for 16%. Fibers converged towards the gyrus in partially intermingled strata and then crossed extensively as they reached the grey/white matter interface. Association fibers, traveling mostly at the extremities of the gyrus were then found along the gyrus convexity. Projection fibers approached the gyrus at its center but projected to the superior border and anteroinferior extremity with low density in the middle of the gyrus convexity. Commissural fibers were also found at its center but then projected at the gyrus’s dorsomedial end and its posterior border.Conclusions: Using ultra-high resolution MRI data and tractography, we depicted the intra-gyral organization of white matter of the PrCG. We observed a basal arrangement in partially intermingled strata, transitioning to numerous crossings at the grey/white matter interface. The distribution of each type of fibers highlights the predominance of associative fibers in the PrCG and its functional heterogeneity. Our results are consistent with recent functional MRI studies in humans showing regions of body/action somato-cognitive functions interrupt and intermingle with regions specialized for motor function (Gordon et al., 2023). Thus, we showed that the PrCG, often simplified as the primary motor gyrus, has a strong associative component that intermingles with motor regions. The ability of ultra-high resolution MRI to reconstruct fiber pathways in and around the gyrus demonstrates the potential of this technique to bridge data acquired from macaque studies to human neuroanatomy.
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