Exploring the macaque precentral intragyral white matter using ultra-high field 11.7T dMRI

Presented During:

Wednesday, June 26, 2024: 11:30 AM - 12:45 PM
COEX  
Room: Conference Room E 1  

Poster No:

2194 

Submission Type:

Abstract Submission 

Authors:

Fanny Darrault1, Maëlig Chauvel2,3, Cyril Poupon3, Ivy Uszynski3, Christophe Destrieux1,4, Igor Lima Maldonado1,4, Frédéric Andersson1

Institutions:

1UMR 1253, iBrain, Université de Tours, Inserm, Tours, France, 2Max Planck Institute for Human Cognitive and Brain Sciences, Leipzig, Germany, 3BAOBAB, NeuroSpin, Paris-Saclay University, CNRS, CEA, Gif-sur-Yvette, Essonne, 4CHRU de Tours, Tours, France

Co-Author(s):

Fanny Darrault  
UMR 1253, iBrain, Université de Tours, Inserm
Tours, France
Maëlig Chauvel  
Max Planck Institute for Human Cognitive and Brain Sciences|BAOBAB, NeuroSpin, Paris-Saclay University, CNRS, CEA
Leipzig, Germany|Gif-sur-Yvette, Essonne
Cyril Poupon  
BAOBAB, NeuroSpin, Paris-Saclay University, CNRS, CEA
Gif-sur-Yvette, Essonne
Ivy Uszynski  
BAOBAB, NeuroSpin, Paris-Saclay University, CNRS, CEA
Gif-sur-Yvette, Essonne
Christophe Destrieux  
UMR 1253, iBrain, Université de Tours, Inserm|CHRU de Tours
Tours, France|Tours, France
Igor Lima Maldonado  
UMR 1253, iBrain, Université de Tours, Inserm|CHRU de Tours
Tours, France|Tours, France
Frédéric Andersson  
UMR 1253, iBrain, Université de Tours, Inserm
Tours, France

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 diffusion 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/mm² along 25/60/90 diffusion directions; TE=24.33ms; TR=250ms; 250μm3 isotropic resolution; total scan duration=99h) for the diffusion 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% (Fig. 1). 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 (Fig. 2).

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.
Supporting Image: fig1_tracto.png
Supporting Image: Fig2_densitymaps-trajet.png
 

Modeling and Analysis Methods:

Connectivity (eg. functional, effective, structural)
Diffusion MRI Modeling and Analysis

Neuroanatomy, Physiology, Metabolism and Neurotransmission:

Cortical Anatomy and Brain Mapping
White Matter Anatomy, Fiber Pathways and Connectivity 1

Novel Imaging Acquisition Methods:

Diffusion MRI 2

Keywords:

Cortex
HIGH FIELD MR
MRI
Tractography
White Matter
WHITE MATTER IMAGING - DTI, HARDI, DSI, ETC
Other - Precentral gyrus

1|2Indicates the priority used for review

Provide references using author date format

Dannhoff G, et al., Depicting the anatomy of the gyral white matter: ubi sumus? quo vadimus?, Brain Communications, Volume 5, Issue 5, 2023, fcad265, https://doi.org/10.1093/braincomms/fcad265
Gordon EM, et al., A somato-cognitive action network alternates with effector regions in motor cortex. Nature. 2023 May;617(7960):351-359. doi: 10.1038/s41586-023-05964-2. Epub 2023 Apr 19. PMID: 37076628; PMCID: PMC10172144.
Schmahmann, Jeremy D., and Deepak N. Pandya, Fiber Pathways of the Brain (New York, 2006; online edn, Oxford Academic, 1 May 2009),
Perrin, M., et al., (2005). Fiber tracking in q-ball fields using regularized particle trajectories. In Information Processing in Medical Imaging: 19th International Conference, IPMI 2005, Glenwood Springs, CO, USA, July 10-15, 2005. Proceedings 19 (pp. 52-63). Springer Berlin Heidelberg.
Ginkgo Toolbox repository: https://framagit.org/cpoupon/gkg