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The structural connectivity of the human angular gyrus as revealed by microdissection and diffusion tractography

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Abstract

The angular gyrus (AG) has been described in numerous studies to be consistently activated in various functional tasks. The angular gyrus is a critical connector epicenter linking multiple functional networks due to its location in the posterior part of the inferior parietal cortex, namely at the junction between the parietal, temporal, and occipital lobes. It is thus crucial to identify the different pathways that anatomically connect this high-order association region to the rest of the brain. Our study revisits the three-dimensional architecture of the structural AG connectivity by combining state-of-the-art postmortem blunt microdissection with advanced in vivo diffusion tractography to comprehensively describe the association, projection, and commissural fibers that connect the human angular gyrus. AG appears as a posterior “angular stone” of associative connections belonging to mid- and long-range dorsal and ventral fibers of the superior and inferior longitudinal systems, respectively, to short-range parietal, occipital, and temporal fibers, including U-shaped fibers in the posterior transverse system. Thus, AG is at a pivotal dorso-ventral position reflecting its critical role in the different functional networks, particularly in language elaboration and spatial attention and awareness in the left and right hemispheres, respectively. We also reveal striatal, thalamic, and brainstem connections and a typical inter-hemispheric homotopic callosal connectivity supporting the suggested AG role in the integration of sensory input for modulating motor control and planning. The present description of AG’s highly distributed wiring diagram may drastically improve intraoperative subcortical testing and post-operative neurologic outcomes related to surgery in and around the angular gyrus.

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Data availability

The in vivo diffusion MRI dataset analyzed in the current study belongs to the BIL&GIN database. The BIL&GIN is not freely available, but a data-sharing model based on collaborative research agreements has been implemented. Request for joint research projects can be made through the BIL&GIN website or by email to the corresponding author of the present paper.

Code availability

Software application or custom code: no specific code developed, not applicable.

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Authors and Affiliations

  1. Groupe d’Imagerie Neurofonctionnelle, Centre Broca Nouvelle-Aquitaine - 3ème étage, Université Bordeaux, Institut des Maladies Neurodégénératives CNRS UMR 5293, 146 rue Léo Saignat - CS 61292 - Case 28, 33000, Bordeaux, France

    Laurent Petit & Sandrine Cremona

  2. Department of Neurosurgery, Medical University of Graz, Graz, Austria

    Kariem Mahdy Ali

  3. Electrical and Computer Engineering, Vanderbilt University, Nashville, USA

    François Rheault

  4. Sherbrooke Connectivity Imaging Lab (SCIL), Université de Sherbrooke, Sherbrooke, Canada

    Arnaud Boré & Maxime Descoteaux

  5. Department of Neurosurgery, Azienda Provinciale per i Servizi Sanitari, “S. Chiara” Hospital, Trento, Italy

    Francesco Corsini & Silvio Sarubbo

  6. Neurosurgery Unit, Department of Neurosciences, Bambino Gesù Children’s Hospital, IRCCS, Rome, Italy

    Alessandro De Benedictis

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  1. Laurent Petit
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The present manuscript is not submitted elsewhere for simultaneous consideration; the submitted work is original and has not been published elsewhere in any form or language (partially or in whole); no re-use of material to avoid the concerns about text-recycling (self-plagiarism) in the present manuscript; the part of the study, including in vivo diffusion MRI data, was approved by the local ethics committee (CCPRB Basse-Normandie, France).The part of the study, including postmortem dissection data, was approved by the Ethical Committee of the Azienda Provinciale per i Servizi Sanitari, Trento, Italy (N° 06/2018).

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For the part of the study involving in vivo diffusion MRI data, all participants gave written consent prior to participation in the study and no opposition to the publication of any type of results generated with their data.

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Supplementary file1 (DOCX 45 KB)

429_2022_2551_MOESM2_ESM.pdf

Supplementary file2. Axial, sagittal and coronal sections of the 23 probabilistic maps of the present AG connectivity in MNI space. For a given tract, the color bar indicates the frequency of voxels containing the tract from 50 to 100% of the participants where the tract was frequently observed (close to the total of 411 participants, actc color scale) or from 10 to 100% of the participants where the tract was less frequently observed (plasma color scale). For example, for a tract observed in all participants, a value of 80 in a voxel means that 329 out of 411 individual tracts are passing through this voxel. L left, R right. Displays made with MRIcroGL (http://www.nitrc.org/projects/mricrogl/). (PDF 11495 KB)

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Petit, L., Ali, K.M., Rheault, F. et al. The structural connectivity of the human angular gyrus as revealed by microdissection and diffusion tractography. Brain Struct Funct 228, 103–120 (2023). https://doi.org/10.1007/s00429-022-02551-5

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