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22-08-2022 | Original Article

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

Authors: Laurent Petit, Kariem Mahdy Ali, François Rheault, Arnaud Boré, Sandrine Cremona, Francesco Corsini, Alessandro De Benedictis, Maxime Descoteaux, Silvio Sarubbo

Published in: Brain Structure and Function | Issue 1/2023

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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Avants BB, Tustison NJ, Song G (2009) Advanced normalization tools (ANTS). Insight J 2:1–35

Box GEP, Cox DR (1964) An analysis of transformations. J Roy Stat Soc Ser B (methodol) 26(2):211–252

Bullock D, Takemura H, Caiafa CF, Kitchell L, McPherson B, Caron B, Pestilli F (2019) Associative white matter connecting the dorsal and ventral posterior human cortex. Brain Struct Funct 224(8):2631–2660. https://doi.org/10.1007/s00429-019-01907-8CrossRef

Catani M, Robertsson N, Beyh A, Huynh V, de Santiago RF, Howells H, Barrett RLC, Aiello M, Cavaliere C, Dyrby TB, Krug K, Ptito M, D’Arceuil H, Forkel SJ, Dell’Acqua F (2017) Short parietal lobe connections of the human and monkey brain. Cortex 97:339–357. https://doi.org/10.1016/j.cortex.2017.10.022CrossRef

Cattaneo L, Barchiesi G (2011) Transcranial magnetic mapping of the short-latency modulations of corticospinal activity from the ipsilateral hemisphere during rest. Front Neural Circuits 5:14. https://doi.org/10.3389/fncir.2011.00014CrossRef

Cattaneo L, Giampiccolo D, Meneghelli P, Tramontano V, Sala F (2020) Cortico-cortical connectivity between the superior and inferior parietal lobules and the motor cortex assessed by intraoperative dual cortical stimulation. Brain Stimul 13(3):819–831. https://doi.org/10.1016/j.brs.2020.02.023CrossRef

Caverzasi E, Papinutto N, Amirbekian B, Berger MS, Henry RG (2014) Q-Ball of Inferior Fronto-Occipital Fasciculus and Beyond. PLoS ONE 9(6):e100274. https://doi.org/10.1371/journal.pone.0100274CrossRef

Chenot Q, Tzourio-Mazoyer N, Rheault F, Descoteaux M, Crivello F, Zago L, Mellet E, Jobard G, Joliot M, Mazoyer B, Petit L (2019) A population-based atlas of the human pyramidal tract in 410 healthy participants. Brain Struct Funct 224(2):599–612. https://doi.org/10.1007/s00429-018-1798-7CrossRef

Crosby E, Humphrey T, Lauer EW (1962) Correlative anatomy of the nervous system. The MacMillan Company, New York

De Benedictis A, Petit L, Descoteaux M, Marras CE, Barbareschi M, Corsini F, Dallabona M, Chioffi F, Sarubbo S (2016) New insights in the homotopic and heterotopic connectivity of the frontal portion of the human corpus callosum revealed by microdissection and diffusion tractography. Hum Brain Mapp 37(12):4718–4735. https://doi.org/10.1002/hbm.23339CrossRef

De Benedictis A, Nocerino E, Menna F, Remondino F, Barbareschi M, Rozzanigo U, Corsini F, Olivetti E, Marras CE, Chioffi F, Avesani P, Sarubbo S (2018) Photogrammetry of the human brain: a novel method for three-dimensional quantitative exploration of the structural connectivity in neurosurgery and neurosciences. World Neurosurg 115:e279–e291. https://doi.org/10.1016/j.wneu.2018.04.036CrossRef

De Benedictis A, Marras CE, Petit L, Sarubbo S (2021) The inferior fronto-occipital fascicle: a century of controversies from anatomy theaters to operative neurosurgery. J Neurosurg Sci 65(6):605–615. https://doi.org/10.23736/S0390-5616.21.05360-1CrossRef

Dejerine J, Dejerine-Klumpke A (1895) Anatomie des centres nerveux. Tome 1. Rueff et Cie, Paris

Dejerine J, Dejerine-Klumpke A (1901) Anatomie des centres nerveux. Tome 2. Rueff et Cie, Paris

Di Carlo DT, Benedetto N, Duffau H, Cagnazzo F, Weiss A, Castagna M, Cosottini M, Perrini P (2019) Microsurgical anatomy of the sagittal stratum. Acta Neurochir (wien) 161(11):2319–2327. https://doi.org/10.1007/s00701-019-04019-8CrossRef

Di Tommaso P, Chatzou M, Floden EW, Barja PP, Palumbo E, Notredame C (2017) Nextflow enables reproducible computational workflows. Nat Biotechnol 35(4):316–319. https://doi.org/10.1038/nbt.3820CrossRef

Gallivan JP, Culham JC (2015) Neural coding within human brain areas involved in actions. Curr Opin Neurobiol 33:141–149. https://doi.org/10.1016/j.conb.2015.03.012CrossRef

Guevara M, Guevara P, Román C, Mangin J-F (2020) Superficial white matter: a review on the dMRI analysis methods and applications. Neuroimage 212:116673. https://doi.org/10.1016/j.neuroimage.2020.116673CrossRef

Hau J, Sarubbo S, Perchey G, Crivello F, Zago L, Mellet E, Jobard G, Joliot M, Mazoyer BM, Tzourio-Mazoyer N, Petit L (2016) Cortical terminations of the inferior fronto-occipital and uncinate fasciculi: anatomical stem-based virtual dissection. Front Neuroanat 10:58. https://doi.org/10.3389/fnana.2016.00058CrossRef

Jiao Y, Lin F, Wu J, Li H, Fu W, Huo R, Cao Y, Wang S, Zhao J (2020) Plasticity in language cortex and white matter tracts after resection of dominant inferior parietal lobule arteriovenous malformations: a combined fMRI and DTI study. J Neurosurg 134(3):953–960. https://doi.org/10.3171/2019.12.JNS191987CrossRef

Kinomura S, Larsson J, Gulyas B, Roland PE (1996) Activation by attention of the human reticular formation and thalamic intralaminar nuclei. Science 271:512–515CrossRef

Kiriyama I, Miki H, Kikuchi K, Ohue S, Matsuda S, Mochizuki T (2009) Topographic analysis of the inferior parietal lobule in high-resolution 3D MR imaging. AJNR Am J Neuroradiol 30(3):520–524. https://doi.org/10.3174/ajnr.A1417CrossRef

Koch G, Cercignani M, Pecchioli C, Versace V, Oliveri M, Caltagirone C, Rothwell J, Bozzali M (2010) In vivo definition of parieto-motor connections involved in planning of grasping movements. Neuroimage 51(1):300–312. https://doi.org/10.1016/j.neuroimage.2010.02.022CrossRef

Kurtzer GM, Sochat V, Bauer MW (2017) Singularity: Scientific containers for mobility of compute. PLoS ONE 12(5):e0177459. https://doi.org/10.1371/journal.pone.0177459CrossRef

LaBerge D (1995) Computational and anatomical models of selective attention in object identification. In: Gazzaniga MS (ed) The cognitive neurosciences, vol 41. MIT Press, Cambridge, pp 649–663

Latini F, Trevisi G, Fahlstrom M, Jemstedt M, Alberius Munkhammar A, Zetterling M, Hesselager G, Ryttlefors M (2020) New insights into the anatomy, connectivity and clinical implications of the middle longitudinal fasciculus. Front Neuroanat 14(106):610324. https://doi.org/10.3389/fnana.2020.610324CrossRef

Ludwig E, Klingler J (1956) Atlas cerebri humani. S. Karger, Basel

Maffei C, Sarubbo S, Jovicich J (2019) Diffusion-based tractography atlas of the human acoustic radiation. Sci Rep 9(1):4046. https://doi.org/10.1038/s41598-019-40666-8CrossRef

Mahdy Ali K, Avesani P (2021) The vertical superior longitudinal fascicle and the vertical occipital fascicle. J Neurosurg Sci 65(6):581–589. https://doi.org/10.23736/S0390-5616.21.05368-6CrossRef

Maier-Hein KH, Neher PF, Houde JC, Cote MA, Garyfallidis E, Zhong J, Chamberland M, Yeh FC, Lin YC, Ji Q, Reddick WE, Glass JO, Chen DQ, Feng Y, Gao C, Wu Y, Ma J, He R, Li Q, Westin CF, Deslauriers-Gauthier S, Gonzalez JOO, Paquette M, St-Jean S, Girard G, Rheault F, Sidhu J, Tax CMW, Guo F, Mesri HY, David S, Froeling M, Heemskerk AM, Leemans A, Bore A, Pinsard B, Bedetti C, Desrosiers M, Brambati S, Doyon J, Sarica A, Vasta R, Cerasa A, Quattrone A, Yeatman J, Khan AR, Hodges W, Alexander S, Romascano D, Barakovic M, Auria A, Esteban O, Lemkaddem A, Thiran JP, Cetingul HE, Odry BL, Mailhe B, Nadar MS, Pizzagalli F, Prasad G, Villalon-Reina JE, Galvis J, Thompson PM, Requejo FS, Laguna PL, Lacerda LM, Barrett R, Dell’Acqua F, Catani M, Petit L, Caruyer E, Daducci A, Dyrby TB, Holland-Letz T, Hilgetag CC, Stieltjes B, Descoteaux M (2017) The challenge of mapping the human connectome based on diffusion tractography. Nat Commun 8(1):1349. https://doi.org/10.1038/s41467-017-01285-xCrossRef

Makris N, Preti MG, Wassermann D, Rathi Y, Papadimitriou GM, Yergatian C, Dickerson BC, Shenton ME, Kubicki M (2013) Human middle longitudinal fascicle: segregation and behavioral-clinical implications of two distinct fiber connections linking temporal pole and superior temporal gyrus with the angular gyrus or superior parietal lobule using multi-tensor tractography. Brain Imaging Behav 7(3):335–352. https://doi.org/10.1007/s11682-013-9235-2CrossRef

Makris N, Zhu A, Papadimitriou GM, Mouradian P, Ng I, Scaccianoce E, Baselli G, Baglio F, Shenton ME, Rathi Y, Dickerson B, Yeterian E, Kubicki M (2017) Mapping temporo-parietal and temporo-occipital cortico-cortical connections of the human middle longitudinal fascicle in subject-specific, probabilistic, and stereotaxic Talairach spaces. Brain Imaging Behav 11(5):1258–1277. https://doi.org/10.1007/s11682-016-9589-3CrossRef

Mandonnet E, Sarubbo S, Petit L (2018) The nomenclature of human white matter association pathways: proposal for a systematic taxonomic anatomical classification. Front Neuroanat 12:94. https://doi.org/10.3389/fnana.2018.00094CrossRef

Martino J, Brogna C, Robles SG, Vergani F, Duffau H (2010) Anatomic dissection of the inferior fronto-occipital fasciculus revisited in the lights of brain stimulation data. Cortex 46(5):691–699. https://doi.org/10.1016/j.cortex.2009.07.015CrossRef

Matsumoto R, Nair DR, Ikeda A, Fumuro T, LaPresto E, Mikuni N, Bingaman W, Miyamoto S, Fukuyama H, Takahashi R, Najm I, Shibasaki H, Lüders HO (2012) Parieto-frontal network in humans studied by cortico-cortical evoked potential. Hum Brain Mapp 33(12):2856–2872. https://doi.org/10.1002/hbm.21407CrossRef

Mazoyer B, Mellet E, Perchey G, Zago L, Crivello F, Jobard G, Delcroix N, Vigneau M, Leroux G, Petit L, Joliot M, Tzourio-Mazoyer N (2016) BIL&GIN: A neuroimaging, cognitive, behavioral, and genetic database for the study of human brain lateralization. Neuroimage. https://doi.org/10.1016/j.neuroimage.2015.02.071CrossRef

Mesulam M-M (2008) Representation, inference, and transcendent encoding in neurocognitive networks of the human brain. Ann Neurol 64(4):367–378CrossRef

Meynert T (1885) Psychiatry: clinical treatise on the diseases of the fore-brain, trans. B. Sachs. GP Putnam, New York & London

Nieuwenhuys R, Voogd J, van Huijzen C (2008) The human central nervous system, 4th edn. Springer-Verlag, BerlinCrossRef

Niu M, Palomero-Gallagher N (2022) Architecture and connectivity of the human angular gyrus and of its homolog region in the macaque brain. Brain Struct Funct. https://doi.org/10.1007/s00429-022-02509-7CrossRef

Oishi K, Faria A, Jiang H, Li X, Akhter K, Zhang J, Hsu JT, Miller MI, van Zijl PCM, Albert M, Lyketsos CG, Woods R, Toga AW, Pike GB, Rosa-Neto P, Evans A, Mazziotta J, Mori S (2009) Atlas-based whole brain white matter analysis using large deformation diffeomorphic metric mapping: application to normal elderly and Alzheimer’s disease participants. Neuroimage 46(2):486–499CrossRef

Palejwala AH, O’Connor KP, Pelargos P, Briggs RG, Milton CK, Conner AK, Milligan TM, O’Donoghue DL, Glenn CA, Sughrue ME (2020) Anatomy and white matter connections of the lateral occipital cortex. Surg Radiol Anat 42(3):315–328. https://doi.org/10.1007/s00276-019-02371-zCrossRef

Petit L, Rheault F, Descoteaux M, Tzourio-Mazoyer N Half of the streamlines built in a whole human brain tractogram is anatomically uninterpretable. In: 25th Conference of the Organization for Human Brain Mapping, Roma, 2019.

Petit L, Pouget P (2019) The comparative anatomy of frontal eye fields in primates. Cortex 118:51–64. https://doi.org/10.1016/j.cortex.2019.02.023CrossRef

Rebelo D, Oliveira F, Abrunhosa A, Januario C, Lemos J, Castelo-Branco M (2021) A link between synaptic plasticity and reorganization of brain activity in Parkinson’s disease. Proc Natl Acad Sci U S A 118(3):e2013962118. https://doi.org/10.1073/pnas.2013962118CrossRef

Rheault F, Poulin P, Valcourt Caron A, St-Onge E, Descoteaux M (2020) Common misconceptions, hidden biases and modern challenges of dMRI tractography. J Neural Eng 17(1):011001. https://doi.org/10.1088/1741-2552/ab6aadCrossRef

Richard N, Desmurget M, Teillac A, Beuriat PA, Bardi L, Coude G, Szathmari A, Mottolese C, Sirigu A, Hiba B (2021) Anatomical bases of fast parietal grasp control in humans: a diffusion-MRI tractography study. Neuroimage 235:118002. https://doi.org/10.1016/j.neuroimage.2021.118002CrossRef

Rozzi S, Calzavara R, Belmalih A, Borra E, Gregoriou GG, Matelli M, Luppino G (2006) Cortical connections of the inferior parietal cortical convexity of the macaque monkey. Cereb Cortex 16(10):1389–1417. https://doi.org/10.1093/cercor/bhj076CrossRef

Sarubbo S, Le Bars E, Moritz-Gasser S, Duffau H (2012) Complete recovery after surgical resection of left Wernicke’s area in awake patient: a brain stimulation and functional MRI study. Neurosurg Rev 35(2):287–292. https://doi.org/10.1007/s10143-011-0351-4CrossRef

Sarubbo S, De Benedictis A, Maldonado IL, Basso G, Duffau H (2013) Frontal terminations for the inferior fronto-occipital fascicle: anatomical dissection, DTI study and functional considerations on a multi-component bundle. Brain Struct Funct 218:21–37. https://doi.org/10.1007/s00429-011-0372-3CrossRef

Sarubbo S, De Benedictis A, Merler S, Mandonnet E, Balbi S, Granieri E, Duffau H (2015) Towards a functional atlas of human white matter. Hum Brain Mapp 36(8):3117–3136. https://doi.org/10.1002/hbm.22832CrossRef

Sarubbo S, De Benedictis A, Merler S, Mandonnet E, Barbareschi M, Dallabona M, Chioffi F, Duffau H (2016) Structural and functional integration between dorsal and ventral language streams as revealed by blunt dissection and direct electrical stimulation. Hum Brain Mapp 37(11):3858–3872. https://doi.org/10.1002/hbm.23281CrossRef

Sarubbo S, Tate M, De Benedictis A, Merler S, Moritz-Gasser S, Herbet G, Duffau H (2020) Mapping critical cortical hubs and white matter pathways by direct electrical stimulation: an original functional atlas of the human brain. Neuroimage 205:116237. https://doi.org/10.1016/j.neuroimage.2019.116237CrossRef

Schilling KG, Tax CMW, Rheault F, Landman BA, Anderson AW, Descoteaux M, Petit L (2022) Prevalence of white matter pathways coming into a single white matter voxel orientation: the bottleneck issue in tractography. Hum Brain Mapp 43(4):1196–1213. https://doi.org/10.1002/hbm.25697CrossRef

Schmahmann JD, Pandya DN (2006) Fiber pathways of the brain. Oxford University Press, New YorkCrossRef

Seghier ML (2013) The angular gyrus: multiple functions and multiple subdivisions. Neuroscientist 19(1):43–61. https://doi.org/10.1177/1073858412440596CrossRef

Sparing R, Thimm M, Hesse MD, Kust J, Karbe H, Fink GR (2009) Bidirectional alterations of interhemispheric parietal balance by non-invasive cortical stimulation. Brain 132(Pt 11):3011–3020. https://doi.org/10.1093/brain/awp154CrossRef

Theaud G, Houde JC, Bore A, Rheault F, Morency F, Descoteaux M (2020) TractoFlow: a robust, efficient and reproducible diffusion mri pipeline leveraging nextflow & singularity. Neuroimage 218:116889. https://doi.org/10.1016/j.neuroimage.2020.116889CrossRef

Thiebaut de Schotten M, Urbanski M, Duffau H, Volle E, Levy R, Dubois B, Bartolomeo P (2005) Direct evidence for a parietal-frontal pathway subserving spatial awareness in humans. Science 309(5744):2226–2228CrossRef

Thiebaut de Schotten M, Dell’Acqua F, Forkel SJ, Simmons A, Vergani F, Murphy DGM, Catani M (2011) A lateralized brain network for visuospatial attention. Nat Neurosci 14(10):1245–1246CrossRef

Vavassori L, Sarubbo S, Petit L (2021) Hodology of the superior longitudinal system of the human brain: a historical perspective, the current controversies, and a proposal. Brain Struct Funct 226(5):1363–1384. https://doi.org/10.1007/s00429-021-02265-0CrossRef

Vigneau M, Beaucousin V, Hervé P-Y, Duffau H, Crivello F, Houde O, Mazoyer B, Tzourio-Mazoyer N (2006) Meta-analyzing left hemisphere language areas: phonology, semantics, and sentence processing. Neuroimage 30(4):1414–1432CrossRef

Wang Y, Fernandez-Miranda JC, Verstynen T, Pathak S, Schneider W, Yeh F-C (2013) Rethinking the role of the middle longitudinal fascicle in language and auditory pathways. Cereb Cortex 23(10):2347–2356. https://doi.org/10.1093/cercor/bhs225CrossRef

Wang X, Pathak S, Stefaneanu L, Yeh FC, Li S, Fernandez-Miranda JC (2016) Subcomponents and connectivity of the superior longitudinal fasciculus in the human brain. Brain Struct Funct 221(4):2075–2092. https://doi.org/10.1007/s00429-015-1028-5CrossRef

Wu Y, Sun D, Wang Y, Wang Y (2016a) Subcomponents and connectivity of the inferior fronto-occipital fasciculus revealed by diffusion spectrum imaging fiber tracking. Front Neuroanat 10:88. https://doi.org/10.3389/fnana.2016.00088CrossRef

Wu Y, Sun D, Wang Y, Wang Y, Wang Y (2016b) Tracing short connections of the temporo-parieto-occipital region in the human brain using diffusion spectrum imaging and fiber dissection. Brain Res 1646:152–159. https://doi.org/10.1016/j.brainres.2016.05.046CrossRef

Xu Y, He Y, Bi Y (2017) A Tri-network Model of Human Semantic Processing. Front Psychol 8:1538. https://doi.org/10.3389/fpsyg.2017.01538CrossRef

Yeatman JD, Weiner KS, Pestilli F, Rokem A, Mezer A, Wandell BA (2014) The vertical occipital fasciculus: a century of controversy resolved by in vivo measurements. Proc Natl Acad Sci U S A 111(48):E5214-5223. https://doi.org/10.1073/pnas.1418503111CrossRef

Yeh FC (2020) Shape analysis of the human association pathways. Neuroimage 223:117329. https://doi.org/10.1016/j.neuroimage.2020.117329CrossRef

Yeterian EH, Pandya DN (1993) Striatal connections of the parietal assoiation cortices in rhesus monkey. JCompNeurol 332:175–197

Zaca D, Corsini F, Rozzanigo U, Dallabona M, Avesani P, Annicchiarico L, Zigiotto L, Faraca G, Chioffi F, Jovicich J, Sarubbo S (2018) Whole-brain network connectivity underlying the human speech articulation as emerged integrating direct electric stimulation, resting state fMRI and tractography. Front Hum Neurosci 12:405. https://doi.org/10.3389/fnhum.2018.00405CrossRef

Zemmoura I, Blanchard E, Raynal PI, Rousselot-Denis C, Destrieux C, Velut S (2016) How Klingler’s dissection permits exploration of brain structural connectivity? An electron microscopy study of human white matter. Brain Struct Funct 221(5):2477–2486. https://doi.org/10.1007/s00429-015-1050-7CrossRef

Title: The structural connectivity of the human angular gyrus as revealed by microdissection and diffusion tractography
Authors: Laurent Petit
Kariem Mahdy Ali
François Rheault
Arnaud Boré
Sandrine Cremona
Francesco Corsini
Alessandro De Benedictis
Maxime Descoteaux
Silvio Sarubbo
Publication date: 22-08-2022
Publisher: Springer Berlin Heidelberg
Published in: Brain Structure and Function / Issue 1/2023
Print ISSN: 1863-2653
Electronic ISSN: 1863-2661
DOI: https://doi.org/10.1007/s00429-022-02551-5

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

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