Brain folding shapes the branching pattern of the middle cerebral artery

Shalóm, Diego; Trevisan, Marcos; Mallela, Arka N.; Núñez, Maximiliano; Goldschmidt, Ezequiel

doi:10.1371/journal.pone.0245167

Cited by 9 publications

(9 citation statements)

References 25 publications

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“…As we have shown before, the formation of the Sylvian fissure follows different principles compared to the development of any other brain fold and that singularity explains why arteries do not cross the Sylvian fissure. ( 20 , 21 , 38 ) Those findings are confirmed by the results of this paper.…”

Section: Discussionsupporting

confidence: 91%

Heterogeneous migration of neuronal progenitors to the insula shapes the human brain

Mallela

Deng²,

Gholipour

et al. 2022

Preprint

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The global geometry of the human cerebrum forms in a highly conserved fashion. Mechanisms that explain individual gyral formation fail to explain both the global configuration of the cerebral lobes and the unique geometry and configuration of the insular gyri. To quantify this, we calculated morphologic data in the insula and other lobes in both adults (N=107 adult patients) and in a fetal brain atlas constructed from in utero brain MRIs of 81 healthy human fetuses (gestational age 21-38 weeks). We find that the insula is morphologically different in adults and that these differences emerge during fetal development. Specifically, the insula exhibits shallower sulci (p<0.0001), less extrinsic curvature (p<0.0001), and less complex surface (p<0.0001) in adults and progressively throughout fetal development. In utero, the insular volume demonstrates logistic growth of an order of magnitude lower than the other lobes (α=0.002 vs. 0.05/0.03/0.04/0.02) and a surface area that grows linearly, in contrast with the exponential growth of the other lobes, resulting in a significantly smaller insula in adults (p<0.0001). We demonstrate that the lenticular nuclei significantly obstruct 60-70% of radial pathways from the ventricular zone (VZ) to the insula compared to the other lobes (p<0.01), forcing an oblique or tangential migration path to the insula in contrast to the direct radial pathway from VZ to all other cortices. To validate this hypothesis, using fetal diffusion tractography, we identify streams of putative insular progenitor cells that originate from the VZ near the pallial-subpallial boundary and migrate tangentially around the lenticular nuclei of the basal ganglia to form the insula. Shape analysis confirms that these streams to the insula are quantitatively different with higher curl (p < 0.001) and elongation (p < 0.001). This alternative mechanism to direct radial migration can explain the altered morphology of the insula, the slow volumetric and surface area growth of the insula, and ultimately how the operculae overgrow the insula and create the global configuration of the human cerebrum.

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Section: Discussionsupporting

confidence: 91%

Heterogeneous migration of neuronal progenitors to the insula shapes the human brain

Mallela

Deng²,

Gholipour

et al. 2022

Preprint

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“…The middle cerebral artery (MCA) enters the Sylvian fissure at the antero-ventral border of the insula—the limen insula—with its branches diverging to the frontal and temporal lobes ( 58 ). It is only after the operculae close over the insula do MCA branches reconverge at the Sylvian fissure late in gestation ( 24 , 59 ). At this point, the MCA is too developed to send branches across the fissure.…”

Section: Discussionmentioning

confidence: 99%

Heterogeneous growth of the insula shapes the human brain

Mallela

Deng

Gholipour

et al. 2023

Proc. Natl. Acad. Sci. U.S.A.

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The human cerebrum consists of a precise and stereotyped arrangement of lobes, primary gyri, and connectivity that underlies human cognition [P. Rakic, Nat. Rev. Neurosci. 10 , 724–735 (2009)]. The development of this arrangement is less clear. Current models explain individual primary gyrification but largely do not account for the global configuration of the cerebral lobes [T. Tallinen, J. Y. Chung, J. S. Biggins, L. Mahadevan, Proc. Natl. Acad. Sci. U.S.A. 111 , 12667–12672 (2014) and D. C. Van Essen, Nature 385 , 313–318 (1997)]. The insula, buried in the depths of the Sylvian fissure, is unique in terms of gyral anatomy and size. Here, we quantitatively show that the insula has unique morphology and location in the cerebrum and that these key differences emerge during fetal development. Finally, we identify quantitative differences in developmental migration patterns to the insula that may underlie these differences. We calculated morphologic data in the insula and other lobes in adults (N = 107) and in an in utero fetal brain atlas (N = 81 healthy fetuses). In utero, the insula grows an order of magnitude slower than the other lobes and demonstrates shallower sulci, less curvature, and less surface complexity both in adults and progressively throughout fetal development. Spherical projection analysis demonstrates that the lenticular nuclei obstruct 60 to 70% of radial pathways from the ventricular zone (VZ) to the insula, forcing a curved migration to the insula in contrast to a direct radial pathway. Using fetal diffusion tractography, we identify radial glial fascicles that originate from the VZ and curve around the lenticular nuclei to form the insula. These results confirm existing models of radial migration to the cortex and illustrate findings that suggest differential insular and cerebral development, laying the groundwork to understand cerebral malformations and insular function and pathologies.

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“…The middle cerebral artery (MCA) emerges from the internal carotid artery (ICA) in the interpeduncular fossa, at the lateral angle of the Willis circle (Almeida et al, 2017). From the carotid bifurcation, MCA runs in the lateral direction to reach the sylvian fissure (Shalom et al, 2021). It runs posterior to the lesser wing of the sphenoid, turns in the sylvian fissure between the temporal and frontal lobes to reach the insular surface (Almeida et al, 2017;Gibo et al, 1981), and divides into two secondary trunks (superior and inferior).…”

Section: Introductionmentioning

confidence: 99%

“…MCA tributaries pass through the medial surface of the opercula of the frontal, parietal, and temporal lobes, then run over the brain surface as cortical branches, supplying the lateral and inferior surfaces of the cerebral hemispheres (Ture et al, 2000). As MCA supplies a large part of the cerebral hemispheres, it is the most exposed vessel during surgical intervention and its acute obstruction can lead to the development of brain infarct in most of the cases (Shalom et al, 2021).…”

Section: Introductionmentioning

confidence: 99%

Variations in branching pattern of middle cerebral artery using CT angiography in South Indian population

Sharma¹,

Verma²,

Adithan³

2023

EJA

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Middle cerebral artery (MCA) variants are rare compared to that of the other two cerebral arteries. Incidence of variations like duplication, fenestration, accessory vessel and early branching ranges from 0.17 to 4%. However, the literature describing MCA variations using CT Angiography (CTA) is limited, so this study was planned to determine the incidence of MCA branching pattern in Indian population using CTA. Datasets of CTA of 578 MCA from 289 patients (180 males and 109 females), with average age of 49.29±16.16 years (range of 11 to 85 years), from a tertiary care hospital were systematically reviewed for variations in branching pattern. Cases involving aneurysms and infarcts were excluded from the study. Four branching patterns of MCA were seen. Pattern I: single trunk in 0.17% (1/578) cases, on left side. Pattern II: early bifurcation in 0.52% (2/578) cases, two cases on right and one on left side. Pattern III: bifurcation, in 97.75%, (565/578) cases, 46.15% (6/13) cases on right and 53.84% (7/13) on left side. Pattern IV: trifurcation, in 1% (6/578), two cases on right and four on left side. Duplicated MCA seen in 0.34% (2/578) cases, both on the right side. The fenestration of MCA seen in 0.17% (1/578), on the left side. No case of accessory MCA was seen. Awareness of these anatomical variations in the branching pattern of MCA is valuable for clinicians and surgeons handling cases of intracranial aneurysms and infarcts. Thus, data from this study would help surgeons minimize errors and provide the best possible outcome to the patients

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Brain folding shapes the branching pattern of the middle cerebral artery

Cited by 9 publications

References 25 publications

Heterogeneous migration of neuronal progenitors to the insula shapes the human brain

Heterogeneous migration of neuronal progenitors to the insula shapes the human brain

Heterogeneous growth of the insula shapes the human brain

Variations in branching pattern of middle cerebral artery using CT angiography in South Indian population

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