Spatial convergence of distant cortical regions during folding explains why arteries do not cross the sylvian fissure

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OBJECTIVE

Cortical folding places regions that are separated by a large distance along the cortical surface in close proximity. This process is not homogeneous; regions such as the insular opercula have a much higher cortical surface distance (CSD) to euclidean distance (ED) than others. Here the authors explore the hypothesis that in the folded brain the CSD, and not the ED, determines regions of common irrigation, because this measure corresponds more closely with the distance along the prefolded brain, where the subarachnoid arterial vascular network starts forming.

METHODS

The authors defined a convergence index that compared the ED to the CSD and applied it to the cortical surface reconstruction of an average brain. They then compared cortical convergence to the irrigation patterns of major sulci and fissures of the brain, by assessing whether these structures were crossed or not crossed by arterial vessels in 20 fixed hemispheres.

RESULTS

The regions of highest convergence (top 1%) were clustered around the sylvian fissure, which is the only brain depression with high convergence values along its edges. Arterial crossings were commonly observed in every major sulcus of the brain, with the exception of the sylvian fissure, constituting a highly significant difference (p < 10−4).

CONCLUSIONS

Arteries do not cross regions of high convergence. In the adult brain the CSD, rather than the ED, predicts the regional irrigation pattern. The distant origin of the frontal and temporal lobes creates a region of high cortical convergence, which explains why arteries do not cross the sylvian fissure.

ABBREVIATIONS ACA = anterior cerebral artery; CSD = cortical surface distance; ED = euclidean distance; MCA = middle cerebral artery; PCA = posterior cerebral artery; PMA = postmenstrual age.
Article Information

Contributor Notes

Correspondence Ezequiel Goldschmidt: University of Pittsburgh School of Medicine, University of Pittsburgh Medical Center, UPMC Presbyterian Hospital, Pittsburgh, PA. goldschmidted@upmc.edu.INCLUDE WHEN CITING Published online November 22, 2019; DOI: 10.3171/2019.9.JNS192151.Disclosures Dr. Friedlander is a consultant for NeuBase Therapeutics and DiFusion, Inc., and he also has direct stock ownership in both companies.
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References
  • 1

    Arnold WHKleiner A: 3D reconstruction of the cardiovascular and central nervous system of a human embryo Carnegie-stage 15—case report. Ann Anat 186:1331392004

    • Search Google Scholar
    • Export Citation
  • 2

    Bayly PVTaber LAKroenke CD: Mechanical forces in cerebral cortical folding: a review of measurements and models. J Mech Behav Biomed Mater 29:5685812014

    • Search Google Scholar
    • Export Citation
  • 3

    Campero AAjler PEmmerich JGoldschmidt EMartins CRhoton A: Brain sulci and gyri: a practical anatomical review. J Clin Neurosci 21:221922252014

    • Search Google Scholar
    • Export Citation
  • 4

    Campero AAjler PGarategui LGoldschmidt EMartins CRhoton A: Pterional transsylvian-transinsular approach in three cavernomas of the left anterior mesiotemporal region. Clin Neurol Neurosurg 130:14192015

    • Search Google Scholar
    • Export Citation
  • 5

    Campero AAjler PGoldschmidt ERica CMartins CRhoton A: Three-step anterolateral approaches to the skull base. J Clin Neurosci 21:180318072014

    • Search Google Scholar
    • Export Citation
  • 6

    de Juan Romero CBorrell V: Genetic maps and patterns of cerebral cortex folding. Curr Opin Cell Biol 49:31372017

  • 7

    Fischl BSereno MIDale AM: Cortical surface-based analysis. II: Inflation, flattening, and a surface-based coordinate system. Neuroimage 9:1952071999

    • Search Google Scholar
    • Export Citation
  • 8

    Gibo HCarver CCRhoton AL JrLenkey CMitchell RJ: Microsurgical anatomy of the middle cerebral artery. J Neurosurg 54:1511691981

    • Search Google Scholar
    • Export Citation
  • 9

    Lasjaunias Pter Brugge KGBerenstein A: Surgical Neuroangiography. Berlin: Springer2006

  • 10

    Mall FP: On the development of the blood-vessels of the brain in the human embryo. Am J Anat 4:1181905

  • 11

    Mazziotta JCToga AWEvans AFox PLancaster J: A probabilistic atlas of the human brain: theory and rationale for its development. Neuroimage 2:891011995

    • Search Google Scholar
    • Export Citation
  • 12

    McHugh ML: The chi-square test of independence. Biochem Med (Zagreb) 23:1431492013

  • 13

    Menshawi KMohr JPGutierrez J: A functional perspective on the embryology and anatomy of the cerebral blood supply. J Stroke 17:1441582015

    • Search Google Scholar
    • Export Citation
  • 14

    Padget DH: The development of the cranial arteries in the human embryo in Contributions to EmbryologyVol 32No 212. Washington, DC: Carnegie Institution of Washington1948

    • Search Google Scholar
    • Export Citation
  • 15

    Raybaud C: Normal and abnormal embryology and development of the intracranial vascular system. Neurosurg Clin N Am 21:3994262010

  • 16

    Sarnat HBFlores-Sarnat L: Telencephalic flexure and malformations of the lateral cerebral (Sylvian) fissure. Pediatr Neurol 63:23382016

    • Search Google Scholar
    • Export Citation
  • 17

    Schaer MCuadra MBTamarit LLazeyras FEliez SThiran JP: A surface-based approach to quantify local cortical gyrification. IEEE Trans Med Imaging 27:1611702008

    • Search Google Scholar
    • Export Citation
  • 18

    Serag AAljabar PBall GCounsell SJBoardman JPRutherford MA: Construction of a consistent high-definition spatio-temporal atlas of the developing brain using adaptive kernel regression. Neuroimage 59:225522652012

    • Search Google Scholar
    • Export Citation
  • 19

    Stefani MASchneider FLMarrone ACSeverino AGJackowski APWallace MC: Anatomic variations of anterior cerebral artery cortical branches. Clin Anat 13:2312362000

    • Search Google Scholar
    • Export Citation
  • 20

    Streeter GL: The development of the venous sinuses of the dura mater in the human embryo. Am J Anat 18:1451781915

  • 21

    Su SWhite TSchmidt MKao CYSapiro G: Geometric computation of human gyrification indexes from magnetic resonance images. Hum Brain Mapp 34:123012442013

    • Search Google Scholar
    • Export Citation
  • 22

    Tallinen TBiggins JS: Mechanics of invagination and folding: hybridized instabilities when one soft tissue grows on another. Phys Rev E Stat Nonlin Soft Matter Phys 92:0227202015

    • Search Google Scholar
    • Export Citation
  • 23

    Tallinen TChung JYBiggins JSMahadevan L: Gyrification from constrained cortical expansion. Proc Natl Acad Sci U S A 111:12667126722014

    • Search Google Scholar
    • Export Citation
  • 24

    Türe UYaşargil DCHAl-Mefty OYaşargil MG: Topographic anatomy of the insular region. J Neurosurg 90:7207331999

  • 25

    Vilela P: Cranial vessel embryology and imaging anatomy in Barkhof FJager RThurnher M (eds): Clinical Neuroradiology. Cham: Springer2019 pp 142

    • Search Google Scholar
    • Export Citation
  • 26

    Wang DBuckner RLFox MDHolt DJHolmes AJStoecklein S: Parcellating cortical functional networks in individuals. Nat Neurosci 18:185318602015

    • Search Google Scholar
    • Export Citation
  • 27

    Warkany JLemire RJ: Arteriovenous malformations of the brain: a teratologic challenge. Teratology 29:3333531984

  • 28

    Wen HTRhoton AL Jrde Oliveira ECastro LHMFigueiredo EGTeixeira MJ: Microsurgical anatomy of the temporal lobe: part 2—sylvian fissure region and its clinical application. Neurosurgery 65 (6 Suppl):1362009

    • Search Google Scholar
    • Export Citation
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