Different Principles Govern Different Scales of Brain Folding

Mallela, Arka N.; Deng, Hansen; Bush, Alan; Goldschmidt, Ezequiel

doi:10.1093/cercor/bhaa086

Cited by 9 publications

(17 citation statements)

References 58 publications

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“…Bush et al previously suggested that the Sylvian fissure appears by convergence of the anterior and posterior poles of the embryonic telencephalon and proposed a convergence index for the adult brain, calculated as the Euclidean distance/transcortical distance ratio, that returns its highest values around the fissure [20]. Recently, Mallela et al showed that, contrary to intralobar sulci, the subarachnoid space in the Sylvian fissure contracts as the fissure grows; the edges of this singular fold do not bend, they converge [21]. Here, we show that the distance between the frontal and temporal lobes diminishes with gestational time as does the volume of the Sylvian fissure as a result of represents the volumetric growth of the frontal lobe, central core, temporal and parietal lobes respectively.…”

Section: Discussionmentioning

confidence: 99%

“…The Symmetric Normalization (SyN) algorithm in the Advanced Normalization Tools (ANTs) package, that registers weekly image pairs (Week 24 to 25, etc.) was used to quantify week-to-week changes as described by Mallela et al [21] The original segmentations in the Gholipour atlas [22] was used as the ground truth to validate the accuracy of our registration.…”

Section: Anatomical Dissectionsmentioning

confidence: 99%

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Brain folding shapes the branching pattern of the middle cerebral artery

et al. 2021

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The folds of the brain offer a particular challenge for the subarachnoid vascular grid. The primitive blood vessels that occupy this space, when the brain is flat, have to adapt to an everchanging geometry while constructing an efficient network. Surprisingly, the result is a non-redundant arterial system easily challenged by acute occlusions. Here, we generalize the optimal network building principles of a flat surface growing into a folded configuration and generate an ideal middle cerebral artery (MCA) configuration that can be directly compared with the normal brain anatomy. We then describe how the Sylvian fissure (the fold in which the MCA is buried) is formed during development and use our findings to account for the differences between the ideal and the actual shaping pattern of the MCA. Our results reveal that folding dynamics condition the development of arterial anastomosis yielding a network without loops and poor response to acute occlusions.

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Section: Discussionmentioning

confidence: 99%

Section: Anatomical Dissectionsmentioning

confidence: 99%

Brain folding shapes the branching pattern of the middle cerebral artery

et al. 2021

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“…The insula is also the focal point around which the Sylvian fissure, and accordingly the operculae of the frontal, parietal, and temporal lobes, are arranged. [18][19][20] Here we show that the distinct C-shape of the cerebrum is a function of these operculae closing over the insula during fetal development. Accordingly, understanding the determinants of how the other lobes overgrow the insula to close to Sylvian fissure is paramount to understanding the global configuration of cerebrum.…”

Section: Introductionmentioning

confidence: 56%

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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“…Since 13 gw, cells from the subpallial neurons migrate into the insular cortex along the radial glial fascicle reaching the final configuration before birth ( 16 ). Mallela et al ( 17 , 18 ) found different gene expressions from the opercula to the insula resulting in the highest proliferation of the former allowing their growth over the insula. This different origin might explain the fact that the tracts that developed later connecting frontal, temporal, and parietooccipital regions ‘avoid crossing the insula', thus being located ventral or dorsal to it, and in some cases wrapping around it with specific curved patterns ( 19 – 21 ).…”

Section: Discussionmentioning

confidence: 99%

“…Since 13 gw, cells from the subpallial neurons migrate into the insular cortex along the radial glial fascicle reaching the final configuration before birth (16). Mallela et al (17,18) found different gene expressions from the opercula to the insula resulting in the highest proliferation of the former allowing their growth over the insula. This different origin might explain the fact that the tracts that developed later FIGURE 8 | An 18-year-old left-handed girl presented with medically refractory epilepsy that was symptomatic since the age of 3 years due to a perinatal stroke in the territory of the left middle cerebral artery.…”

Section: Figure 5 | (A)mentioning

confidence: 99%

Cadaveric White Matter Dissection Study of the Telencephalic Flexure: Surgical Implications

et al. 2022

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Neurosurgery has traditionally been overtly focused on the study of anatomy and functions of cortical areas with microsurgical techniques aimed at preserving eloquent cortices. In the last two decades, there has been ever-increasing data emerging from advances in neuroimaging (principally diffusion tensor imaging) and clinical studies (principally from awake surgeries) that point to the important contribution of white matter tracts (WMT) that influence neurological function as part of a brain network. Major scientific consortiums worldwide, currently working on this human brain connectome, are providing evidence that is dramatically altering the manner in which we view neurosurgical procedures. The development of the telencephalic flexure, a major landmark during the human embryogenesis of the central nervous system (CNS), severely affects the cortical/subcortical anatomy in and around the sylvian fissure and thus the different interacting brain networks. Indeed, the telencephalic flexure modifies the anatomy of the human brain with the more posterior areas becoming ventral and lateral and associative fibers connecting the anterior areas with the previous posterior ones follow the flexure, thus becoming semicircular. In these areas, the projection, association, and commissural fibers intermingle with some WMT remaining curved and others longitudinal. Essentially the ultimate shape and location of these tracts are determined by the development of the telencephalic flexure. Five adult human brains were dissected (medial to lateral and lateral to medial) with a view to describing this intricate anatomy. To better understand the 3D orientation of the WMT of the region we have correlated the cadaveric data with the anatomy presented in the literature of the flexure during human neuro-embryogenesis in addition to cross-species comparisons of the flexure. The precise definition of the connectome of the telencephalic flexure is primordial during glioma surgery and for disconnective epilepsy surgery in this region.

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Different Principles Govern Different Scales of Brain Folding

Cited by 9 publications

References 58 publications

Brain folding shapes the branching pattern of the middle cerebral artery

Brain folding shapes the branching pattern of the middle cerebral artery

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

Cadaveric White Matter Dissection Study of the Telencephalic Flexure: Surgical Implications

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