Mechanical morphogenesis and the development of neocortical organisation

Foubet, Ophélie; Toro, Roberto

doi:10.1101/021311

Cited by 6 publications

(4 citation statements)

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“…We thus suspect that yielding constantly occurs during V. cholerae biofilm growth. More generally, reorganization and yielding of growing biological materials are commonly observed during morphogenesis, for example in plants [60], fruit flies [61,62] and brain tissues [63]. Thus, the effects of viscoelasticity [64] and elastoplasticity (Figs.…”

Section: Discussionmentioning

confidence: 99%

Nonuniform growth and surface friction determine bacterial biofilm morphology on soft substrates

Fei

Sheng

Yan

et al. 2020

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

108

115

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During development, organisms acquire three-dimensional shapes with important physiological consequences. While the basic mechanisms underlying morphogenesis are known in eukaryotes, it is often difficult to manipulate them in vivo. To circumvent this issue, here we present a study of developing Vibrio cholerae biofilms grown on agar substrates in which the spatiotemporal morphological patterns were altered by varying the agar concentration. Expanding biofilms are initially flat, but later experience a mechanical instability and become wrinkled. Whereas the peripheral region develops ordered radial stripes, the central region acquires a zigzag herringbone-like wrinkle pattern. Depending on the agar concentration, the wrinkles initially appear either in the peripheral region and propagate inward (low agar concentration) or in the central region and propagate outward (high agar concentration). To understand these experimental observations, we developed a model that considers diffusion of nutrients and their uptake by bacteria, bacterial growth/biofilm matrix production, mechanical deformation of both the biofilm and the agar, and the friction between them. Our model demonstrates that depletion of nutrients beneath the central region of the biofilm results in radially-dependent growth profiles, which in turn, produce anisotropic stresses that dictate the morphology of wrinkles. Furthermore, we predict that increasing surface friction (agar concentration) reduces stress anisotropy and shifts the location of the maximum compressive stress, where the wrinkling instability first occurs, toward the center of the biofilm, in agreement with our experimental observations. Our results are broadly applicable to bacterial biofilms with similar morphologies and also provide insight into how other bacterial biofilms form distinct wrinkle patterns.The intricate shapes of organisms are determined by the spatiotemporal patterns of growth as well as the mechanical properties of their underlying biological components [1-3]. Three-dimensional (3D) shape transformations in developing organisms often arise via differential growth of connected tissues [1, 4]. Such asymmetric growth patterns generate compressive stresses within the faster growing tissues, which may cause mechanical instabilities [5][6][7]. Growth-induced mechanical instabilities drive the formation of many convoluted morphologies, such as the gyrification of brains [2, 8, 9], the vilification and looping of guts [10, 11], and the branching of lungs [12] as well as 3D structures of synthetic systems with patterned swelling [5,[13][14][15][16].Biofilms, which are surface-associated bacterial communities encapsulated by a self-produced extracellular matrix [17, 18], also display a variety of 3D developmental morphologies ranging from radial stripes, to concentric rings, to disordered labyrinth and herringbone patterns [19][20][21][22][23]. In the case of Vibrio cholerae, a model * wingreen@princeton.edu † andrej@princeton.edu biofilm former, quantitative imaging revealed a 3...

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Section: Discussionmentioning

confidence: 99%

Nonuniform growth and surface friction determine bacterial biofilm morphology on soft substrates

Fei

Sheng

Yan

et al. 2020

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

108

115

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“…Cortical folding is a very complex process, involving factors at different scales; see (Zilles et al, 2013 ; Ronan and Fletcher, 2015 ; Borrell, 2018 ; Kroenke and Bayly, 2018 ; Foubet et al, 2019 ) for recent reviews on the phylogenetic, cellular and mechanical factors of the cortical folding process. Briefly, several intermingled factors contribute to the fetal processes that influence the shape of the cerebral cortex, including cortical growth (Kuida et al, 1996 ; Haydar et al, 1999 ; Chenn and Walsh, 2002 ; Toro and Burnod, 2005 ), differential expansion of superior and inferior cortical layers (Richmann et al, 1975 ; Kriegstein et al, 2006 ), apoptosis or programmed cell death (Haydar et al, 1999 ), differential growth of the cortical mantle relatively to the underlying white matter (Tallinen et al, 2016 ), transitory compartments such as the subplate (Rana et al, 2019 ), differential neuropil developments (Llinares-Benadero and Borrell, 2019 ; Mangin et al, 2019 ), mechanical constraints (Foubet et al, 2019 ) along with differential tangential expansion (Ronan et al, 2013 ) induced by a genetics-based protomap and/or structural connectivity through axonal tension forces (Van Essen, 1997 , 2020 ).…”

Section: Cerebral Cortex Sulcationmentioning

confidence: 99%

Towards Deciphering the Fetal Foundation of Normal Cognition and Cognitive Symptoms From Sulcation of the Cortex

et al. 2021

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Growing evidence supports that prenatal processes play an important role for cognitive ability in normal and clinical conditions. In this context, several neuroimaging studies searched for features in postnatal life that could serve as a proxy for earlier developmental events. A very interesting candidate is the sulcal, or sulco-gyral, patterns, macroscopic features of the cortex anatomy related to the fold topology—e.g., continuous vs. interrupted/broken fold, present vs. absent fold-or their spatial organization. Indeed, as opposed to quantitative features of the cortical sheet (e.g., thickness, surface area or curvature) taking decades to reach the levels measured in adult, the qualitative sulcal patterns are mainly determined before birth and stable across the lifespan. The sulcal patterns therefore offer a window on the fetal constraints on specific brain areas on cognitive abilities and clinical symptoms that manifest later in life. After a global review of the cerebral cortex sulcation, its mechanisms, its ontogenesis along with methodological issues on how to measure the sulcal patterns, we present a selection of studies illustrating that analysis of the sulcal patterns can provide information on prenatal dispositions to cognition (with a focus on cognitive control and academic abilities) and cognitive symptoms (with a focus on schizophrenia and bipolar disorders). Finally, perspectives of sulcal studies are discussed.

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“…Many aspects of the organisation, development and evolution of the cerebral and cerebellar cortex are, however, very different. It is interesting then to compare folding in both structures as a first step towards understanding how the mechanics of folding could influence the organisation in these two different types of tissue (Franze 2013, Kroenke and Bayly 2018, Foubet et al 2019, Heuer and Toro 2019).…”

Section: Introductionmentioning

confidence: 99%

“…The process leading to folding in both the cerebrum and the cerebellum is likely to be a mechanical instability (buckling) triggered by the growth of the external layers on top of the elastic core (Toro and Burnod 2005, Tallinen et al 2014, Foubet et al 2019, Heuer and Toro 2019, Lawton et al 2019, Llinares-Benadero and Borrell 2019, Van Essen 2020). However, while the folds of the cerebral cortex seem to be able to take any orientation (especially in large gyrencephalic brains such as those of humans or cetaceans), the cerebellar folia are almost completely parallel to one another, accordion-like, forming the same characteristic type of tree-like structures from mice, to humans and whales (Leto et al 2016).…”

Section: Introductionmentioning

confidence: 99%

Diversity and evolution of cerebellar folding in mammals

Heuer

Traut

Sousa

et al. 2022

Preprint

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The process of brain folding is thought to play an important role in the development and organisation of the cerebrum and the cerebellum. The study of cerebellar folding is challenging due to the small size and abundance of its folia. In consequence, little is known about its anatomical diversity and evolution. We constituted an open collection of histological data from 56 mammalian species and manually segmented the cerebrum and the cerebellum. We developed methods to measure the geometry of cerebellar folia and to estimate the thickness of the molecular layer. We used phylogenetic comparative methods to study the diversity and evolution of cerebellar folding and its relationship with the anatomy of the cerebrum. Our results show that the evolution of cerebellar and cerebral anatomy follows a stabilising selection process. Ancestral estimations indicate that size and folding of the cerebrum and cerebellum increase and decrease concertedly through evolution. Our analyses confirm the strong correlation between cerebral and cerebellar volumes across species, and show that large cerebella are disproportionately more folded than smaller ones. Compared with the extreme variations in cerebellar surface area, folial wavelength and molecular layer thickness varied only slightly, showing a much smaller increase in the larger cerebella. These findings provide new insight into the diversity and evolution of cerebellar folding and its potential influence on brain organisation across species.

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Mechanical morphogenesis and the development of neocortical organisation

Cited by 6 publications

References 83 publications

Nonuniform growth and surface friction determine bacterial biofilm morphology on soft substrates

Nonuniform growth and surface friction determine bacterial biofilm morphology on soft substrates

Towards Deciphering the Fetal Foundation of Normal Cognition and Cognitive Symptoms From Sulcation of the Cortex

Diversity and evolution of cerebellar folding in mammals

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