Biomechanical models and mechanisms of cellular morphogenesis and cerebral cortical expansion and folding

ElsevierVolume 140, 15 May 2023, Pages 90-104Seminars in Cell & Developmental BiologyAuthor links open overlay panelHighlights•

Mechanical tension mediated by the cytoskeleton plays a key role in many aspects of morphogenesis.

Expansion and folding of cerebral cortex are key to achieving a large cortical surface area while keeping wiring compact.

The Composite Tension Plus (CT+) model invokes 10 distinct mechanisms to account for cortical expansion and folding.

Abstract

Morphogenesis of the nervous system involves a highly complex spatio-temporal pattern of physical forces (mainly tension and pressure) acting on cells and tissues that are pliable but have an intricately organized cytoskeletal infrastructure. This review begins by covering basic principles of biomechanics and the core cytoskeletal toolkit used to regulate the shapes of cells and tissues during embryogenesis and neural development. It illustrates how the principle of ‘tensegrity’ provides a useful conceptual framework for understanding how cells dynamically respond to forces that are generated internally or applied externally. The latter part of the review builds on this foundation in considering the development of mammalian cerebral cortex. The main focus is on cortical expansion and folding – processes that take place over an extended period of prenatal and postnatal development. Cortical expansion and folding are likely to involve many complementary mechanisms, some related to regulating cell proliferation and migration and others related to specific types and patterns of mechanical tension and pressure. Three distinct multi-mechanism models are evaluated in relation to a set of 18 key experimental observations and findings. The Composite Tension Plus (CT+) model is introduced as an updated version of a previous multi-component Differential Expansion Sandwich Plus (DES+) model (Van Essen, 2020); the new CT+ model includes 10 distinct mechanisms and has the greatest explanatory power among published models to date. Much needs to be done in order to validate specific mechanistic components and to assess their relative importance in different species, and important directions for future research are suggested.

AbbreviationsCMS

Cerebellar Multi-layer Sandwich

CT+

Composite Tension Plus

DES+

Differential Expansion Sandwich Plus

DTE

differential tangential expansion

OCL

outer cortical and leptomeningeal

TBM

tension-based morphogenesis

Keywords

Tension

Cytoskeleton

Embryogenesis

Gyrification

© 2022 The Author. Published by Elsevier Ltd.

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