Buckling without bending morphogenesis: nonlinearities, spatial confinement, and branching hierarchies

Abstract

During morphogenesis, a featureless convex cerebellum develops folds. As it does so, the cortex thickness is thinnest at the crest (gyri) and thickest at the trough (sulci) of the folds. This observation cannot be simply explained by elastic theories of buckling. A recent minimal model explained this phenomenon by modeling the developing cortex as a growing fluid under the constraints of radially spanning elastic fibers, a plia membrane and a nongrowing sub-cortex (Engstrom et al 2019 Phys. Rev. X 8 041053). In this minimal buckling without bending morphogenesis (BWBM) model, the elastic fibers were assumed to act linearly with strain. Here, we explore how nonlinear elasticity influences shape development within BWBM. The nonlinear elasticity generates a quadratic nonlinearity in the differential equation governing the system's shape and leads to sharper troughs and wider crests, which is an identifying characteristic of cerebellar folds at later stages in development. As developing organs are typically not in isolation, we also explore the effects of steric confinement, and observe flattening of the crests. Finally, as a paradigmatic example, we propose a hierarchical version of BWBM from which a novel mechanism of branching morphogenesis naturally emerges to qualitatively predict later stages of the morphology of the developing cerebellum.