Differential Tangential Expansion as a Mechanism for Cortical Gyrification

Abstract

Gyrification, the developmental buckling of the cortex, is not a random process—the forces that mediate expansion do so in such a way as to generate consistent patterns of folds across individuals and even species. Although the origin of these forces is unknown, some theories have suggested that they may be related to external cortical factors such as axonal tension. Here, we investigate an alternative hypothesis, namely, whether the differential tangential expansion of the cortex alone can account for the degree and pattern-specificity of gyrification. Using intrinsic curvature as a measure of differential expansion, we initially explored whether this parameter and the local gyrification index (used to quantify the degree of gyrification) varied in a regional-specific pattern across the cortical surface in a manner that was replicable across independent datasets of neurotypicals. Having confirmed this consistency, we further demonstrated that within each dataset, the degree of intrinsic curvature of the cortex was predictive of the degree of cortical folding at a global and regional level. We conclude that differential expansion is a plausible primary mechanism for gyrification, and propose that this perspective offers a compelling mechanistic account of the co-localization of cytoarchitecture and cortical folds.

Intrinsic gray-matter connectivity of the brain in adults with autism spectrum disorder

“…As assessed here, wiring costs do not represent the actual length of axonal connections but are indicative of the intrinsic "wiring potential" of a brain region (i.e., reduced costs may facilitate the formation of intrinsic cortico-cortical circuits). As such, intrinsic measures reflect the actual intrinsic architecture of the brain, which may differ across different regions and may also include different neural components characterizing the lateral (i.e., horizontal) architecture of the cortex (30,32).…”

“…An uneven distribution of surface units (e.g., minicolumns) most likely arises as a consequence of nonuniform surface expansion during development, which is commensurate with a differential decrease in neuronal density and an increase in intercellular spacing (25,32). For example, it has previously been demonstrated that some regions expand earlier and to a higher extent than others in typical brain development, and such differential expansion will also affect the distances between regions on the cortical surface (e.g., ref.…”

The mechanical control of nervous system development

“…In this hypothesis, the tangential expansion of cortical regions, which is driven by the local augmented proliferation of cells and changes in cell sizes and shapes, is assumed to be the driving force for cerebral convolutional development (Mares and Lodin, 1970;Caviness, 1975;Smart and McSherry, 1986;Ronan et al, 2013). Thus, forces driving brain folding are predominantly intracortical.…”

Universality in human cortical folding in health and disease

“…The mechanisms that drive gyrification have been a matter of intense research interest lately (1)(2)(3)(4), with a number of proposals being put forward to explain it. Most such studies have focused on human cortices, using detailed MRI data to postulate folding as driven by the [possibly differential (5) or multilayered (6)] expansion of the cortical surface. In contrast, we have recently proposed a model (7), in which folding is a consequence of the dynamics of surface expansion and self-avoidance coupled with a negative tension term.…”