Geometric constraints on the architecture of mammalian cortical connectomes.

Abstract

The intricate network of axonal fibers forming the mammalian cortical connectome exhibits a complex topology, being neither completely regular nor random. It also has a characteristic topography in which distinct regions have specific connectivity profiles. How such properties arise remains a mystery. Here, we formulate a simple analytical model derived from neural field theory that prioritizes physical constraints on connectome architecture, assuming that connectivity is preferentially concentrated between cortical locations that facilitate the excitation of resonant geometric modes of the cortex. Our model outperforms existing approaches in reproducing topological and topographical properties of cortical connectomes mapped via either non-invasive diffusion magnetic resonance imaging (MRI) or invasive viral tract tracing at spatial scales spanning multiple orders of magnitude in humans, chimpanzees, macaques, marmosets, and mice. Our findings point to a fundamental role of geometry in shaping the multiscale architecture of cortical connectomes that has been conserved across 90 million years of evolution.