Early Path Dominance as a Principle for Neurodevelopment

To understand how brain networks acquire their topological structures during development, we perform a computational study of percolation across human diffusion magnetic resonance imaging for adults (UK Biobank, N =19,380), adolescents (Adolescent Brain Cognitive Development Study, N =15,593) and neonates (Developing Human Connectome Project, N =758), as well as mouse viral tracing (Allen Institute). We perform targeted attack, a systematic unlinking of the network, to analyze its effects on global communication across the network through its giant cluster. We find that brain networks differ from scale-free and small-world structures. Time-reversing the attack computation suggests a mechanism for how brains develop, the validity for which we establish experimentally for targeted attack on increasing white matter tract lengths and densities being invariant to aging and disease. We derive an analytical equation using percolation theory for the fraction of brain regions in the giant cluster as a function of connectivity. Based on a close match between theory and experiment, our results demonstrate that tracts are limited to emanate from regions already in the giant cluster and tracts that appear earliest in neurodevelopment are those that become the longest and densest. Significance As brains develop through neural growth and specialization, what mechanism ensures that new neurons are integrated into a fully connected brain, avoiding “bridges to nowhere”? Here, we study brain structure development from the perspective of percolation, a global measure of communication. Analyzing over 35,000 diffusion MRI scans on human individuals, from newborns to adults, we identify the following rules of brain neurogenesis through percolation theory: earlier tracts become longer and denser while maintaining a giant cluster. This signature, invariant to age or mental health, suggests a fundamental condition for the brain to function as an emergent whole.