Human brain dynamics are shaped by rare long-range connections over and above cortical geometry

Abstract

A fundamental topological principle is that the container always shapes the content. Inneuroscience, this translates into how the brain anatomy shapes brain dynamics. Fromneuroanatomy, the topology of the mammalian brain can be approximated by localconnectivity, accurately described by an exponential distance rule (EDR). The compact,folded geometry of the cortex is shaped by this local connectivity, and the geometricharmonic modes can reconstruct much of the functional dynamics. However, this ignoresthe fundamental role of the rare long-range(LR) cortical connections, crucial for improvinginformation processing in the mammalian brain, but not captured by local corticalfolding and geometry. Here, we show the superiority of harmonic modes combining rareLR connectivity with EDR (EDR+LR) in capturing functional dynamics (specificallyLR functional connectivity and task-evokedbrain activity) compared to geometry andEDR representations. Importantly, the orchestration of dynamics is carried out by amore efficient manifold made up of a low number of fundamental EDR+LR modes.Our results show the importance of rare LR connectivity for capturing the complexityof functional brain activity through a low-dimensionalmanifold shaped by fundamentalEDR+LR modes.