Human cortical networks trade communication efficiency for computational reliability

Abstract

Brains are often described as cost-efficient communication networks that optimally balance long-connection costs against fast communication. Inspired by the “use it or lose it” principle, we present a game-theoretic model of self-organizing neural units showing the brain is suboptimal in both regards. Regional competition for connectivity under propagative dynamics yields networks resembling the human cortex yet more efficient and economical. In addition, using a reservoir computing framework, we find comparable information processing capacity, but synthetic optimal communication networks show lower computational reliability. Last, virtual lesions reveal why these networks are fragile: To optimize communication, they funnel information through a spatially clustered “oligarchy” of transmodal hubs. The human brain instead uses a distributed “rich-club” backbone that better resists targeted attacks, despite higher wiring costs and less efficient communication. Cortical networks thus trade both cost and efficiency for reliable computation, highlighting computational reliability as an overlooked and perhaps even more prominent driver of brain connectivity than wiring cost or communication efficiency.