Segregation of the Brain into Gray and White Matter: A Design Minimizing Conduction Delays

Abstract

A ubiquitous feature of the vertebrate anatomy is the segregation of the brain into white and gray matter. Assuming that evolution maximized brain functionality, what is the reason for such segregation? To answer this question, we posit that brain functionality requires high interconnectivity and short conduction delays. Based on this assumption we searched for the optimal brain architecture by comparing different candidate designs. We found that the optimal design depends on the number of neurons, interneuronal connectivity, and axon diameter. In particular, the requirement to connect neurons with many fast axons drives the segregation of the brain into white and gray matter. These results provide a possible explanation for the structure of various regions of the vertebrate brain, such as the mammalian neocortex and neostriatum, the avian telencephalon, and the spinal cord. Vertebrate brains generally contain two kinds of tissue: gray matter and white matter. Gray matter contains local networks of neurons that are wired by dendrites and mostly nonmyelinated local axons. White matter contains long-range axons that implement global communication via often myelinated axons. What is the evolutionary advantage of segregating the brain into white and gray matter rather than intermixing them? In this study, the authors postulate that brain functionality benefits from high synaptic connectivity and short conduction delays—the time required for a signal from one neuron soma to reach another. Using this postulate, they show quantitatively that the existence of many fast, long-range axons drives the segregation of the brain into gray and white matter. The theory not only provides a possible explanation for the structure of various brain regions such as cerebral cortex, neostriatum, and spinal cord, but also makes several testable predictions such as the scaling estimate of the cortical thickness.