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Osteocytes and their cell processes reside in a large, interconnected networkof voids pervading the mineralized bone matrix of most vertebrates. Thisosteocyte lacuno-canalicular network (OLCN) is believed to play important rolesin mechanosensing, mineral homeostasis, and for the mechanical properties ofbone. While the extracellular matrix structure of bone is extensively studiedon ultrastructural and macroscopic scales, there is a lack of quantitativeknowledge on how the cellular network is organized. Using a recently introducedimaging and quantification approach, we analyze the OLCN in different bonetypes from mouse and sheep that exhibit different degrees of structuralorganization not only of the cell network but also of the fibrous matrixdeposited by the cells. We define a number of robust, quantitative measuresthat are derived from the theory of complex networks. These measures enable usto gain insights into how efficient the network is organized with regard tointercellular transport and communication. Our analysis shows that the cellnetwork in regularly organized, slow-growing bone tissue from sheep is lessconnected, but more efficiently organized compared to irregular andfast-growing bone tissue from mice. On the level of statistical topologicalproperties (edges per node, edge length and degree distribution), both networktypes are indistinguishable, highlighting that despite pronounced differencesat the tissue level, the topological architecture of the osteocyte canalicularnetwork at the subcellular level may be independent of species and bone type.Our results suggest a universal mechanism underlying the self-organization ofindividual cells into a large, interconnected network during bone formation andmineralization.

The Small World of Osteocytes: Connectomics of the Lacuno-Canalicular Network in Bone