  Osteocytes and their cell processes reside in a large, interconnected network
of voids pervading the mineralized bone matrix of most vertebrates. This
osteocyte lacuno-canalicular network (OLCN) is believed to play important roles
in mechanosensing, mineral homeostasis, and for the mechanical properties of
bone. While the extracellular matrix structure of bone is extensively studied
on ultrastructural and macroscopic scales, there is a lack of quantitative
knowledge on how the cellular network is organized. Using a recently introduced
imaging and quantification approach, we analyze the OLCN in different bone
types from mouse and sheep that exhibit different degrees of structural
organization not only of the cell network but also of the fibrous matrix
deposited by the cells. We define a number of robust, quantitative measures
that are derived from the theory of complex networks. These measures enable us
to gain insights into how efficient the network is organized with regard to
intercellular transport and communication. Our analysis shows that the cell
network in regularly organized, slow-growing bone tissue from sheep is less
connected, but more efficiently organized compared to irregular and
fast-growing bone tissue from mice. On the level of statistical topological
properties (edges per node, edge length and degree distribution), both network
types are indistinguishable, highlighting that despite pronounced differences
at the tissue level, the topological architecture of the osteocyte canalicular
network at the subcellular level may be independent of species and bone type.
Our results suggest a universal mechanism underlying the self-organization of
individual cells into a large, interconnected network during bone formation and
mineralization.
