Abstract
Continual bone apposition at the cranial sutures provides the unique opportunity to understand how bone is built. Bone harvested from 16-week-old Sprague Dawley rat calvaria was either (i) deproteinised to isolate the inorganic phase (i.e., bone mineral) for secondary electron scanning electron microscopy or (ii) resin embedded for X-ray micro-computed tomography, backscattered electron scanning electron microscopy, and micro-Raman spectroscopy. Interdigitated finger-like projections form the interface between frontal and parietal bones. Viewed from the surface, bone mineral at the mineralisation front is comprised of nanoscale mineral platelets arranged into discrete, ~0.6–3.5 μm high and ~0.2–1.5 μm wide, marquise-shaped motifs that gradually evolve into a continuous interwoven mesh of mineralised bundles. Marquise-shaped motifs also contribute to the burial of osteoblastic–osteocytes by contributing to the roof over the lacunae. In cross-section, apices of the finger-like projections resemble islands of mineralised tissue, where new bone apposition at the surface is evident as low mineral density areas, while the marquise-shaped motifs appear as near-equiaxed assemblies of mineral platelets. Carbonated apatite content is higher towards the internal surface of the cranial vault. Up to 4 μm from the bone surface, strong Amide III, Pro, Hyp, and Phe signals, distinct PO43− bands, but negligible CO32– signal indicate recent bone formation and/or delayed maturation of the mineral. We show, for the first time, that the extracellular matrix of bone is assembled into micrometre-sized units, revealing a superstructure above the mineralised collagen fibril level, which has significant implications for function and mechanical competence of bone.
Highlights
The neurocranium comprises of flat bones that protect the brain from high-impact loads (Jung et al, 2018)
During intramembranous bone formation, the advancing cranial bone fronts invade the mesenchymal tissue, dividing it to an ectoperiosteum and the dura mater until the opposing bone fronts are separated by only narrow bands of mesenchymal tissue that forms the cranial sutures (Opperman, 2000)
Cranial bones remain mechanically competent even at low strain levels in contrast to load-bearing long bones where bone formation and maintenance of bone quality is facilitated by a homeostatic feedback mechanism, where low levels of stress would lead to disuse osteopenia (Turner, 1991; Rawlinson et al, 2009)
Summary
The neurocranium comprises of flat bones that protect the brain from high-impact loads (Jung et al, 2018). Cranial bones remain mechanically competent even at low strain levels in contrast to load-bearing long bones where bone formation and maintenance of bone quality is facilitated by a homeostatic feedback mechanism, where low levels of stress (i.e., comparable to those experiences by cranial bones) would lead to disuse osteopenia (Turner, 1991; Rawlinson et al, 2009). This suggests marked dissimilarities between the regulatory mechanisms of bone homeostasis in long bones and in flat cranial bones (Hillam et al, 2015)
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