As a mechano-biological interface, the meninges dissipate external forces, maintain neuroimmune homeostasis, and dynamically regulate the brain’s microenvironment. A comprehensive study of the regional heterogeneities in meninges can improve predictions of extra-axial hemorrhage and enhance bio-fidelity of finite element (FE) modeling of head trauma under multiple injury scenarios and pathological conditions. Here, we characterized the mechanical properties of porcine leptomeninges by performing rheological shear modeling and atomic force microscopy indentation experiments. Anatomical areas encompassed the piriform, occipital, frontal, parietal, and temporal lobes, along with the cerebellum lobe. Both macromechanical and micromechanical properties indicate that the modulus of the cerebellar lobe region is much higher than that of other lobes of the pia mater. Meanwhile, the regions of the leptomeninges also displayed local mechanical anisotropy. Regional variations in the mechanical properties were further characterized by analyzing the spatial distribution in protein compositions (collagen and elastin) through 2-photon microscopy and RNA sequencing. The cerebellum lobe was found to exhibit markedly elevated levels of collagen, elastin, and cell junction proteins. Additionally, the cerebellum lobe was also identified to have markedly greater thickness compared to other lobes. Taken together, the results revealed the intricate biomechanical architecture of the leptomeninges and underscore the need to analyze its heterogeneities when modeling FE models or other computational models during traumatic brain injury.
