Department of Mechanical Engineering, Binghamton University, Binghamton, NY, 13902, USA.
Brain Decoding Research Center and School of Automation, Northwestern Polytechnical University, Xi'an, 710072, Shaanxi, China.
Sci Rep. 2023 Aug 14;13(1):13177. doi: 10.1038/s41598-023-40086-9.
The important mechanical parameters and their hierarchy in the growth and folding of the human brain have not been thoroughly understood. In this study, we developed a multiscale mechanical model to investigate how the interplay between initial geometrical undulations, differential tangential growth in the cortical plate, and axonal connectivity form and regulate the folding patterns of the human brain in a hierarchical order. To do so, different growth scenarios with bilayer spherical models that features initial undulations on the cortex and uniform or heterogeneous distribution of axonal fibers in the white matter were developed, statistically analyzed, and validated by the imaging observations. The results showed that the differential tangential growth is the inducer of cortical folding, and in a hierarchal order, high-amplitude initial undulations on the surface and axonal fibers in the substrate regulate the folding patterns and determine the location of gyri and sulci. The locations with dense axonal fibers after folding settle in gyri rather than sulci. The statistical results also indicated that there is a strong correlation between the location of positive (outward) and negative (inward) initial undulations and the locations of gyri and sulci after folding, respectively. In addition, the locations of 3-hinge gyral folds are strongly correlated with the initial positive undulations and locations of dense axonal fibers. As another finding, it was revealed that there is a correlation between the density of axonal fibers and local gyrification index, which has been observed in imaging studies but not yet fundamentally explained. This study is the first step in understanding the linkage between abnormal gyrification (surface morphology) and disruption in connectivity that has been observed in some brain disorders such as Autism Spectrum Disorder. Moreover, the findings of the study directly contribute to the concept of the regularity and variability of folding patterns in individual human brains.
人类大脑生长和折叠过程中的重要力学参数及其层次关系尚未被彻底理解。在本研究中，我们开发了一个多尺度力学模型，以研究初始几何起伏、皮质板的差异切向生长以及轴突连接的形成和调节之间的相互作用如何按层次顺序形成并调节人类大脑的折叠模式。为此，我们使用具有皮质初始起伏的双层球形模型开发了不同的生长场景，并对其进行了统计分析和成像观察验证。结果表明，差异切向生长是皮质折叠的诱导因素，并且在层次顺序上，表面上的高幅度初始起伏和白质中的轴突纤维的异质性分布调节折叠模式并决定脑回和脑沟的位置。折叠后密集轴突纤维的位置位于脑回而不是脑沟中。统计结果还表明，正向（外凸）和负向（内凹）初始起伏的位置与折叠后的脑回和脑沟的位置之间存在很强的相关性。此外，3 铰链脑回折叠的位置与初始正起伏和密集轴突纤维的位置强烈相关。另一个发现是，轴突纤维密度与局部脑回指数之间存在相关性，这在成像研究中已经观察到，但尚未得到根本解释。这项研究是理解异常脑回（表面形态）与某些脑疾病（如自闭症谱系障碍）中观察到的连接中断之间联系的第一步。此外，该研究的发现直接有助于理解个体人大脑折叠模式的规律性和可变性的概念。
