Spatial distribution of human arachnoid trabeculae

Abstract

Traumatic brain injury (TBI) is a common injury modality affecting a diverse patient population. Axonal injury occurs when the brain experiences excessive deformation as a result of head impact. Previous studies have shown that the arachnoid trabeculae (AT) in the subarachnoid space significantly influence the magnitude and distribution of brain deformation during impact. However, the quantity and spatial distribution of cranial AT in humans is unknown. Quantification of these microstructural features will improve understanding of force transfer during TBI, and may be a valuable dataset for microneurosurgical procedures. In this study, we quantify the spatial distribution of cranial AT in seven post-mortem human subjects. Optical coherence tomography (OCT) was used to conduct in situ imaging of AT microstructure across the surface of the human brain. OCT images were segmented to quantify the relative amounts of trabecular structures through a volume fraction (VF) measurement. The average VF for each brain ranged from 22.0% to 29.2%. Across all brains, there was a positive spatial correlation, with VF significantly greater by 12% near the superior aspect of the brain (p < .005), and significantly greater by 5%-10% in the frontal lobes (p < .005). These findings suggest that the distribution of AT between the brain and skull is heterogeneous, region-dependent, and likely contributes to brain deformation patterns. This study is the first to image and quantify human AT across the cerebrum and identify region-dependencies. Incorporation of this spatial heterogeneity may improve the accuracy of computational models of human TBI and enhance understanding of brain dynamics.

Keywords: cadaver; imaging; optical coherence tomography; pia-arachnoid complex; traumatic brain injury.

Figure 1

(A) Post‐mortem human subject heads were placed in a stereotactic frame. (B) The optical coherence tomography (OCT) lens and saline injection system were positioned such that saline injection occurred immediately adjacent to the imaged sulcus

Figure 2

Example three‐dimensional volume of human pia‐arachnoid complex obtained from optical coherence tomography (OCT). OCT Settings were 800 A‐scans per B‐scan, 400 B‐scans per C‐scan, and one C‐scan. This resulted in a voxel resolution of 6.25 µm (x) × 1.61 µm (y) × 12.5 µm (z)

Figure 3

Representative scan locations (black boxes) for pia‐arachnoid complex imaging

Figure 4

(A) Filtered two‐dimensional optical coherence tomography image of Subject 1. (B) Selected region of interest. (C) Segmented arachnoid trabeculae in the region of interest. Volume fraction was calculated by dividing the segmented arachnoid trabeculae pixels (red) by the region of interest (blue)

Figure 5

(A) Volume fraction (VF) data for each subject. Subjects 3 and 5 had significantly greater VF than the remaining subjects (p < .001). (B) Hemisphere VF data were not significantly different. (C) VF was significantly greater in superior regions and (D) frontal regions of the brain (** = p < .05 for paired analysis). Error bars denote standard deviations

Figure 6

Volume fraction (VF) distribution maps across the seven brains. Each region represents the average VF of a single scan location

Figure 7

Combined volume fraction (VF) distribution map for all seven brains. Average VF of a single scan location for each brain was normalized by the mean VF of each brain.

Figure 8

(A) Weight functions for statistical spatial correlations are exponential at low r_c and become linear with larger values of r_c. (B) Spatial statistics become statistically significant at r_c ≥ 20 mm. (C) Moran's I and (D) Geary's C become less positively correlated at larger values of r_c. This indicates the existence of local clustering in arachnoid trabeculae densities

Figure 9

(A) In situ optical coherence tomography imaging of the human pia‐arachnoid complex from our study shows equal or better resolution of subarachnoid structures when compared to (B) intra‐operative in vivo imaging. Image (B) modified from Hartman et al. 2019. Reprinted by permission of Sage Publications, Ltd