The Presence of the Temporal Horn Exacerbates the Vulnerability of Hippocampus During Head Impacts

Abstract

Hippocampal injury is common in traumatic brain injury (TBI) patients, but the underlying pathogenesis remains elusive. In this study, we hypothesize that the presence of the adjacent fluid-containing temporal horn exacerbates the biomechanical vulnerability of the hippocampus. Two finite element models of the human head were used to investigate this hypothesis, one with and one without the temporal horn, and both including a detailed hippocampal subfield delineation. A fluid-structure interaction coupling approach was used to simulate the brain-ventricle interface, in which the intraventricular cerebrospinal fluid was represented by an arbitrary Lagrangian-Eulerian multi-material formation to account for its fluid behavior. By comparing the response of these two models under identical loadings, the model that included the temporal horn predicted increased magnitudes of strain and strain rate in the hippocampus with respect to its counterpart without the temporal horn. This specifically affected cornu ammonis (CA) 1 (CA1), CA2/3, hippocampal tail, subiculum, and the adjacent amygdala and ventral diencephalon. These computational results suggest that the presence of the temporal horn exacerbate the vulnerability of the hippocampus, highlighting the mechanobiological dependency of the hippocampus on the temporal horn.

Keywords: brain-ventricle interface; finite element analysis; fluid-structure interaction; hippocampal injury; temporal horn; traumatic brain injury.

FIGURE 1

Finite element models of the human head with and without the temporal horn. (A) Head model with the skull open to expose the subarachnoid CSF and brain. A skull-fixed coordinate system and corresponding axes are illustrated with the origin at the center of gravity of the head. (B) Brain model with fine mesh. (C) Ventricles (i.e., lateral ventricles without the temporal horn, and third ventricle) in the NTH-model. (D) Ventricles (i.e., lateral ventricles with the temporal horn, and third ventricle) in the TH-model and hippocampus. (E) Isometric view of deep brain structures, cerebral ventricles, falx, and dura mater (in translucency) in the TH-Model. (F) Left and right hippocampal formations with subfields. CSF: cerebrospinal fluid; Ventral DC: ventral diencephalon; CA: cornu ammonis; DG: dentate gyrus; HP Tail: hippocampal tail.

FIGURE 2

Brain-ventricle interfaces of the TH-Model (A) and NTH-Model (B). For each model, an isometric view of the brain model, the cerebral ventricle, and void mesh are shown on the left. Coronal sections at the planes indicated in the left subfigures are shown on the right. For better illustration, only half of the brain is visible. The cerebral ventricles are shown as blue shaded elements and the void mesh as wireframe elements. ALE: arbitrary Lagrangian-Eulerian.

FIGURE 3

Comparison of the maximum principal strain (A,B) and strain rate (C,D) distribution between the TH-model and NTH-model for three concussive and three sub-concussive impacts (Cases 1–3 and 4–6 respectively). The temporal horn and adjacent tissue are highlighted by black dashed ellipses.

FIGURE 4

Comparison of strain distribution (A,B) and strain rate distribution (C,D) in the hippocampi between the TH-model and NTH-model of three concussive impacts (Cases 1–3) and three sub-concussive impacts (Cases 4–6). Subfigure (E) illustrates the hippocampal subfields. CA: cornu ammonis; DG: dentate gyrus; HP Tail: hippocampal tail.

FIGURE 5

Comparison of the 95th percentile maximum principle strain and strain rate in the hippocampal subfields and the whole hippocampus between the TH-Model and NTH-model of three concussive impacts (Cases 1–3) and three sub-concussive impacts (Cases 4–6). (A) Comparison of strain in the hippocampal subfields of three concussive impacts. (B) Comparison of strain in the hippocampal subfields of three sub-concussive impacts. (C) Comparison of strain rate in the hippocampal subfields of three concussive impacts. (D) Comparison of strain rate in the hippocampal subfields of three sub-concussive impacts. Percentages in strain difference and strain rate difference are calculated with the results of the NTH-Model as the baseline. CA: cornu ammonis; DG: dentate gyrus; HP Tail: hippocampal tail.

FIGURE 6

Maximum shear stresses in the hippocampus (A) and temporal horn/its substitute (B) predicted by the TH-Model and NTH-Model in six cases; (C) Contours of maximum shear stress in the CSF within the temporal horn in the TH-Model and its substitute in the NTH-Model; (D) Contours of maximum shear stress endured by the hippocampi in the TH-Model and NTH-Model. Note that, in the NTH-Model, the temporal horn is modeled as brain, not fluid.