Statistical Characterization of Human Brain Deformation During Mild Angular Acceleration Measured In Vivo by Tagged Magnetic Resonance Imaging

Abstract

Understanding of in vivo brain biomechanical behavior is critical in the study of traumatic brain injury (TBI) mechanisms and prevention. Using tagged magnetic resonance imaging, we measured spatiotemporal brain deformations in 34 healthy human volunteers under mild angular accelerations of the head. Two-dimensional (2D) Lagrangian strains were examined throughout the brain in each subject. Strain metrics peaked shortly after contact with a padded stop, corresponding to the inertial response of the brain after head deceleration. Maximum shear strain of at least 3% was experienced at peak deformation by an area fraction (median±standard error) of 23.5±1.8% of cortical gray matter, 15.9±1.4% of white matter, and 4.0±1.5% of deep gray matter. Cortical gray matter strains were greater in the temporal cortex on the side of the initial contact with the padded stop and also in the contralateral temporal, frontal, and parietal cortex. These tissue-level deformations from a population of healthy volunteers provide the first in vivo measurements of full-volume brain deformation in response to known kinematics. Although strains differed in different tissue type and cortical lobes, no significant differences between male and female head accelerations or strain metrics were found. These cumulative results highlight important kinematic features of the brain's mechanical response and can be used to facilitate the evaluation of computational simulations of TBI.

Figures

Fig. 1

Head support device showing right to left rotation direction (arrow) for tagged image acquisitions during mild head acceleration. The head support pivots about a superior (S) to inferior (I) axis (dotted line), so that subjects' heads were rotated toward their left shoulder. Axial tagged image planes of 8 mm thickness were acquired 10 mm apart (center-to-center) as indicated on the T1-weighted image of a representative subject to provide adequate volume coverage of brain tissues. Tag lines, which are applied immediately after the volunteer initiates the rotation, were aligned at 30 deg from the anterior (A) to posterior (P) and left (L) to right (R) axes to provide sensitivity to in-plane motion in the x and y directions after the approximately 30 deg rotation [30].

Fig. 2

Position, velocity, and acceleration (mean±95% CI) of the head cradle were recorded during mild angular accelerations of the head for the representative subject (left column). The average kinematics traces (n = 33) were then aggregated across subjects for which positions were measured (middle and right columns). Tagged MRI acquisition (light gray background) was triggered prior to contact of the head cradle to the rubber stop and spanned up to 13 frames of 18.06 ms each.

Fig. 3

Anatomic images and strain maps are shown for a representative subject. (a) Registered anatomy from the T1-weighted (T1w) MPRAGE image and whole brain segmentation (Seg) permitted the identification and grouping of brain tissues of interest (cortical gray matter (CGM), white matter (WM), and deep gray matter (DGM)). The maximum values for in-plane principal strain (E1, E2) and maximum shear strain (γmax) experienced by each voxel through all frames were determined and mapped to the segmented anatomy. Because E1 and E2 were primarily tensile and compressive, respectively, −[E2] is shown to permit visualization with E1 and γmax on the same color scale. γmax maps are shown as a function of time. (b) Area fractions of peak E1, E2, and γmax and area fraction of γmax by frame were computed for a threshold of 3% absolute strain in the whole brain and tissue types of interest. Corresponding with the greater proportion of areas of higher strain within the strain maps, strain area fractions peaked at frame 3 (54 ms) and were greatest in the cortical gray matter, followed by the white matter and deep gray matter.

Fig. 4

Area fractions (n = 34, median±standard error) of in-plane principal strains (Ε1, Ε2) and maximum shear strain (γmax) were calculated at a 3% threshold for peak strains (Max) and on a by-frame basis in all brain tissues, cortical gray matter, cerebral white matter, and deep gray matter. The effect of tissue type on Ε1, Ε2, and γmax area fractions was significant (all p < 0.0001), with metrics greatest within the cortical gray matter for all frames and peak strains (not indicated on graphs). The area fractions of white matter and deep gray matter were significantly different in peak strains (§, all p < 0.02) and in some frames associated with the initial impact (#, p < 0.005). These strain metrics are consistent with axes of rotation that lay within the brain during angular acceleration, with the highest strains furthest from the axis of rotation.

Fig. 5

Area fractions of peak and by-frame maximum shear strain (γmax) in the cortical lobes were calculated at a 3% threshold for all subjects (n = 34). The representative and group median (+ standard error of the mean (SEM)) values plotted on a polar plot with octants representing the frontal (F), temporal (T), parietal (P), and occipital (O) lobes of left and right hemispheres.

Fig. 6

Area fractions of peak strains in female and male groups were compared across tissue type and cortical lobes. Males tended to show higher strain metrics in all tissue types, although these differences were not statistically significant. Female subjects tended toward higher strain area fractions in the occipital cortex, while male subjects showed higher strains in the parietal cortex.