Group characterization of impact-induced, in vivo human brain kinematics

Abstract

Brain movement during an impact can elicit a traumatic brain injury, but tissue kinematics vary from person to person and knowledge regarding this variability is limited. This study examines spatio-temporal brain-skull displacement and brain tissue deformation across groups of subjects during a mild impact in vivo. The heads of two groups of participants were imaged while subjected to a mild (less than 350 rad s-2) impact during neck extension (NE, n = 10) and neck rotation (NR, n = 9). A kinematic atlas of displacement and strain fields averaged across all participants was constructed and compared against individual participant data. The atlas-derived mean displacement magnitude was 0.26 ± 0.13 mm for NE and 0.40 ± 0.26 mm for NR, which is comparable to the displacement magnitudes from individual participants. The strain tensor from the atlas displacement field exhibited maximum shear strain (MSS) of 0.011 ± 0.006 for NE and 0.017 ± 0.009 for NR and was lower than the individual MSS averaged across participants. The atlas illustrates common patterns, containing some blurring but visible relationships between anatomy and kinematics. Conversely, the direction of the impact, brain size, and fluid motion appear to underlie kinematic variability. These findings demonstrate the biomechanical roles of key anatomical features and illustrate common features of brain response for model evaluation.

Trial registration: ClinicalTrials.gov NCT01633268.

Keywords: dynamic magnetic resonance imaging; finite strain; head impact; traumatic brain injury.

Figures

Figure 1.

Extraction of kinematic data in a single participant. MRI data were acquired during two types of motion, NE and NR (direction of motion prior to impact is shown with arrows). Processing via HARP-FE included filtering phase images, which include directional ‘tags’ that move with the tissue, and fitting an FE model. The result of tissue tracking included displacements relative to the skull and a strain field. A, anterior; P, posterior; R, right; L, left; I, inferior; S, superior. Strain expressed as the maximum principal strain, displacement expressed in millimetres.

Figure 2.

Datasets for group (atlas) analysis. The tissue motion estimation via HARP-FE registers the same FE model using CSF labels across all the participants. As a result, the data (anatomical T1 data and kinematic results) are pre-emptively co-registered. Atlas generation is hence focused on temporal and inertial alignment of the multidimensional data.

Figure 3.

Superimposed plots of individual results in the database. Rotational accelerations approximate the magnitude of head rotation. Displacement and strain (expressed as the MSS) correspond to the mean across the brain volume. Variability is more visible in the vertical direction, but some temporal misalignment was highlighted by the arrows. The dotted line indicates the time frame immediately after peak acceleration (impact).

Figure 4.

Results of T1-weighted intensity averaging. The average (left column) contains structures that can be seen in the representative participant (right column). Some blurring due to anatomical variability appears in the cortical grey matter.

Figure 5.

Inertial factor compared to skull–brain displacement and strain. Each participant includes a value for inertial factor (volume times peak acceleration) and the 95th percentile skull–brain displacement magnitude (top) and strain (bottom) across its corresponding brain. In both the NE group (dots) and NR (squares), the line shows a simple linear regression through the origin (which lies outside the axes shown).

Figure 6.

Atlas quantities compared to individual quantities. The lines show the spatial mean of the displacement magnitude ||U|| and strain metric γmax. Both include error bars that correspond to the inter-subject variability (as the standard error of the mean). The strain results (lower row) include the strain metric extracted from the atlas displacements (solid line), and as a group average (dotted line). The area represents the inter-subject spread in relative displacement magnitude and strain values (figure 3). NE, neck extension; NR, neck rotation.

Figure 7.

3D visualization of the impact-induced skull–brain displacements in a representative participant and the atlas. Two types of motion, NE and NR, are illustrated (direction of motion prior to impact is shown with arrows). A, anterior; P, posterior; R, right; L, left; I, inferior; S, superior. T1-intensity values appear in arbitrary units (arb. units).

Figure 8.

Average magnitude of skull–brain displacements. The colour map shows group average of skull–brain displacements from the NE and NR experiments. The NE and NR results appear side to side. The slices are organized from top to bottom as follows: (a) coronal anterior to posterior, (b) sagittal left to right, and (c) axial superior to inferior. T1-weighted images are provided for reference. Slice orientation follows neurological convention.

Figure 9.

Close-up of displacement magnitude (coronal). The displacement magnitude map, overlaid with the T1-weighted image in a posterior coronal view, was evaluated at six locations: at the longitudinal fissure (a), near the superior white matter (b,c), near the intersection between the falx and the tentorium (d), and near the transverse fissure. In the plot below each image the error bars show the values of inter-subject variability in displacement ||δU|| at each of the points. NE, neck extension; NR, neck rotation.

Figure 10.

Average through-plane displacements. The colour maps represent the displacement component of the group average in the direction normal to the view plane U ·n. The groups included NE and NR. The organization of the slices is explained in figure 8.

Figure 11.

Average brain deformation. The group average MSS values from the NE and NR experiments were projected to the mesh centroid. The organization of the slices is explained in figure 8.

Figure 12.

Close-up of brain deformation magnitude (coronal view). The MSS maps appear overlaid with the T1-weighted images. The locations of the points in which the strain results were evaluated are explained in figure 9. Error bars show the values of inter-subject variability in MSS [δY]max at each of the points. NE, neck extension; NR, neck rotation.