The biomechanical signature of loss of consciousness: computational modelling of elite athlete head injuries

Abstract

Sports related head injuries can cause transient neurological events including loss of consciousness and dystonic posturing. However, it is unknown why head impacts that appear similar produce distinct neurological effects. The biomechanical effect of impacts can be estimated using computational models of strain within the brain. Here, we investigate the strain and strain rates produced by professional American football impacts that led to loss of consciousness, posturing or no neurological signs. We reviewed 1280 National Football League American football games and selected cases where the team's medical personnel made a diagnosis of concussion. Videos were then analysed for signs of neurological events. We identified 20 head impacts that showed clear video signs of loss of consciousness and 21 showing clear abnormal posturing. Forty-one control impacts were selected where there was no observable evidence of neurological signs, resulting in 82 videos of impacts for analysis. Video analysis was used to guide physical reconstructions of these impacts, allowing us to estimate the impact kinematics. These were then used as input to a detailed 3D high-fidelity finite element model of brain injury biomechanics to estimate strain and strain rate within the brain. We tested the hypotheses that impacts producing loss of consciousness would be associated with the highest biomechanical forces, that loss of consciousness would be associated with high forces in brainstem nuclei involved in arousal and that dystonic posturing would be associated with high forces in motor regions. Impacts leading to loss of consciousness compared to controls produced higher head acceleration (linear acceleration; 81.5 g ± 39.8 versus 47.9 ± 21.4; P = 0.004, rotational acceleration; 5.9 krad/s2 ± 2.4 versus 3.5 ± 1.6; P < 0.001) and in voxel-wise analysis produced larger brain deformation in many brain regions, including parts of the brainstem and cerebellum. Dystonic posturing was also associated with higher deformation compared to controls, with brain deformation observed in cortical regions that included the motor cortex. Loss of consciousness was specifically associated with higher strain rates in brainstem regions implicated in maintenance of consciousness, including following correction for the overall severity of impact. These included brainstem nuclei including the locus coeruleus, dorsal raphé and parabrachial complex. The results show that in head impacts producing loss of consciousness, brain deformation is disproportionately seen in brainstem regions containing nuclei involved in arousal, suggesting that head impacts produce loss of consciousness through a biomechanical effect on key brainstem nuclei involved in the maintenance of consciousness.

Keywords: TBI; biomechanics; concussion; loss of consciousness; sports tbi.

Figure 1

Methods and workflow. Videos of professional American football games were analysed to select cases of (A) players who lost consciousness, experienced dystonic posturing or did not show any visible signs of injury but were later diagnosed with a concussion by a team’s medical professional. (B) Impacts were analysed using Kinovea and (C) were physically reconstructed in a lab to estimate the accelerations of the head during the impact. (D) Information on head acceleration was then used as input for finite element modelling of the biomechanics of the injury, producing metrics such as strain and strain rate. (E) Biomechanical metrics were then analysed using neuroimaging techniques such as voxel-wise analyses, and (F) region of interest analysis was performed to test specific hypotheses.

Figure 2

Case studies of injuries with different clinical features. Case studies of (A) LOC; (B) posturing; and (C) no neurological signs (control). The left panel shows head impact kinematics (linear and rotational acceleration). The middle panel shows the 90th percentile strain in brain regions of interest (individual = dot, box plots show median and IQR of all other impacts with whiskers indicating 1.5 times IQR). The right panel shows whole brain analysis of Green–Lagrange strain. BS = brainstem; CC = corpus callosum; CST = corticospinal tract; LUL = left upper limb; RUL = right upper limb; SMA = supplementary motor area; Th = thalamus; Th R = thalamic radiation.

Figure 3

Kinematics and biomechanics of impacts. (A) Plots of rotational and linear acceleration and velocity; (B) Strain and strain rates for impacts leading to LOC (left), posturing (middle) or no visible signs (control, right). Format of box plots as in Fig. 2. Horizontal bars and asterisks highlight where groups are significantly different after post hoc testing (P < 0.05).

Figure 4

Spatial distribution of strain, strain rate across head injury subtypes. (A) The mean of maximum strain and (B) mean of maximum strain rate (s-1) across (i) LOC cases; (ii) posturing group; and (iii) control cases calculated for each voxel. y coordinates provided in MNI space.

Figure 5

Areas of the brain with strain and strain rate differences across head injury subtypes. Voxel-wise analysis of strain and strain rates. (A) Areas of significantly higher maximum strain in (i) LOC compared to control group impacts; and (ii) posturing group compared to control group impacts. (B) Areas of significantly higher maximum strain in (i) LOC compared to control group impacts; (ii) posturing group compared to control group impacts; and (iii) LOC compared to posturing. Areas coloured are thresholded to indicate voxels which are significantly different between groups (TFCE corrected P < 0.05) across the brain. x, y and z coordinates provided in MNI space.

Figure 6

Strain rates associated with loss of consciousness controlling for overall biomechanical severity. Voxel-wise analysis including 90th percentile as a covariate. (A) Areas of increased strain rate for LOC compared control impacts; (B) Areas of increased strain rate for LOC compared to posturing impacts; (C) Overlay of increased strain rate for LOC versus posturing and control impacts. x, y and z coordinates provided in MNI space. Thresholding as in Fig. 5.

Figure 7

Overlap of strain rate differences with lesions associated with coma and LOC. (A) Areas of the brainstem with disproportionately higher strain rates in impacts with LOC compared with posturing impacts, compared with (B) lesions in the brainstem significantly associated with LOC (P < 0.05) from prior work and (C) lesions significantly associated with brain-stem coma (z > 3.54) from prior work. (D) Overlap between strain rate results (in A) with lesion maps from B (in blue) and C (in red). Yellow areas indicate overlap between all three maps. z coordinates are provided in MNI space.

Figure 8

Proposed mechanism for traumatic loss of consciousness. High strain rates within the dorsal brainstem affect key arousal nuclei associated with arousal: the parabrachial complex, locus coeruleus and dorsal raphé. Axonal membrane disturbance temporarily impairs action potential firing, leading to transient reductions in noragenergic, dompaminergic, serotonergic and gulatamatergic projections (red-blue) to the cortex and subsequent LOC.