Deformation of the human brain induced by mild acceleration

Abstract

Rapid deformation of brain matter caused by skull acceleration is most likely the cause of concussion, as well as more severe traumatic brain injury (TBI). The inability to measure deformation directly has led to disagreement and confusion about the biomechanics of concussion and TBI. In the present study, brain deformation in human volunteers was measured directly during mild, but rapid, deceleration of the head (20-30 m/sec2 peak, approximately 40 msec duration), using an imaging technique originally developed to measure cardiac deformation. Magnetic resonance image sequences with imposed "tag" lines were obtained at high frame rates by repeating the deceleration and acquiring a subset of image data each repetition. Displacements of points on tag lines were used to estimate the Lagrangian strain tensor field. Qualitative (visual) and quantitative (strain) results illustrate clearly the deformation of brain matter due to occipital deceleration. Strains of 0.02-0.05 were typical during these events (0.05 strain corresponds roughly to a 5% change in the dimension of a local tissue element). Notably, compression in frontal regions and stretching in posterior regions were observed. The motion of the brain appears constrained by structures at the frontal base of the skull; it must pull away from such constraints before it can compress against the occipital bone. This mechanism is consistent with observations of contrecoup injury in occipital impact.

Figure 1

Photographs of the MR compatible device that constrains head motion and produces repeatable accelerations for measurement of intra-cranial strain. The head is in an elastic suspension that provides controlled deceleration of 20−30 m/s² (2−3G).

Figure 2

Schematic diagrams of head motion in the (a) sagittal and (b) axial plane. Arrows indicate the approximate trajectory of the mass center of the skull in each plane.

Figure 3

Acceleration profiles measured with an accelerometer strapped to the head, shown relative to the optical trigger signal (square wave) that synchronizes the MRI. Peak acceleration magnitudes are obtained shortly after the optical trigger, as the elastic suspension slows head motion. These four consecutive events are extremely similar, showing good evidence of repeatability of head acceleration. For the entire series of eleven impacts from which these four events are taken, peak accelerations (mean±std. dev.) were (i) 21.1±2.9 m/s². Calibration tests performed on other dates had peak accelerations of (ii) 25.7±2.7 m/s² (11 impacts), (iii) 26.9±2.9 m/s² (6 impacts), (iv) 32.5±3.2 m/s² (25 impacts). Acceleration data were not acquired during imaging, as the measurement system interfered with the MR signal.

Figure 4

(a) Sagittal image plane. (b) Initially-horizontal and (c) initially-vertical tag lines in the sagittal image obtained 78 ms after tagging, 5−10 ms after peak deceleration of the skull. Horizontal and vertical tag lines were applied immediately after triggering, before the head drops; the tag lines rotate and deform with the tissue. (d) Axial image plane. (e) Initially-horizontal and (f) initially-vertical tag lines in the axial image obtained 5−10 ms after peak deceleration. The arrow in panel (d) indicates the postulated region of tethering described in the text. Black bars next to panels (b) and (e) show the location of contact with the elastic support at the back of the head. Tag lines are initially perfectly straight and either horizontal and vertical in the image plane.

Figure 5

(a) Reference (0 ms after tagging) and (b) deformed (78 ms post-tagging) phase contours (deformation 5× actual) from pairs of tagged sagittal MR images. (c) Maximum principal Lagrangian strain field, ε₁, for the deformed sagittal image. (d) Reference and (e) deformed phase contours from pairs of tagged axial images. (f) Maximum principal Lagrangian strain, ε₁, field for the deformed axial image. The value ε₁ describes the maximum elongation of an element, relative to its original length, when the element is oriented so it experiences only elongation and shortening. In principal strain figures, the length of each line reflects the magnitude of ε₁; the direction of each line shows the orientation of principal strain.

Figure 6

Sagittal and axial Lagrangian strain tensor fields at several time points after tagging at 0 ms. Peak deceleration occurred at 70−75 ms. Note anterior shortening and posterior elongation in both planes, hypothesized to be due to frontal tethering of the brain. The black bars in the upper left images show the location of contact with the elastic support at the back of the head.

Figure 7

Fraction of the area of the strain field in which the maximum principal Lagrangian strain, ε₁, exceeds a given value λ. (a) Sagittal area fraction vs λ for various times after tagging. (b) Sagittal area fraction vs time for several strain levels. (c) Axial area fraction vs λ for various times. (d) Axial area fraction vs time for several strain levels. Note that data are not available between 18 ms and 78 ms; strain was not computed during the fast free-fall phase of head motion because of tag line blurring.