The Relationship of Three-Dimensional Human Skull Motion to Brain Tissue Deformation in Magnetic Resonance Elastography Studies

Abstract

In traumatic brain injury (TBI), membranes such as the dura mater, arachnoid mater, and pia mater play a vital role in transmitting motion from the skull to brain tissue. Magnetic resonance elastography (MRE) is an imaging technique developed for noninvasive estimation of soft tissue material parameters. In MRE, dynamic deformation of brain tissue is induced by skull vibrations during magnetic resonance imaging (MRI); however, skull motion and its mode of transmission to the brain remain largely uncharacterized. In this study, displacements of points in the skull, reconstructed using data from an array of MRI-safe accelerometers, were compared to displacements of neighboring material points in brain tissue, estimated from MRE measurements. Comparison of the relative amplitudes, directions, and temporal phases of harmonic motion in the skulls and brains of six human subjects shows that the skull-brain interface significantly attenuates and delays transmission of motion from skull to brain. In contrast, in a cylindrical gelatin "phantom," displacements of the rigid case (reconstructed from accelerometer data) were transmitted to the gelatin inside (estimated from MRE data) with little attenuation or phase lag. This quantitative characterization of the skull-brain interface will be valuable in the parameterization and validation of computer models of TBI.

In vivo characterization of 3D skull and brain motion during dynamic head vibration using magnetic resonance elastography

“…Typically 2 sets of MEGs with the same amplitude but opposite polarity are used to acquire positive and negative phase images , and phase difference images are calculated to remove any unwanted background phase and double the motion SNR, which could lead to significant temporal and spatial phase wrapping. A separate MRE scan can be performed using a low MEG amplitude to achieve wrap‐free phase that can be used to check the phase unwrapping, however, this doubles the scan time. Here, we propose a dual‐sensitivity motion encoding scheme (as seen in Figure ), in which the amplitudes of the positive and negative MEGs are slightly different.…”

“…MRE displacements from the brain and skull ROIs were fitted to a model of rigid‐body motion to obtain rigid‐body translation ( , , and ) and rotation ( , , and ) . The rigid‐body fitting origin was defined as the center of mass of the brain for each volunteer.…”

“…The harmonic vibrations in MRE with multiple phase offsets resulted in a set of complex translational and rotational coefficients. Several quantities were calculated to compare the skull and brain motion among 6 volunteers, including (1) the amplitude of translational and rotational motion of the skull and brain in the x‐, y‐, and z‐directions respectively; (2) the ratios of brain to skull in the amplitude of translational and rotational motion in the x‐, y‐, and z‐directions; (3) the 3D trajectory of translational motion of the skull and brain as well as their spatial angle (α); (4) the temporal phase delay between the skull and brain translational motion, which was calculated as the weighted average over the x‐, y‐, and z‐ translational phase delays weighted by the amplitude of each translational component; and (5) the temporal phase delay between the skull and brain rotational motion calculated the same as the weighted average over the x‐, y‐, and z‐ rotational phase delays. In this study, x‐, y‐, and z‐directions denote left‐to‐right (LR), anterior‐to‐posterior (AP), and superior‐to‐inferior (SI) directions, respectively.…”

“…It is therefore reasonable to assume that characterization of the skull motion independent of the brain motion using MRE can provide an understanding of the skull–brain coupling resulting from the substructures between the skull and brain interface. Recent studies have used MRE combined with accelerometers or pressure sensors to investigate the motion transmission and attenuation through the skull to the brain . These studies provide indirect insight into in vivo brain motion relative to the skull.…”

Measurement and Finite Element Model Validation of Immature Porcine Brain–Skull Displacement during Rapid Sagittal Head Rotations

“…Together, the arachnoid and pia mater constitute the leptomeninges, or pia–arachnoid complex (PAC), consisting of cerebrospinal fluid (CSF), vasculature, arachnoid trabeculae, and the membranes themselves. Various techniques have been used to investigate the motion of the brain in response to the roughly rigid body motion of the skull including high-speed videography and replacement of a portion of the skull with a lucite calvarium (Pudenz and Shelden, 1946 ), flash X-ray cinematography (Hodgson et al, 1966 ; Gurdjian et al, 1968 ; Shatsky, 1973 ; Shatsky et al, 1974 ; Stalnaker et al, 1977 ), high-speed biplane X-ray and neutral density targets (Hardy et al, 2001 , 2007 ; Zou et al, 2007 ), tagged magnetic resonance imaging (Bayly et al, 2005 ; Sabet et al, 2008 ; Feng et al, 2010 ), and most recently, magnetic resonance elastography (Badachhape et al, 2017 ) and three-dimensional digital sonomicrometry (Alshareef et al, 2017 ). Furthermore, finite element models have employed differing brain–skull boundary condition representations, including rigid attachment between the brain and skull, frictionless sliding, frictional contact, a layer(s) of fluid elements, a layer(s) of solid elements, or linear elastic connector elements between the outer brain and inner skull surfaces (Zhang et al, 2001 , 2002 ; Kleiven and Hardy, 2002 ; Wittek and Omori, 2003 ; Cloots et al, 2008 ; Takhounts et al, 2008 ; Couper and Albermani, 2010 ; Coats et al, 2012 ; McAllister et al, 2012 ).…”