Ruth J. Okamoto

Strain energy and kinetic energy in the human brain were estimated by magnetic resonance elastography (MRE) during harmonic excitation of the head, and compared to characterize the effect of loading direction and frequency on brain deformation. In brain MRE, shear waves are induced by external vibration of the skull and imaged by a modified MR imaging sequence; the resulting harmonic displacement fields are typically “inverted” to estimate mechanical properties, like stiffness or damping. However, measurements of tissue motion from MRE also illuminate key features of the response of the brain to skull loading. In this study, harmonic excitation was applied in two different directions and at five different frequencies from 20 to 90 Hz. Lateral loading induced primarily left-right head motion and rotation in the axial plane; occipital loading induced anterior-posterior head motion and rotation in the sagittal plane. The ratio of strain energy to kinetic energy (SE/KE) depended strongly on both direction and frequency. The ratio of SE/KE was approximately four times larger for lateral excitation than for occipital excitation and was largest at the lowest excitation frequencies studied. These results are consistent with clinical observations that suggest lateral impacts are more likely to cause injury than occipital or frontal impacts, and also with observations that the brain has low-frequency (∼10 Hz) natural modes of oscillation. The SE/KE ratio from brain MRE is potentially a simple and powerful dimensionless metric of brain vulnerability to deformation and injury.

Noninvasive measurements of brain deformation in human participants in vivo are needed to develop models of brain biomechanics and understand traumatic brain injury (TBI). Tagged magnetic resonance imaging (tagged MRI) and magnetic resonance elastography (MRE) are two techniques to study human brain deformation; these techniques differ in the type of motion and difficulty of implementation. In this study, oscillatory strain fields in the human brain caused by impulsive head acceleration and measured by tagged MRI were compared quantitatively to strain fields measured by MRE during harmonic head motion at 10 and 50 Hz. Strain fields were compared by registering to a common anatomical template, then computing correlations between the registered strain fields. Correlations were computed between tagged MRI strain fields in six participants and MRE strain fields at 10 Hz and 50 Hz in six different participants. Correlations among strain fields within the same experiment type were compared statistically to correlations from different experiment types. Strain fields from harmonic head motion at 10 Hz imaged by MRE were qualitatively and quantitatively similar to modes excited by impulsive head motion, imaged by tagged MRI. Notably, correlations between strain fields from 10 Hz MRE and tagged MRI did not differ significantly from correlations between strain fields from tagged MRI. These results suggest that low-frequency modes of oscillation dominate the response of the brain during impact. Thus, low-frequency MRE, which is simpler and more widely available than tagged MRI, can be used to illuminate the brain's response to head impact.

It is important to understand mechanical anisotropy in fibrous soft tissues because of the relationship of anisotropy to tissue function, and because anisotropy may change due to injury and disease. We have developed a method to noninvasively investigate anisotropy, based on MR imaging of harmonic ultrasound-induced motion (MR-HUM), using focused ultrasound (FUS) and magnetic resonance elastography (MRE). MR-HUM produces symmetric, radial waves inside a tissue, which enables a simple assessment of anisotropy using features of the resulting shear wave fields. This method was applied to characterize ex vivo muscle tissue, which is known to exhibit mechanical anisotropy. Finite element (FE) simulations of the experiment were performed to illustrate and validate the approach. Anisotropy was characterized by ratios of apparent shear moduli and strain components in different directions.

Measurements of dynamic deformation of the human brain, induced by external harmonic vibration of the skull, were analyzed to illuminate the mechanics of mild traumatic brain injury (TBI). Shear wave propagation velocity vector fields were obtained to illustrate the role of the skull and stiff internal membranes in transmitting motion to the brain. Relative motion between the cerebrum and cerebellum was quantified to assess the vulnerability of connecting structures. Mechanical deformation was quantified throughout the brain to investigate spatial patterns of strain and axonal stretch. Strain magnitude was generally attenuated as shear waves propagated into interior structures of the brain; this attenuation was greater at higher frequencies. Analysis of shear wave propagation direction indicates that the stiff membranes (falx and tentorium) greatly affect brain deformation during imposed skull motion as they serve as sites for both initiation and reflection of shear waves. Relative motion between the cerebellum and cerebrum was small in comparison with the overall motion of both structures, which suggests that such relative motion might play only a minor role in TBI mechanics. Strain magnitudes and the amount of axonal stretch near the bases of sulci were similar to those in other areas of the cortex, and local strain concentrations at the gray-white matter boundary were not observed. We tentatively conclude that observed differences in neuropathological response in these areas might be due to heterogeneity in the response to mechanical deformation rather than heterogeneity of the deformation itself.